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Emergence and progression of ‘non-semantic’ deficits in semantic dementia
cortex 45 (2009) 483–494
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Research report
Emergence and progression of ‘non-semantic’ deficits in semantic dementia Diana Cainea,*, Nora Breenb and Karalyn Pattersonc a
University of Manchester, Manchester, UK Royal Prince Alfred Hospital, Sydney, Australia c MRC Cognition and Brain Sciences Unit, Cambridge, UK b
article info
abstract
Article history:
Although semantic dementia (SD) is defined as a selective disruption of conceptual know-
Received 4 December 2006
ledge, a number of group studies have now demonstrated that SD patients also show
Reviewed 18 May 2007
impaired performance on tasks not usually considered to have a high semantic load
Revised 18 June 2007
(e.g., reading words aloud and lexical or object decision). The aim of the current study
Accepted 2 July 2007
was to document the relative deterioration, over time, of a number of semantic and so-
Action editor Art Shiamura
called ‘non-semantic’ tasks in LF, a single case of SD for whom – by virtue of his work as
Published online 20 February 2008
a published cartoonist – we also have extensive data regarding his pre-morbid linguistic and drawing skills.
Keywords:
In five testing rounds over a period of five years we administered semantic tests of
Semantic dementia
object naming and object definition (on both of which LF was progressively impaired, as
Semantic impairment
expected for a diagnosis of SD), plus verbal and non-verbal ‘non-semantic’ tasks of reading
Acquired dysgraphia
aloud, spelling, object and lexical decision, and delayed copy drawing.
Surface dyslexia Delayed copy drawing
Initially, his only striking ‘non-semantic’ deficit was in the domain of spelling – a pronounced surface dysgraphia in an individual with demonstrably superior pre-morbid spelling skill. Over time, and in line with his declining semantic system, LF’s performance gradually deteriorated on all of the ‘non-semantic’ tasks. The most vulnerable items on most tasks were those with low frequency and an atypical form. This report adds to the growing body of evidence that a number of cognitive processes not usually considered to be ‘semantic’ in their demands rely on the integrity of semantic knowledge for successful execution. Furthermore, it provides the first indication that these non-semantic deficits might emerge in an order predictable from the typicality structure of the relevant domain. Crown Copyright ª 2008 Published by Elsevier Srl. All rights reserved.
Semantic dementia (SD) is a progressive neurodegenerative disorder defined by its pathognomonic feature, a selective disruption to conceptual knowledge. Notwithstanding the highly focal nature of the disease, if tested appropriately SD patients
are also typically impaired on cognitive processes usually thought to be executed independently of semantics. Here we present the longitudinal investigation of patient LF, whose published cartoons over 30 years were abundant evidence of
* Corresponding author. School of Psychological Sciences (NARU), Zochonis Building, University of Manchester, Oxford Road, Manchester M13 9PL, UK. E-mail address: [email protected] (D. Caine). 0010-9452/$ – see front matter Crown Copyright ª 2008 Published by Elsevier Srl. All rights reserved. doi:10.1016/j.cortex.2007.07.005
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sophisticated pre-morbid language and draughting skills, and in whom, because of his unusually early presentation, we had the opportunity to chart, over time, the effect of progressive deterioration in semantic knowledge on a range of tasks not usually thought to be dependent on intact semantic knowledge for their successful execution. The earliest report of a ‘non-semantic’ deficit dates from one of the first experimental studies of SD by Warrington (1975). Although this was primarily an investigation of the patients’ conceptual knowledge, not of their language abilities, the basic psychological assessment indicates errors (by three well-educated patients) in spelling and in reading aloud words with exceptional spelling–sound correspondences. There has, since then, been considerable debate as to whether the almost ubiquitous occurrence amongst SD patients of this ‘surface’ form of acquired dyslexia (i.e., reading words by their surface appearance, resulting in mispronunciations that would be legitimate for words with regular spelling–sound correspondences), is causally-related to their semantic deficit or coincidental with it (Coltheart, 2004; Coltheart et al., 2001; Plaut et al., 1996; Woollams et al., 2007). Since that time too, a number of group studies have shown SD patients to be reliably and predictably impaired on several other purportedly ‘non-semantic’ tasks: past-tense verb transformations (Cortese et al., 2006; Patterson et al., 2001), spelling (Graham et al., 2000), delayed copy drawing (Bozeat et al., 2003; Lambon Ralph and Howard, 2000), lexical decision (Diesfeldt, 1992; Moss et al., 1995; Rogers et al., 2004) and object decision (Rogers et al., 2003; Rogers et al., 2004). In the first study to examine the performance of a group of SD patients on all six of these tasks, Patterson et al. (2006) observed not only that deficits co-occur on all tasks in the same patients but also that each of the tasks is affected in a similar, principled way. In the group of 14 patients participating in that study, success on all of the tasks was subject to a frequencyby-typicality interaction: that is, the patients performed most poorly on lower-frequency items with an atypical surface structure. Moreover, the nature of the errors they produced was consistent across tasks in that, just as for reading aloud, most often the error responses comprised elements that would be legitimate for the more typical instances of a domain, reflecting the patients’ residual knowledge of typicality structure for that domain. Finally, the authors demonstrated that the extent of the deficit on each of these so-called ‘nonsemantic’ tasks was predicted by the severity of the patient’s semantic impairment. Why have we used the term ‘non-semantic’ and why does it appear in inverted commas? The term refers to the fact that these tasks are commonly considered to be non-semantic in their processing demands. In each case, it has been claimed that successful performance requires only access to a cognitive system which (a) incorporates entries corresponding to familiar words (a lexicon) or objects (stored structural descriptions) and (b) in the sequence of processing, precedes and acts as a gateway to semantic knowledge about the word or object. Such arguments have been explicitly voiced, for example, by Coltheart (2004) with respect to reading aloud and lexical decision, by Miozza and Gordon (2005) for past-tense verb inflection, and by Riddoch and Humphreys (1987) for object decision. In addition, it is obvious that normal individuals
can perform tasks such as reading aloud or spelling to dictation or delayed copy drawing, on stimuli that have no corresponding semantic representations: people can read aloud new (or non-sense) words, can produce orthographic representations for spoken words or names that they have never heard before, and can produce delayed copies of non-sense drawings. All of these six tasks, then, have typically been considered non-semantic by many theorists because, it has been argued, they can be accomplished with reference either to stored pre-semantic representations, or to general knowledge/memory, or both, but do not require access to conceptual knowledge about the particular word or object. We consistently place the term in inverted commas, because the accumulating evidence suggests that SD patients are impaired at these tasks precisely because of their semantic deficit, and hence that normal performance does rely, to some extent, on conceptual knowledge of the stimulus materials. In other words, it seems that the standard view of these tasks as non-semantic is probably inaccurate. The cross-sectional study by Patterson et al. (2006) provided compelling evidence of the generality of these observations amongst SD patients, but cross-sectional group studies cannot reveal the longitudinal pattern with which the various associated impairments emerge and progress. The present study aimed to do just this: to investigate the evolution, over time, of ‘non-semantic’ deficits in a single SD patient. This is not a question of idle curiosity. The theory (Rogers et al., 2004) which predicts that semantic deterioration will inevitably be accompanied by a typicality modulated form of impairment on certain ‘non-semantic’ tasks also predicts that the various tasks should be differentially sensitive to declining conceptual knowledge, because the domains assessed by the tasks have different typicality structures. For example, reading written words aloud and writing spoken words to dictation might be thought of as the identical transformation in opposite directions, one from orthography to phonology and the other from phonology to orthography. At least in English, however, there is far more ambiguity about the mappings from phonology to orthography than from orthography to phonology. Within the class of vowels, for instance, there are approximately 20 different vowel phonemes in standard British English; but by Barry and Seymour’s (1988) analysis, there are at least 42 different spellings by which the 20 vowel sounds can be represented in orthography. These authors conclude, ‘‘it follows that sound-to-spelling relationships will necessarily be inconsistent and often markedly more so than spelling-to-sound correspondences’’ (Barry and Seymour, 1988, p. 7). From this perspective, then, surface dysgraphia would be expected to appear at an early stage of semantic decline, with surface dyslexia emerging at a somewhat later stage. Alternatively, since many SD patients are already impaired at reading as well as spelling by the time that they receive formal assessment, the prediction is that the surface dysgraphia will typically be more severe than its counterpart-deficit in the reading domain. SD is of course variable in its severity, and also can display somewhat differing profiles – especially early on – as a function of whether the inevitably bilateral temporal lobe atrophy is more pronounced in the left or right hemisphere (Lambon Ralph et al., 2001). In most respects, however, it is otherwise
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a rather consistent disorder from one case to another. What, then, were the grounds for selecting this particular patient for longitudinal investigation? In the first place, although a senior manager by day, the patient LF was also a published cartoonist and a private essayist. We therefore had access to an unusually rich sample of data reflecting his pre-morbid linguistic ability, draughtsmanship and semantic competence. Examples can be seen in Fig. 1. The first cartoon there dates from approximately six years before he first presented for investigation, the second from the year in which he was diagnosed, the third from the last round of assessment. The shift, from nuanced, sophisticated language and humour in
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the first image, to simpler language and a less subtle form of humour in the second and especially the third, is a poignant reflection of his declining facility with words and meanings. Secondly, and most important for the goal of this study, he presented unusually early in the course of the disease so that we were able to track his condition from a time when semantic impairment was more circumscribed than is usually the case. In consequence he represented at the outset an unusual opportunity to plot the unfolding nature of the disease, especially in relation to its impact on ‘non-semantic’ tasks.
2.
Methods
2.1.
Case history
At the time of his first presentation, LF was a 56-year-old man with a one- to two-year history of word-finding difficulty in daily life. In the workplace this had become sufficiently noticeable as to be the regular butt of office humour. He had hitherto been the resident expert for his colleagues’ queries about words, their meanings and spellings. Initially, and for some time, he attributed his difficulties to age and stress, and was inclined to disregard them. Then, because of an unrelated workplace restructure, he was required to re-apply and be interviewed for his own position, a post he had held for several years. He failed dismally, and he was not re-appointed. Following this episode he sought medical investigation. An MRI brain scan at that time showed striking anterior temporal atrophy, with associated ex-vacuo-dilatation of the left temporal horn, much more marked on the left than the right (see Fig. 2). A PET-FDG study at around the same time showed
Fig. 1 – Three cartoons created by LF dating from a) six years prior to initial presentation; b) the year of diagnosis; c) the latest testing round.
Fig. 2 – Transverse MRI brain scan at time of diagnosis showing characteristic marked atrophy of anterior left temporal lobe, with some but much less marked atrophy of the right.
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marked glucose hypometabolism of the left temporal lobe, which appeared smaller than the right. At the time of the first assessment he looked well and vigorous, he was impeccably dressed, his conversational speech was fluent, socially appropriate and even wryly humorous, and he seemed to have no difficulty understanding what was said to him. There was nothing about his appearance or conversation to indicate anything untoward. He was able to recount, in considerable detail, a recent overseas trip he and his wife had taken, including enumerating less familiar town names (e.g., Lucerne) in the sequence in which they had been visited, and activities (their gondola ride in Venice for instance). Episodic memory was clearly robust. By the time of the final round of testing, self care had become more lax and, while he was still quite eager to communicate, his conversation was limited to a few, well-worn self-referential topics, and his face wore an expression of perpetual bewilderment, reflecting his incomprehension. He could no longer read or watch television with any pleasure, and his once inventive artistic talent was now reduced, on the whole, to occasional slavish copying of pictures or photographs.
2.2.
two naming tests: the Boston Naming Test (Kaplan et al., 1983) and the 48-item Hodges et al. set (Hodges et al., 1992).
2.3.
Longitudinal investigation
Shortly following his initial clinical assessment, and on each of four subsequent occasions, LF was administered three semantic tests plus five of the ‘non-semantic’ tasks mentioned above. The first two sessions were approximately six months apart, the next two each approximately a year apart, and the final round two years after that. In all, the investigation took place over a five-year period. The longitudinal investigation was as follows:
2.3.1.
Semantic knowledge
2.3.1.1. NAMING. LF was assessed on a further test of naming, developed by Graham et al. (1994), consisting of 106 items from three frequency bands (high, middle, low). For the present analysis high and middle frequencies were combined to form a single higher-frequency band, to be contrasted with low frequency items. The patient was asked to name the 106 line drawings of objects.
Clinical neuropsychological assessment 2.3.1.2. WORD–PICTURE
Data from the initial standard neuropsychological assessment is presented in Table 1. Testing comprised the Wechsler Memory Scales – R (Information and Orientation, Logical Memory, Visual Reproduction), Wechsler Adult Intelligence Scales – III (Block Design, Arithmetic, Similarities, Vocabulary, Digit Symbol Substitution), Rey Complex Figure copy and recall, Rey Auditory Verbal Learning Test (RAVLT), Wisconsin Card Sorting Test, National Adult Reading Test and
MATCHING. The identical 106 items were incorporated by Graham et al. (1994) into a comprehension test in which the participant is asked to select the target object (line drawing) from one of five possibilities in a spoken word– picture matching task. The distracter items on each trial comprise a close and a distant semantic foil, a visual foil and a phonological foil (e.g., for the target ‘bear’, the foils were line drawings of a dog, a kangaroo, a motorcycle, hair).
2.3.1.3. VERBAL DESCRIPTION TO NAME. In the final test of semantic
Table 1 – Standard neuropsychology at first evaluation Test (/max; mean s.d.) WMS-R Information/orientation Story recall – immediate (/46; x ¼ 22.5 6.3) Story recall – delayed (/46; x ¼ 18.1 6.0) Visual reproduction – immediate (/41; x ¼ 29.0 5.2) Visual reproduction – delayed (/41; x ¼ 25.4 7.2) WAIS-R (age scaled scores) Block design Arithmetic Similarities Vocabulary Digit symbol substitution Rey figure copy test Copy (/36; x ¼ 35.6 .8) Recall (/36; x ¼ 18.8 7.4) Rey AVLT – immediate, total over five trials (/75; x ¼ 47.6 8.5) Rey AVLT – 20 min delayed recall (/15; x ¼ 10 2.6) Wisconsin CST (/6; 5.6 1.1) NART Boston naming test (/60; x ¼ 54.4 5.2) Hodges et al. naming (/48; x ¼ 43.6 2.3) a Impaired performance.
Score 14 22 17 40 40 14 10 10 8a 13 36 20 33 3 6 categories FSIQ 112 18a 32a
knowledge, LF was asked to describe 12 objects, six living things, six artifacts, in as much detail as he could. The method of scoring was borrowed from that used by Bozeat et al. (2003) to score delayed copy drawings (see below 2.3.2.3). Six neurologically normal control subjects were asked to define the same 12 objects in exactly the same way as LF. There was no time limit. For each object a complete list of the defining features identified by the control subjects was compiled, including the general category to which the object belonged. Only features mentioned by at least four of the six controls were retained as ‘targets’ for scoring LF’s definitions. Thus, for example, for the crocodile the description feature list comprised: animal/reptile, jaws, teeth, skin, water living, dangerous. Where included by controls, a specific feature might be accompanied by one or more modifiers to capture the specific characteristic of that feature in relation to an object. Thus again, for crocodile, modifiers included ‘‘large’’ animal, ‘‘large’’ jaw, ‘‘sharp’’ teeth, ‘‘scaly’’ skin. LF’s definitions were scored by adding up the number of appropriate target features incorporated in his description.
2.3.2.
‘Non-semantic’ tasks
2.3.2.1. SPELLING. Two spelling tests were administered: (i) The first was a 40-item ‘predictability’ spelling test compiled by Graham et al. (2000). In this test single-syllable words
cortex 45 (2009) 483–494
are classified as having high or low predictability spellings on the basis of frequency of phoneme-to-grapheme mapping options within the syllable (initial, medial, final). The test comprises two levels of word frequency, and the words are matched for length across conditions. In each case the experimenter dictated the word, then asked the patient to repeat it to ensure it had been heard correctly before asking the patient to write the word. A sentence using the word was offered for clarification in the case of homophones. (ii) The second consisted of the 106 object names from the Graham et al. (1994) battery as described above. Half of the items have regular spelling–sound correspondences and the other half irregular, a feature which is not especially relevant when the items are being used in the tasks of picture naming or word–picture matching but does enable assessment of the impact of this variable on either reading or (as used here) spelling. It was administered in the same way as the predictability spelling test.
2.3.2.2. READING. The short form of the surface-list reading test (Patterson and Hodges, 1992) consists of 168 single-syllable words, each from 3–6 letters in length, with 42 items in each of the four conditions formed by crossing word frequency (high vs low) and regularity of spelling–sound correspondences (regular vs irregular). The words were presented in random order and the patient was asked to read them aloud. 2.3.2.3. DELAYED COPY DRAWING. Each of 12 line drawings of familiar objects (a subset from the Hodges et al. 48-item semantic battery) was presented individually for about 5 sec for LF to study. The drawing was then taken away and he was asked to count from 1 to 15, which (like SD patients in general) he could do easily. At the end of this approximately 10 sec delay he was asked to draw the picture he had just been looking at. He was not asked to name the object, nor was it named to him at any time during the test. This test was administered at the second, fourth and fifth test rounds. Scoring was done using a modification of the method devised by Bozeat et al. (2003). The six control subjects were asked to produce delayed copy drawings of the 12 items. A list was compiled of all the individual features of each item represented in these drawings. For example, for the crocodile the features were: body, head, feet, snout, tail, eyes, skin. As for the feature list developed to score object descriptions, modifiers (e.g., curved, thin, long) captured differences in form of particular features. Thus the full feature set for the crocodile was: body – long, thin, feet – clawed, head, snout, tail – long, eyes, skin – textured. Again, only features produced by at least two-thirds of control subjects were used as the basis for evaluating the patient’s drawings. As with his verbal definitions, LF’s delayed copy drawings were scored by adding up the number of appropriate target features incorporated in his drawing. Intrusions of incorrect features were also noted. The feature lists for drawings and for descriptions differed in that, in the case of descriptions, shared category features (e.g., body, head, legs, etc.) were not explicitly stated by the normal controls unless there was something distinctive about them. 2.3.2.4. LEXICAL DECISION. This was a version of the test described by Rogers et al. (2004). It is a two-alternative forced choice
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(2AFC) test consisting of 66 pairs, each containing one real word (divided into higher- and lower-frequency sets) and one non-word. In each pair the non-word is a possible pseudo-homophone of the word. There were two typicality conditions, referring to the relationship between the word and non-word. In the Word > Non-Word condition (e.g., rim/ rimb) the word was more orthographically typical of English spelling than the non-word, operationally defined in terms of mean bi- and tri-gram frequencies. In the Non-Word > Word condition (e.g., limb/lim), the non-word was more orthographically typical than the word. The word pairs were presented one at a time, with the real word to the left of the non-word in approximately half the trials, to the right in the other half. The subject was instructed to point to the real word in each pair.
2.3.2.5. OBJECT DECISION. The test described by Rogers et al. (2003) was employed to assess LF’s object decision. As with the lexical decision task, this too was a 2AFC test consisting of 16 pairs, each composed of two line drawings. Here, one drawing was of a real animal, the other a non-real version of the same animal. The frequency manipulation here was based on familiarity ratings of the objects. The typicality manipulation, as with the lexical decision task, refers to the relative typicality of the real versus the non-real version of each object. In the Real > Non-Real condition the real animal was more ordinary or normal than the non-real version (e.g., lion with a tail > lion without a tail); in the NR > R condition the non-real animal was more characteristic of its class than the real one (e.g., gorilla with a tail > gorilla without a tail).
3.
Results
From the standard clinical neuropsychological assessment conducted at the time of presentation (see Table 1) it is clear that the deficits at that time were quite circumscribed. LF scored within normal limits on most tasks with the exception of the vocabulary sub-test of the WAIS-R, the two naming tasks, and the RAVLT, all tests requiring word production. In addition, his object definitions at that time were already greatly impoverished. In contrast, visuospatial ability and visual memory were quite superior. Together, poor performance on naming, vocabulary, word production and object definition in the absence of other cognitive deficits led to an early diagnosis of probable semantic dementia. At the time of the third test round brief assessment showed that he was still performing at an above average level on both the Block Design and Arithmetic sub-tests of the WAIS-R (age scaled scores of 18 and 12, respectively); still achieving six categories on the Wisconsin card sorting test; and both copy and delayed recall of the Rey complex figure were entirely normal. At the same time performance on semantic tasks continued to decline (see Fig. 3). At the final round, when LF was barely capable of making any meaningful utterance, he was still able to score 22/30 on the Mini-Mental Status Examination. His copy of the Rey figure remained remarkably intact although, at this final assessment, recall of the figure was impoverished. The profound impairment to semantic memory occurred therefore on the background of relative preservation
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a
semantic memory given the requirement for verbal output: here, his scores fell from only 37.6% of the maximum possible, even at the first round, to 3.5% (control mean 80.8%, s.d. 9.6). Some examples of his early responses are these:
Performance on semantic tasks
Percent correct
100 80
Peacock: ‘‘It’s a bird, found in forest areas. The male has a large tail it displays. It has a loud voice. Its tail is the largest tail of any bird.’’
60 40 20
Swan: ‘‘I think it’s a bird. It lives in the water.’’
0 1st round
2nd round
3rd round
Word-picture matching
4th round
Goat: ‘‘They’re from the horse, as far as I’m concerned, from the horse background, that’s not the right word. Farm animals, smaller than a normal horse, medium size. They were used on farms as assistants to carry things around.’’
5th round
Naming
Description to name
Naming x frequency
b Percent correct
100
Later descriptions were even more impoverished:
80
Peacock: ‘‘It’s a bird isn’t it? I think they’re a popular bird in terms of the sounds. Can’t remember what they look like. Sings, I think, unless I was thinking of another bird.’’
60 40 20
Swan: ‘‘Can’t think of anything, can’t remember what they look like.’’
0 1st round
2nd round
3rd round HF
4th round
5th round
Goat: ‘‘A goat is a farm animal, light coloured, can’t remember what they look like, farm animals. Don’t know what you get from a goat.’’
LF
Fig. 3 – Graphs showing LF’s longitudinal performance on semantic tasks: a) percent correct scores on naming, word–picture matching and description to name at each of the five test rounds; b) Naming performance on pictures with names in two frequency conditions. Controls perform at close to 100% on these tasks; in b) the dashed line represents control mean scores for lower-frequency items.
In contrast, on word–picture matching, a much less stringent test of semantic ability, his scores were accordingly much less impaired until the very last testing round. His first round score was close to that of controls (97.2% correct, compared with control mean of 99.3%, s.d. .8), had fallen at the fourth round but was still as high as 91.5%, and only dropped significantly at the final assessment 41.9%. At the last round, he frequently offered ‘‘don’t know’’ and had to be prompted to make a response. Consonant with this, there was a random character to his responses with errors from all classes of foils.
of other aspects of cognition until quite late in the disease course.
3.1.
Longitudinal investigation of semantic knowledge 3.2. Longitudinal investigation of performance on ‘non-semantic’ tasks
Over the five assessment rounds LF’s semantic knowledge deteriorated steadily. Total score for naming of pictures on the Graham et al. (1994) task declined from 65.1% to 5.7% over time (see Table 2 and Fig. 3). Naming was always substantially worse for lower frequency than for higher-frequency items. LF’s semantic impairment was even more evident in his impaired descriptions of objects in response to their spoken names. This is, of course, a particularly challenging test of
Fig. 4 shows LF’s progressive decline in spelling and reading aloud. For each task the results are presented in terms of item frequency and typicality. The graphs represent the number of correct responses as a percentage of the total number of items in that condition. The dashed line in each graph represents mean score for control subjects in the low frequency,
Table 2 – Longitudinal investigation of semantic knowledge (control means, standard deviations in brackets) Test Naming (92.5% 4.2) Word–picture match (99.3% .8) Description to name (80.8% 9.6) Scores as % correct responses.
1st round
2nd round
3rd round
4th round
5th round
65.1 97.2 40.0
66.0 90.6 29.4
45.3 96.2 17.6
36.8 91.5 12.9
5.7 49.1 3.5
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Percent correct
a
Response type as a proportion of items
Predictability Spelling
a
100
Predictability spelling
.8
80 60 40
.6
20 0
.4
1st round 2nd round 3rd round 4th round 5th round HF Reg
LF Reg
HF Irr
LF Irr .2
Percent correct
b
Spelling (Graham et al. 1994) 100 0
80
1
2
3
4
LARC
Visual/other
5
60 Correct
40 20
b
0 1st round
2nd round HF Reg
3rd round LF Reg
4th round HF Irr
5th round
Graham et al. spelling
.8
LF Irr .6
Percent correct
c
Reading (Surface List) 100 .4
80 60
.2
40 20 0 1st round
2nd round HF Reg
3rd round LF Reg
4th round HF Irr
5th round
0 1
LF Irr
Fig. 4 – LF’s longitudinal performance (% correct) on two tests of spelling (a) predictability spelling; b) Graham et al. (1994), and (c) reading aloud. In each graph the dashed line represents controls’ mean score for that task on the LF’s irregular word condition.
2
3
Correct
c
LARC
4
5
Visual/other
Surface list reading
1 .8 .6
atypical condition of the task: spelling (predictability list) 94.8%; reading aloud 95.6%. For each of these tasks LF’s performance on the low frequency, irregular items was the most vulnerable. This was so at the first testing round, and remained the case as the disease progressed. Spelling errors were most often phonologically plausible alternatives to the target: for example, his responses parashoot, sizzers, scwirral, and kanough are all plausible enough not to require specifying the target word. Occasionally LF’s errors combined phonologically plausible incorrect elements with some apparent residual knowledge of the target’s unique spelling (e.g., ‘‘bouquet’’/bokait). Fig. 5 presents LF’s spelling and reading performance with all responses classified as correct or as one of his two main types of error. LARC errors (standing for Legitimate Alternative Rendering of Components: Patterson et al., 1995) are called ‘legitimate’ alternatives because the response would be correct if the stimulus word were typical rather than atypical. Examples of LARC errors for the two tasks are as follows: in reading aloud, sew/‘‘sue’’; in spelling to dictation, ‘‘cough’’/coff (see Table 3). Visual and other errors refer to any incorrect responses that cannot be classified
.4 .2 0 1
2 Correct
3 LARC
4
5
Visual/other
Fig. 5 – LF’s longitudinal performance on the same three tasks as in Fig. 4, but here with responses assigned to one of three bins: correct, LARC errors, other sorts of error.
as LARC errors. Fig. 5 demonstrates that, over time, LF’s correct responses declined and LARC errors rose almost to equal them in the case of reading and substantially to overtake them in the case of spelling. Other types of errors remained infrequent for both tasks and at all test sessions. Performance on the delayed copy task also declined over time (see Fig. 6 for an example: LF’s delayed copy of a peacock at testing rounds 2, 4 and 5). The first time his drawing was
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Table 3 – Examples of LARC errors in LF’s spelling to dictation for the same three words ( giraffe, xylophone and silhouette) across testing rounds Round
1
2
3
4
5
Jeraf gerafe jeraph jirraph gerafe Zilophone pzylophone zilaphone zialafone zillofone Cilluet syloet siloett cillowet sellewet
assessed, at the second testing round, his score was 89.4% of the maximum possible, 61.7% at the last. This compared with a control mean of 94.5% (s.d. 3.4; range 90.9%–98.4%). Initially his drawings of artefacts (e.g., toaster, helicopter, motorcycle) were as competent and detailed as those of the control subjects. At the last testing round, these objects were no longer recognizable for the paucity of detail he was able to produce (see Fig. 7). An additional phenomenon accompanied his delayed copy of animals over time. Although there were inaccuracies, even on the first occasion that the test was administered, all of the six creatures were recognizable. In dramatic contrast, at the final round four of the animals (rhinoceros, swan, goat, crocodile) resembled one another to a remarkable degree, the distinguishing features having been replaced by generic animal heads, bodies, ears, legs and tails (Fig. 8). The crocodile lost the webbing of its feet, the swan acquired extra legs and paws and an animal’s head in place of the bird-like head and beak. The last peacock, from the same testing round (see Fig. 6), lost any remnants of bird-likeness and now had four legs, an animal head and tail. It retained something indeterminate and unusual on its back, the last vestige of knowledge of something special at a peacock’s nether end. The sixth animal tested, the lobster, also became less recognizable over time but, in the same manner as the artefacts, showing loss of detail rather than intrusion of erroneous features. This is hardly surprising, since finally LF had no idea even that a lobster was a living thing. Performance on the object and lexical decision tasks is reported in Fig. 9. Even at the last round LF made too few errors on the former task for any pattern to emerge with respect to frequency. Four of the five errors were, however, of the predicted form; that is, LF selected the more typical, non-real object in preference to the less typical real object (cow without udder, gorilla with tail, frog with paws rather than webbed feet, turtle with ears). There were far more errors in the lexical decision task with an overall decline over time from 93.9% at the second round to 57.8% at the fifth. In general, he did less well with lower than with higher-frequency items but, unexpectedly, there were some errors in all conditions. Fig. 10 displays an additional way of assessing the main question addressed by this study, namely the relative order in which deficits on different ‘non-semantic’ tasks might emerge as the semantic system deteriorates. To be more precise, what Fig. 10 represents is the order in which the predicted form of deficit on these tasks developed over time for LF, namely a disadvantage in dealing with items atypical for the relevant domain. The figure displays – for each testing round and within each task – the relative disadvantage in LF’s scores for atypical relative to typical items. Fig. 10 indicates that, relatively early in his semantic decline (Testing Round 2), LF
Fig. 6 – LF’s delayed copy drawing of a peacock at a) second test round; b) fourth test round; c) final test round. revealed the predicted effect of typicality most markedly in spelling, and to a lesser extent for reading. Over succeeding rounds the effect was present consistently for spelling and increasingly for reading, dramatically so at Round 5. By Round 5, the predicted typicality effect had emerged for the two forced
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Percent correct
a
Object Decision 100 80 60 40 20 0 1st round
2nd round
HF R>NR
Percent correct
b
3rd round
LF R>NR
4th round
HF NR>R
5th round
LF NR>R
Lexical Decision 100 80 60 40 20 0 1st round
2nd round
HF R>NR
Fig. 7 – Delayed copy of a motorcycle at test rounds 2 and 5 showing preserved draughting skill initially but catastrophic loss of detail over time. choice tasks (lexical decision and object decision) as well, such that LF now showed the predicted pattern for all four tasks.
4.
Discussion
This study reports a longitudinal investigation of a patient with semantic dementia in whom several apparently unrelated and apparently ‘non-semantic’ tasks were all compromised in
3rd round
LF R>NR
4th round
HF NR>R
5th round
LF NR>R
Fig. 9 – Scores (% correct) on the object and lexical decision tasks.
concert with the loss of semantic knowledge. The patient was a man whose pre-morbid skills, in terms of both language competence and draughtsmanship, threw into dramatic relief the deterioration of performance on semantic and ‘nonsemantic’ tasks alike. The case demonstrates that not all of these tasks need be affected at the same time, but that over time they all do become compromised. It also demonstrates that impairment on ‘non-semantic’ tasks (here, spelling in particular) can be evident even when the semantic impairment remains relatively mild. The items most likely to be affected,
Fig. 8 – Drawings of a) rhinoceros, b) goat, c) swan and d) crocodile at the final test round.
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Disadvantage for atypical items 50
Size of discrepancy (%)
40 30 20 10 0 -10 -20 2nd round
3rd round
4th round
5th round
Testing Round Object Decision
Reading
Lexical Decision
Spelling
Fig. 10 – For each testing round and task, the relative disadvantage in LF’s scores for atypical relative to typical items.
on the majority of testing occasions and tasks, were those of lower frequency and, importantly, with a less typical form in the relevant modality or mapping. And on all tasks the nature of the errors was most often to render atypical instances (e.g., words with exceptional sound–spelling correspondence) or features (e.g., animals with uncharacteristic appearance) more typical. By virtue of having been ‘caught’ so early in progression, LF displayed an unusually mild semantic deficit at the first round of testing. Patterson et al. (2006) noted that naming is the semantic task most sensitive to mild semantic impairment whereas word–picture matching is more sensitive to moderate or severe impairment. LF’s naming score at the initial assessment was the principal clue to the possibility of a semantic deficit, though there was further evidence in the already impoverished descriptions he gave in response to object names. While this task relies on the subject’s ability to verbalize, the paucity of content on the test was dramatically at odds with his conversational speech which was, until the fourth testing round, fluent, unhesitating and, even up to that point, quite richly detailed. Although this phenomenon has never to our knowledge been formally assessed, the contrast between spontaneous speech – where the patient can largely control the topic and vocabulary – as opposed to ‘responsive mode’ speech in which the experimenter calls the tune, is dramatically apparent to all clinicians and researchers who interact with SD patients. As the disease progressed, of course, LF’s semantic impairment became more noticeable in spontaneous conversation as well as much more pervasive on formal testing. Word–picture matching, in contrast, remained only mildly impaired until the final testing round. The substantial anomia paired with only rather mildly disrupted single-word comprehension (at least on a relatively easy word–picture matching task) that LF displayed over several years is characteristic of SD patients whose
anterior temporal lobe atrophy is strongly lateralised to the left (Lambon Ralph et al., 2001). Notwithstanding relatively mild semantic loss, impaired performance on one ‘non-semantic’ task, spelling, was already evident at LF’s first testing round; and Fig. 10 indicates the order in which the other deficits emerged. Whilst acknowledging the caution appropriate in drawing general conclusions on the basis of data from a single case, we derive two tentative conclusions, or hypotheses, from Fig. 10. The first reinforces and extends the conclusion of Woollams et al. (2007) concerning the association between SD and surface dyslexia: it appears that the question about these associated ‘non-semantic’ deficits in SD is not whether an SD patient will have them but only when. That is, the degree of semantic degradation that will engender impairment in reading or lexical decision or delayed copy drawing seems to vary somewhat from one patient to another (not to mention variability in the sensitivity of different tests designed to assess these cognitive abilities); but where patients have been followed longitudinally, there is as yet no indication that any of these abilities ever remains immune to semantic decline. In this regard, it is important to note that this is not a matter of globally deteriorating cognition in which everything eventually fails. Were that the case, one would have to expect that sometimes SD patients would be unable to do these tasks at all, or that the nature of their impairment would often assume a different pattern. Instead, the patients continue to perform these tasks and consistently fail only in the specific frequency-and-typicality modulated fashion revealed here for LF and for 14 other SD patients studied by Patterson et al. (2006). The second hypothesis to which LF’s data give some credence is this: although there may always remain a degree of unpredictability in the stage of semantic decline at which a particular SD patient will reveal one of these particular deficits on a particular test of the pertinent ability, the order in which the different deficits emerge may be rather more predictable, based on an analysis of the typicality structure relevant to that task. We have only limited support for this hypothesis from LF, because we have not as yet attempted a formal or quantified analysis of the systematicity in these various domains. As a result, our only serious current prediction for LF – and for other SD patients yet to be studied – was that spelling should be vulnerable sooner than reading aloud, because the mappings from sound to spelling in English are substantially less systematic than those from spelling to sound (Barry and Seymour, 1988; Venezky, 1970). There is also a little ‘circumstantial’ support for this prediction from two previous reports on spelling in SD. In the cross-sectional study by Patterson et al. (2006), every single one of the 14 patients was more impaired at spelling words with an atypical sound–spelling correspondence than at reading words with an atypical spelling–sound correspondence. And in the study of spelling and reading by Graham et al. (2000), it was striking that, until the very late stages of the disease, SD patients were substantially impaired at reading only for lower-frequency exception words, but were relatively competent at spelling only for higher-frequency regular words. This again makes good sense in terms of a systematicity comparison between reading and spelling. Take, for example, the English words
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MEET and MEAT. These are both ‘regular’ for reading: that is, despite the occasional neighbour with a different pronunciation (like THREAT), almost all words ending in –EET or –EAT are pronounced ‘‘eet’’. Thus faced with an unfamiliar written word with either of these spelling patterns (say PREET or PREAT), one would be fairly safe in saying ‘‘preet’’. But then how is one to choose between these two orthographic correspondences when given the spoken word ‘‘preet’’ to spell? LF’s performance on the delayed copy task was especially striking in view of his obvious, and highly practiced, skill as a draughtsman. Reflecting this natural talent, his early drawings, especially but not only of artefacts, were even better than those of control subjects, but there was clear decline over time. Initially, drawings of both animals and artefacts were prone to relatively minor omissions. More significant errors appeared at the later rounds. Qualitatively, too, the errors were revealing (see Figs. 6–8). His drawing of all of the objects was characterized by loss of detail to the point of their becoming unrecognizable. In the case of animals especially, there was – in addition to the gradual disappearance of distinctive, atypical features (the peacock’s tail, the webbed feet of the crocodile) – their replacement by elements more typical of the domain. The result is a visual equivalent of regularization errors in reading. Thus, for example, the peacock’s head was highly bird-like on the first occasion but looked much more like the head of a dog at the second; its feet had become paws. Finally, it resembled the other animals, with a generic animal head, four legs and a typical animal tail, and what ought to be the fan-like peacock tail has become a unrecognizable load on its back (see Fig. 6). Bearing in mind that LF had been exposed to line drawings of these objects moments before being asked to draw them, these errors are amongst the most intriguing and point to an unexpectedly prominent role for semantic knowledge in this non-verbal task. Loss of detail in LF’s delayed object copies was mirrored in his scores on the Rey complex figure test: his copy and delayed copy scores for this meaningless figure were both within the normal range on the first occasion of testing, whereas at the last he was still able to produce an elegant rendition if the model remained in view, but his delayed recall was so impoverished that it comprised just the shell of the original figure. This is not, however, to say that LF’s decline in these two delayed copy tasks had the same characteristics, and certainly not that we accord it the same interpretation. SD patients invariably have preserved performance for direct copy of both the meaningless Rey figure and meaningful drawings of real objects; and they often achieve success within the normal range (which is far from perfect: delayed recall of non-sense is difficult even for normal mortals) on delayed copy of the meaningless Rey figure, where the delay is usually on the order of 30–45 min. The one task where their performance is very discrepant from normal is briefly delayed copy of meaningful objects. As discussed at some length by Patterson (2007), this makes sense when one realises that – of the four copy tasks under discussion here (direct vs delayed, meaningful vs meaningless) – the combination of delayed and meaningful is the only one where conceptual knowledge of the content to be reproduced will inevitably affect performance. One does not need to know either that a picture represents a swan or that a swan is a bird and therefore has two legs
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in order to produce two legs in direct copy of the swan: there are the two legs in one’s direct view, demanding to be drawn. And when a normal individual has looked at a picture of a swan and of course classified it as such, he or she does not need to remember those two legs in precise physical detail to reproduce them in the delayed copy: the prior semantic classification demands that the response will have two legs. But when an SD patient like LF looks at a picture of a swan, he can neither name it nor classify it as a swan, only as some sort of generic animal. A short time later, he – just like a normal participant – will have lost substantial memory for the precise visual details of the drawing; and also just like a normal participant, his drawing will be informed (or in his case, misinformed) by his prior conceptual classification. Generic animals have four legs; thus LF’s delayed copy of the swan has four legs. This case adds to the growing body of evidence that a number of cognitive processes, not usually considered to be ‘semantic’ in their demands, nevertheless rely on the integrity of semantic knowledge for successful execution. It is a particularly striking demonstration of the ravages of semantic loss because of the robust early skills and linguistic competence of the patient; we had unusually privileged access to evidence of these, by virtue of his second ‘profession’. As a published cartoonist he had been capable of linguistic virtuosity and skilled draughting, lending particular poignancy to the loss of these talents over time. The case adds to our current understanding in demonstrating that not all tasks are equally vulnerable at the same moment in the course of the disease; and in further characterizing the ways in which degraded semantics disrupt the ability to perform so-called ‘nonsemantic’ tasks.
Acknowledgements Our very warm thanks to LF and his wife, who were unfailingly gracious and cooperative through many hours of testing over a long and, what was for both of them, in different ways, difficult time.
references
Barry C and Seymour PHK. Lexical priming and sound-to-spelling contingency effects in nonword spelling. Quarterly Journal of Experimental Psychology, 40A: 5–40, 1988. Bozeat S, Lambon Ralph MA, Graham KS, Patterson K, Wilkin H, Rowland JK, Rogers TT, and Hodges JR. A duck with four legs: investigating the structure of conceptual knowledge using picture drawing in semantic dementia. Cognitive Neuropsychology, 20: 27–47, 2003. Coltheart M. Are there lexicons? Quarterly Journal of Experimental Psychology, 57A: 1153–1171, 2004. Coltheart M, Rastle K, Perry C, Langdon R, and Ziegler J. DRC: a dual route cascaded model of visual word recognition and reading aloud. Psychological Review, 108: 204–256, 2001. Cortese MJ, Balota DA, Sergent-Marshall SD, Buckner RL, and Gold BT. Consistency and regularity in past tense verb generation in healthy aging, Alzheimer’s disease, and
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semantic dementia. Cognitive Neuropsychology, 23: 856–876, 2006. Diesfeldt HFA. Impaired and preserved semantic memory functioning in dementia. In Backman L (Ed), Memory Functioning in Dementia. Amsterdam: Elsevier, 1992. Graham KS, Hodges JR, and Patterson K. The relationship between comprehension and oral reading in progressive fluent aphasia. Neuropsychologia, 32: 299–316, 1994. Graham NL, Patterson K, and Hodges JR. The impact of semantic memory impairment on spelling: evidence from semantic dementia. Neuropsychologia, 38: 143–163, 2000. Hodges JR, Patterson K, Oxbury S, and Funnell E. Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain, 115: 1783–1806, 1992. Kaplan E, Goodglass H, and Weintraub S. Boston Naming Test. Philadelphia: Lea & Febiger, 1983. Lambon Ralph MA and Howard D. Gogi aphasia or semantic dementia? Simulating and assessing poor verbal comprehension in a case of progressive fluent aphasia. Cognitive Neuropsychology, 17: 437–465, 2000. Lambon Ralph MA, McClelland JL, Patterson K, Galton CJ, and Hodges JR. No right to speak? The relationship between object naming and semantic impairment: neuropsychological evidence and a computational model. Journal of Cognitive Neuroscience, 13: 341–356, 2001. Miozza M and Gordon P. Facts, events and inflection: when language and memory dissociate. Journal of Cognitive Neuroscience, 17: 1074–1086, 2005. Moss HE, Tyler LK, Hodges JR, and Patterson K. Exploring the loss of semantic memory in semantic dementia: evidence from a primed monitoring study. Neuropsychology, 9: 16–26, 1995. Patterson K. The reign of typicality in semantic memory: evidence from neuropsychology, brain imaging and computational modelling. Philosophical Transactions of the Royal Society, 362: 813–821, 2007.
Patterson K and Hodges JR. Deterioration of word meaning: implications for reading. Neuropsychologia, 30: 1025–1040, 1992. Patterson K, Suzuki T, Wydell T, and Sasanuma S. Progressive aphasia and surface alexia in Japanese. Neurocase, 1: 155–165, 1995. Patterson K, Lambon Ralph MA, Hodges JR, and McClelland JL. Deficits in irregular past-tense verb morphology associated with degraded semantic knowledge. Neuropsychologia, 30: 1025–1040, 2001. Patterson K, Lambon Ralph MA, Jefferies E, Woollams A, Jones R, Hodges JR, and Rogers TT. ‘Pre-semantic’ cognition in semantic dementia: six deficits in search of an explanation. Journal of Cognitive Neuroscience, 18: 169–183, 2006. Plaut DC, McClelland JL, Seidenberg MS, and Patterson K. Understanding normal and impaired word reading: computational principles in quasi-regular domains. Psychological Review, 103: 56–115, 1996. Riddoch MJ and Humphreys GW. Visual object processing in optic aphasia: a case of semantic access agnosia. Cognitive Neuropsychology, 4: 131–185, 1987. Rogers TT, Lambon Ralph MA, Hodges JR, and Patterson K. Object recognition under semantic impairment: the effects of conceptual regularities on perceptual decisions. Language and Cognitive Processes, 18: 625–662, 2003. Rogers TT, Lambon Ralph MA, Hodges JR, and Patterson K. Natural selection: the impact of semantic impairment on lexical and object decision. Cognitive Neuropsychology, 21: 331–352, 2004. Venezky RL. The Structure of English Orthography. The Hague: Mouton, 1970. Warrington EK. The selective impairment of semantic memory. Quarterly Journal of Experimental Psychology, 27: 635–657, 1975. Woollams AM, Lambon Ralph MA, Plaut DC, and Patterson K. SDsquared: on the association between semantic dementia and surface dyslexia. Psychological Review, 114: 316–339, 2007.
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journal homepage: www.elsevier.com/locate/cortex
Research report
Emergence and progression of ‘non-semantic’ deficits in semantic dementia Diana Cainea,*, Nora Breenb and Karalyn Pattersonc a
University of Manchester, Manchester, UK Royal Prince Alfred Hospital, Sydney, Australia c MRC Cognition and Brain Sciences Unit, Cambridge, UK b
article info
abstract
Article history:
Although semantic dementia (SD) is defined as a selective disruption of conceptual know-
Received 4 December 2006
ledge, a number of group studies have now demonstrated that SD patients also show
Reviewed 18 May 2007
impaired performance on tasks not usually considered to have a high semantic load
Revised 18 June 2007
(e.g., reading words aloud and lexical or object decision). The aim of the current study
Accepted 2 July 2007
was to document the relative deterioration, over time, of a number of semantic and so-
Action editor Art Shiamura
called ‘non-semantic’ tasks in LF, a single case of SD for whom – by virtue of his work as
Published online 20 February 2008
a published cartoonist – we also have extensive data regarding his pre-morbid linguistic and drawing skills.
Keywords:
In five testing rounds over a period of five years we administered semantic tests of
Semantic dementia
object naming and object definition (on both of which LF was progressively impaired, as
Semantic impairment
expected for a diagnosis of SD), plus verbal and non-verbal ‘non-semantic’ tasks of reading
Acquired dysgraphia
aloud, spelling, object and lexical decision, and delayed copy drawing.
Surface dyslexia Delayed copy drawing
Initially, his only striking ‘non-semantic’ deficit was in the domain of spelling – a pronounced surface dysgraphia in an individual with demonstrably superior pre-morbid spelling skill. Over time, and in line with his declining semantic system, LF’s performance gradually deteriorated on all of the ‘non-semantic’ tasks. The most vulnerable items on most tasks were those with low frequency and an atypical form. This report adds to the growing body of evidence that a number of cognitive processes not usually considered to be ‘semantic’ in their demands rely on the integrity of semantic knowledge for successful execution. Furthermore, it provides the first indication that these non-semantic deficits might emerge in an order predictable from the typicality structure of the relevant domain. Crown Copyright ª 2008 Published by Elsevier Srl. All rights reserved.
Semantic dementia (SD) is a progressive neurodegenerative disorder defined by its pathognomonic feature, a selective disruption to conceptual knowledge. Notwithstanding the highly focal nature of the disease, if tested appropriately SD patients
are also typically impaired on cognitive processes usually thought to be executed independently of semantics. Here we present the longitudinal investigation of patient LF, whose published cartoons over 30 years were abundant evidence of
* Corresponding author. School of Psychological Sciences (NARU), Zochonis Building, University of Manchester, Oxford Road, Manchester M13 9PL, UK. E-mail address: [email protected] (D. Caine). 0010-9452/$ – see front matter Crown Copyright ª 2008 Published by Elsevier Srl. All rights reserved. doi:10.1016/j.cortex.2007.07.005
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sophisticated pre-morbid language and draughting skills, and in whom, because of his unusually early presentation, we had the opportunity to chart, over time, the effect of progressive deterioration in semantic knowledge on a range of tasks not usually thought to be dependent on intact semantic knowledge for their successful execution. The earliest report of a ‘non-semantic’ deficit dates from one of the first experimental studies of SD by Warrington (1975). Although this was primarily an investigation of the patients’ conceptual knowledge, not of their language abilities, the basic psychological assessment indicates errors (by three well-educated patients) in spelling and in reading aloud words with exceptional spelling–sound correspondences. There has, since then, been considerable debate as to whether the almost ubiquitous occurrence amongst SD patients of this ‘surface’ form of acquired dyslexia (i.e., reading words by their surface appearance, resulting in mispronunciations that would be legitimate for words with regular spelling–sound correspondences), is causally-related to their semantic deficit or coincidental with it (Coltheart, 2004; Coltheart et al., 2001; Plaut et al., 1996; Woollams et al., 2007). Since that time too, a number of group studies have shown SD patients to be reliably and predictably impaired on several other purportedly ‘non-semantic’ tasks: past-tense verb transformations (Cortese et al., 2006; Patterson et al., 2001), spelling (Graham et al., 2000), delayed copy drawing (Bozeat et al., 2003; Lambon Ralph and Howard, 2000), lexical decision (Diesfeldt, 1992; Moss et al., 1995; Rogers et al., 2004) and object decision (Rogers et al., 2003; Rogers et al., 2004). In the first study to examine the performance of a group of SD patients on all six of these tasks, Patterson et al. (2006) observed not only that deficits co-occur on all tasks in the same patients but also that each of the tasks is affected in a similar, principled way. In the group of 14 patients participating in that study, success on all of the tasks was subject to a frequencyby-typicality interaction: that is, the patients performed most poorly on lower-frequency items with an atypical surface structure. Moreover, the nature of the errors they produced was consistent across tasks in that, just as for reading aloud, most often the error responses comprised elements that would be legitimate for the more typical instances of a domain, reflecting the patients’ residual knowledge of typicality structure for that domain. Finally, the authors demonstrated that the extent of the deficit on each of these so-called ‘nonsemantic’ tasks was predicted by the severity of the patient’s semantic impairment. Why have we used the term ‘non-semantic’ and why does it appear in inverted commas? The term refers to the fact that these tasks are commonly considered to be non-semantic in their processing demands. In each case, it has been claimed that successful performance requires only access to a cognitive system which (a) incorporates entries corresponding to familiar words (a lexicon) or objects (stored structural descriptions) and (b) in the sequence of processing, precedes and acts as a gateway to semantic knowledge about the word or object. Such arguments have been explicitly voiced, for example, by Coltheart (2004) with respect to reading aloud and lexical decision, by Miozza and Gordon (2005) for past-tense verb inflection, and by Riddoch and Humphreys (1987) for object decision. In addition, it is obvious that normal individuals
can perform tasks such as reading aloud or spelling to dictation or delayed copy drawing, on stimuli that have no corresponding semantic representations: people can read aloud new (or non-sense) words, can produce orthographic representations for spoken words or names that they have never heard before, and can produce delayed copies of non-sense drawings. All of these six tasks, then, have typically been considered non-semantic by many theorists because, it has been argued, they can be accomplished with reference either to stored pre-semantic representations, or to general knowledge/memory, or both, but do not require access to conceptual knowledge about the particular word or object. We consistently place the term in inverted commas, because the accumulating evidence suggests that SD patients are impaired at these tasks precisely because of their semantic deficit, and hence that normal performance does rely, to some extent, on conceptual knowledge of the stimulus materials. In other words, it seems that the standard view of these tasks as non-semantic is probably inaccurate. The cross-sectional study by Patterson et al. (2006) provided compelling evidence of the generality of these observations amongst SD patients, but cross-sectional group studies cannot reveal the longitudinal pattern with which the various associated impairments emerge and progress. The present study aimed to do just this: to investigate the evolution, over time, of ‘non-semantic’ deficits in a single SD patient. This is not a question of idle curiosity. The theory (Rogers et al., 2004) which predicts that semantic deterioration will inevitably be accompanied by a typicality modulated form of impairment on certain ‘non-semantic’ tasks also predicts that the various tasks should be differentially sensitive to declining conceptual knowledge, because the domains assessed by the tasks have different typicality structures. For example, reading written words aloud and writing spoken words to dictation might be thought of as the identical transformation in opposite directions, one from orthography to phonology and the other from phonology to orthography. At least in English, however, there is far more ambiguity about the mappings from phonology to orthography than from orthography to phonology. Within the class of vowels, for instance, there are approximately 20 different vowel phonemes in standard British English; but by Barry and Seymour’s (1988) analysis, there are at least 42 different spellings by which the 20 vowel sounds can be represented in orthography. These authors conclude, ‘‘it follows that sound-to-spelling relationships will necessarily be inconsistent and often markedly more so than spelling-to-sound correspondences’’ (Barry and Seymour, 1988, p. 7). From this perspective, then, surface dysgraphia would be expected to appear at an early stage of semantic decline, with surface dyslexia emerging at a somewhat later stage. Alternatively, since many SD patients are already impaired at reading as well as spelling by the time that they receive formal assessment, the prediction is that the surface dysgraphia will typically be more severe than its counterpart-deficit in the reading domain. SD is of course variable in its severity, and also can display somewhat differing profiles – especially early on – as a function of whether the inevitably bilateral temporal lobe atrophy is more pronounced in the left or right hemisphere (Lambon Ralph et al., 2001). In most respects, however, it is otherwise
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a rather consistent disorder from one case to another. What, then, were the grounds for selecting this particular patient for longitudinal investigation? In the first place, although a senior manager by day, the patient LF was also a published cartoonist and a private essayist. We therefore had access to an unusually rich sample of data reflecting his pre-morbid linguistic ability, draughtsmanship and semantic competence. Examples can be seen in Fig. 1. The first cartoon there dates from approximately six years before he first presented for investigation, the second from the year in which he was diagnosed, the third from the last round of assessment. The shift, from nuanced, sophisticated language and humour in
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the first image, to simpler language and a less subtle form of humour in the second and especially the third, is a poignant reflection of his declining facility with words and meanings. Secondly, and most important for the goal of this study, he presented unusually early in the course of the disease so that we were able to track his condition from a time when semantic impairment was more circumscribed than is usually the case. In consequence he represented at the outset an unusual opportunity to plot the unfolding nature of the disease, especially in relation to its impact on ‘non-semantic’ tasks.
2.
Methods
2.1.
Case history
At the time of his first presentation, LF was a 56-year-old man with a one- to two-year history of word-finding difficulty in daily life. In the workplace this had become sufficiently noticeable as to be the regular butt of office humour. He had hitherto been the resident expert for his colleagues’ queries about words, their meanings and spellings. Initially, and for some time, he attributed his difficulties to age and stress, and was inclined to disregard them. Then, because of an unrelated workplace restructure, he was required to re-apply and be interviewed for his own position, a post he had held for several years. He failed dismally, and he was not re-appointed. Following this episode he sought medical investigation. An MRI brain scan at that time showed striking anterior temporal atrophy, with associated ex-vacuo-dilatation of the left temporal horn, much more marked on the left than the right (see Fig. 2). A PET-FDG study at around the same time showed
Fig. 1 – Three cartoons created by LF dating from a) six years prior to initial presentation; b) the year of diagnosis; c) the latest testing round.
Fig. 2 – Transverse MRI brain scan at time of diagnosis showing characteristic marked atrophy of anterior left temporal lobe, with some but much less marked atrophy of the right.
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marked glucose hypometabolism of the left temporal lobe, which appeared smaller than the right. At the time of the first assessment he looked well and vigorous, he was impeccably dressed, his conversational speech was fluent, socially appropriate and even wryly humorous, and he seemed to have no difficulty understanding what was said to him. There was nothing about his appearance or conversation to indicate anything untoward. He was able to recount, in considerable detail, a recent overseas trip he and his wife had taken, including enumerating less familiar town names (e.g., Lucerne) in the sequence in which they had been visited, and activities (their gondola ride in Venice for instance). Episodic memory was clearly robust. By the time of the final round of testing, self care had become more lax and, while he was still quite eager to communicate, his conversation was limited to a few, well-worn self-referential topics, and his face wore an expression of perpetual bewilderment, reflecting his incomprehension. He could no longer read or watch television with any pleasure, and his once inventive artistic talent was now reduced, on the whole, to occasional slavish copying of pictures or photographs.
2.2.
two naming tests: the Boston Naming Test (Kaplan et al., 1983) and the 48-item Hodges et al. set (Hodges et al., 1992).
2.3.
Longitudinal investigation
Shortly following his initial clinical assessment, and on each of four subsequent occasions, LF was administered three semantic tests plus five of the ‘non-semantic’ tasks mentioned above. The first two sessions were approximately six months apart, the next two each approximately a year apart, and the final round two years after that. In all, the investigation took place over a five-year period. The longitudinal investigation was as follows:
2.3.1.
Semantic knowledge
2.3.1.1. NAMING. LF was assessed on a further test of naming, developed by Graham et al. (1994), consisting of 106 items from three frequency bands (high, middle, low). For the present analysis high and middle frequencies were combined to form a single higher-frequency band, to be contrasted with low frequency items. The patient was asked to name the 106 line drawings of objects.
Clinical neuropsychological assessment 2.3.1.2. WORD–PICTURE
Data from the initial standard neuropsychological assessment is presented in Table 1. Testing comprised the Wechsler Memory Scales – R (Information and Orientation, Logical Memory, Visual Reproduction), Wechsler Adult Intelligence Scales – III (Block Design, Arithmetic, Similarities, Vocabulary, Digit Symbol Substitution), Rey Complex Figure copy and recall, Rey Auditory Verbal Learning Test (RAVLT), Wisconsin Card Sorting Test, National Adult Reading Test and
MATCHING. The identical 106 items were incorporated by Graham et al. (1994) into a comprehension test in which the participant is asked to select the target object (line drawing) from one of five possibilities in a spoken word– picture matching task. The distracter items on each trial comprise a close and a distant semantic foil, a visual foil and a phonological foil (e.g., for the target ‘bear’, the foils were line drawings of a dog, a kangaroo, a motorcycle, hair).
2.3.1.3. VERBAL DESCRIPTION TO NAME. In the final test of semantic
Table 1 – Standard neuropsychology at first evaluation Test (/max; mean s.d.) WMS-R Information/orientation Story recall – immediate (/46; x ¼ 22.5 6.3) Story recall – delayed (/46; x ¼ 18.1 6.0) Visual reproduction – immediate (/41; x ¼ 29.0 5.2) Visual reproduction – delayed (/41; x ¼ 25.4 7.2) WAIS-R (age scaled scores) Block design Arithmetic Similarities Vocabulary Digit symbol substitution Rey figure copy test Copy (/36; x ¼ 35.6 .8) Recall (/36; x ¼ 18.8 7.4) Rey AVLT – immediate, total over five trials (/75; x ¼ 47.6 8.5) Rey AVLT – 20 min delayed recall (/15; x ¼ 10 2.6) Wisconsin CST (/6; 5.6 1.1) NART Boston naming test (/60; x ¼ 54.4 5.2) Hodges et al. naming (/48; x ¼ 43.6 2.3) a Impaired performance.
Score 14 22 17 40 40 14 10 10 8a 13 36 20 33 3 6 categories FSIQ 112 18a 32a
knowledge, LF was asked to describe 12 objects, six living things, six artifacts, in as much detail as he could. The method of scoring was borrowed from that used by Bozeat et al. (2003) to score delayed copy drawings (see below 2.3.2.3). Six neurologically normal control subjects were asked to define the same 12 objects in exactly the same way as LF. There was no time limit. For each object a complete list of the defining features identified by the control subjects was compiled, including the general category to which the object belonged. Only features mentioned by at least four of the six controls were retained as ‘targets’ for scoring LF’s definitions. Thus, for example, for the crocodile the description feature list comprised: animal/reptile, jaws, teeth, skin, water living, dangerous. Where included by controls, a specific feature might be accompanied by one or more modifiers to capture the specific characteristic of that feature in relation to an object. Thus again, for crocodile, modifiers included ‘‘large’’ animal, ‘‘large’’ jaw, ‘‘sharp’’ teeth, ‘‘scaly’’ skin. LF’s definitions were scored by adding up the number of appropriate target features incorporated in his description.
2.3.2.
‘Non-semantic’ tasks
2.3.2.1. SPELLING. Two spelling tests were administered: (i) The first was a 40-item ‘predictability’ spelling test compiled by Graham et al. (2000). In this test single-syllable words
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are classified as having high or low predictability spellings on the basis of frequency of phoneme-to-grapheme mapping options within the syllable (initial, medial, final). The test comprises two levels of word frequency, and the words are matched for length across conditions. In each case the experimenter dictated the word, then asked the patient to repeat it to ensure it had been heard correctly before asking the patient to write the word. A sentence using the word was offered for clarification in the case of homophones. (ii) The second consisted of the 106 object names from the Graham et al. (1994) battery as described above. Half of the items have regular spelling–sound correspondences and the other half irregular, a feature which is not especially relevant when the items are being used in the tasks of picture naming or word–picture matching but does enable assessment of the impact of this variable on either reading or (as used here) spelling. It was administered in the same way as the predictability spelling test.
2.3.2.2. READING. The short form of the surface-list reading test (Patterson and Hodges, 1992) consists of 168 single-syllable words, each from 3–6 letters in length, with 42 items in each of the four conditions formed by crossing word frequency (high vs low) and regularity of spelling–sound correspondences (regular vs irregular). The words were presented in random order and the patient was asked to read them aloud. 2.3.2.3. DELAYED COPY DRAWING. Each of 12 line drawings of familiar objects (a subset from the Hodges et al. 48-item semantic battery) was presented individually for about 5 sec for LF to study. The drawing was then taken away and he was asked to count from 1 to 15, which (like SD patients in general) he could do easily. At the end of this approximately 10 sec delay he was asked to draw the picture he had just been looking at. He was not asked to name the object, nor was it named to him at any time during the test. This test was administered at the second, fourth and fifth test rounds. Scoring was done using a modification of the method devised by Bozeat et al. (2003). The six control subjects were asked to produce delayed copy drawings of the 12 items. A list was compiled of all the individual features of each item represented in these drawings. For example, for the crocodile the features were: body, head, feet, snout, tail, eyes, skin. As for the feature list developed to score object descriptions, modifiers (e.g., curved, thin, long) captured differences in form of particular features. Thus the full feature set for the crocodile was: body – long, thin, feet – clawed, head, snout, tail – long, eyes, skin – textured. Again, only features produced by at least two-thirds of control subjects were used as the basis for evaluating the patient’s drawings. As with his verbal definitions, LF’s delayed copy drawings were scored by adding up the number of appropriate target features incorporated in his drawing. Intrusions of incorrect features were also noted. The feature lists for drawings and for descriptions differed in that, in the case of descriptions, shared category features (e.g., body, head, legs, etc.) were not explicitly stated by the normal controls unless there was something distinctive about them. 2.3.2.4. LEXICAL DECISION. This was a version of the test described by Rogers et al. (2004). It is a two-alternative forced choice
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(2AFC) test consisting of 66 pairs, each containing one real word (divided into higher- and lower-frequency sets) and one non-word. In each pair the non-word is a possible pseudo-homophone of the word. There were two typicality conditions, referring to the relationship between the word and non-word. In the Word > Non-Word condition (e.g., rim/ rimb) the word was more orthographically typical of English spelling than the non-word, operationally defined in terms of mean bi- and tri-gram frequencies. In the Non-Word > Word condition (e.g., limb/lim), the non-word was more orthographically typical than the word. The word pairs were presented one at a time, with the real word to the left of the non-word in approximately half the trials, to the right in the other half. The subject was instructed to point to the real word in each pair.
2.3.2.5. OBJECT DECISION. The test described by Rogers et al. (2003) was employed to assess LF’s object decision. As with the lexical decision task, this too was a 2AFC test consisting of 16 pairs, each composed of two line drawings. Here, one drawing was of a real animal, the other a non-real version of the same animal. The frequency manipulation here was based on familiarity ratings of the objects. The typicality manipulation, as with the lexical decision task, refers to the relative typicality of the real versus the non-real version of each object. In the Real > Non-Real condition the real animal was more ordinary or normal than the non-real version (e.g., lion with a tail > lion without a tail); in the NR > R condition the non-real animal was more characteristic of its class than the real one (e.g., gorilla with a tail > gorilla without a tail).
3.
Results
From the standard clinical neuropsychological assessment conducted at the time of presentation (see Table 1) it is clear that the deficits at that time were quite circumscribed. LF scored within normal limits on most tasks with the exception of the vocabulary sub-test of the WAIS-R, the two naming tasks, and the RAVLT, all tests requiring word production. In addition, his object definitions at that time were already greatly impoverished. In contrast, visuospatial ability and visual memory were quite superior. Together, poor performance on naming, vocabulary, word production and object definition in the absence of other cognitive deficits led to an early diagnosis of probable semantic dementia. At the time of the third test round brief assessment showed that he was still performing at an above average level on both the Block Design and Arithmetic sub-tests of the WAIS-R (age scaled scores of 18 and 12, respectively); still achieving six categories on the Wisconsin card sorting test; and both copy and delayed recall of the Rey complex figure were entirely normal. At the same time performance on semantic tasks continued to decline (see Fig. 3). At the final round, when LF was barely capable of making any meaningful utterance, he was still able to score 22/30 on the Mini-Mental Status Examination. His copy of the Rey figure remained remarkably intact although, at this final assessment, recall of the figure was impoverished. The profound impairment to semantic memory occurred therefore on the background of relative preservation
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a
semantic memory given the requirement for verbal output: here, his scores fell from only 37.6% of the maximum possible, even at the first round, to 3.5% (control mean 80.8%, s.d. 9.6). Some examples of his early responses are these:
Performance on semantic tasks
Percent correct
100 80
Peacock: ‘‘It’s a bird, found in forest areas. The male has a large tail it displays. It has a loud voice. Its tail is the largest tail of any bird.’’
60 40 20
Swan: ‘‘I think it’s a bird. It lives in the water.’’
0 1st round
2nd round
3rd round
Word-picture matching
4th round
Goat: ‘‘They’re from the horse, as far as I’m concerned, from the horse background, that’s not the right word. Farm animals, smaller than a normal horse, medium size. They were used on farms as assistants to carry things around.’’
5th round
Naming
Description to name
Naming x frequency
b Percent correct
100
Later descriptions were even more impoverished:
80
Peacock: ‘‘It’s a bird isn’t it? I think they’re a popular bird in terms of the sounds. Can’t remember what they look like. Sings, I think, unless I was thinking of another bird.’’
60 40 20
Swan: ‘‘Can’t think of anything, can’t remember what they look like.’’
0 1st round
2nd round
3rd round HF
4th round
5th round
Goat: ‘‘A goat is a farm animal, light coloured, can’t remember what they look like, farm animals. Don’t know what you get from a goat.’’
LF
Fig. 3 – Graphs showing LF’s longitudinal performance on semantic tasks: a) percent correct scores on naming, word–picture matching and description to name at each of the five test rounds; b) Naming performance on pictures with names in two frequency conditions. Controls perform at close to 100% on these tasks; in b) the dashed line represents control mean scores for lower-frequency items.
In contrast, on word–picture matching, a much less stringent test of semantic ability, his scores were accordingly much less impaired until the very last testing round. His first round score was close to that of controls (97.2% correct, compared with control mean of 99.3%, s.d. .8), had fallen at the fourth round but was still as high as 91.5%, and only dropped significantly at the final assessment 41.9%. At the last round, he frequently offered ‘‘don’t know’’ and had to be prompted to make a response. Consonant with this, there was a random character to his responses with errors from all classes of foils.
of other aspects of cognition until quite late in the disease course.
3.1.
Longitudinal investigation of semantic knowledge 3.2. Longitudinal investigation of performance on ‘non-semantic’ tasks
Over the five assessment rounds LF’s semantic knowledge deteriorated steadily. Total score for naming of pictures on the Graham et al. (1994) task declined from 65.1% to 5.7% over time (see Table 2 and Fig. 3). Naming was always substantially worse for lower frequency than for higher-frequency items. LF’s semantic impairment was even more evident in his impaired descriptions of objects in response to their spoken names. This is, of course, a particularly challenging test of
Fig. 4 shows LF’s progressive decline in spelling and reading aloud. For each task the results are presented in terms of item frequency and typicality. The graphs represent the number of correct responses as a percentage of the total number of items in that condition. The dashed line in each graph represents mean score for control subjects in the low frequency,
Table 2 – Longitudinal investigation of semantic knowledge (control means, standard deviations in brackets) Test Naming (92.5% 4.2) Word–picture match (99.3% .8) Description to name (80.8% 9.6) Scores as % correct responses.
1st round
2nd round
3rd round
4th round
5th round
65.1 97.2 40.0
66.0 90.6 29.4
45.3 96.2 17.6
36.8 91.5 12.9
5.7 49.1 3.5
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Percent correct
a
Response type as a proportion of items
Predictability Spelling
a
100
Predictability spelling
.8
80 60 40
.6
20 0
.4
1st round 2nd round 3rd round 4th round 5th round HF Reg
LF Reg
HF Irr
LF Irr .2
Percent correct
b
Spelling (Graham et al. 1994) 100 0
80
1
2
3
4
LARC
Visual/other
5
60 Correct
40 20
b
0 1st round
2nd round HF Reg
3rd round LF Reg
4th round HF Irr
5th round
Graham et al. spelling
.8
LF Irr .6
Percent correct
c
Reading (Surface List) 100 .4
80 60
.2
40 20 0 1st round
2nd round HF Reg
3rd round LF Reg
4th round HF Irr
5th round
0 1
LF Irr
Fig. 4 – LF’s longitudinal performance (% correct) on two tests of spelling (a) predictability spelling; b) Graham et al. (1994), and (c) reading aloud. In each graph the dashed line represents controls’ mean score for that task on the LF’s irregular word condition.
2
3
Correct
c
LARC
4
5
Visual/other
Surface list reading
1 .8 .6
atypical condition of the task: spelling (predictability list) 94.8%; reading aloud 95.6%. For each of these tasks LF’s performance on the low frequency, irregular items was the most vulnerable. This was so at the first testing round, and remained the case as the disease progressed. Spelling errors were most often phonologically plausible alternatives to the target: for example, his responses parashoot, sizzers, scwirral, and kanough are all plausible enough not to require specifying the target word. Occasionally LF’s errors combined phonologically plausible incorrect elements with some apparent residual knowledge of the target’s unique spelling (e.g., ‘‘bouquet’’/bokait). Fig. 5 presents LF’s spelling and reading performance with all responses classified as correct or as one of his two main types of error. LARC errors (standing for Legitimate Alternative Rendering of Components: Patterson et al., 1995) are called ‘legitimate’ alternatives because the response would be correct if the stimulus word were typical rather than atypical. Examples of LARC errors for the two tasks are as follows: in reading aloud, sew/‘‘sue’’; in spelling to dictation, ‘‘cough’’/coff (see Table 3). Visual and other errors refer to any incorrect responses that cannot be classified
.4 .2 0 1
2 Correct
3 LARC
4
5
Visual/other
Fig. 5 – LF’s longitudinal performance on the same three tasks as in Fig. 4, but here with responses assigned to one of three bins: correct, LARC errors, other sorts of error.
as LARC errors. Fig. 5 demonstrates that, over time, LF’s correct responses declined and LARC errors rose almost to equal them in the case of reading and substantially to overtake them in the case of spelling. Other types of errors remained infrequent for both tasks and at all test sessions. Performance on the delayed copy task also declined over time (see Fig. 6 for an example: LF’s delayed copy of a peacock at testing rounds 2, 4 and 5). The first time his drawing was
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Table 3 – Examples of LARC errors in LF’s spelling to dictation for the same three words ( giraffe, xylophone and silhouette) across testing rounds Round
1
2
3
4
5
Jeraf gerafe jeraph jirraph gerafe Zilophone pzylophone zilaphone zialafone zillofone Cilluet syloet siloett cillowet sellewet
assessed, at the second testing round, his score was 89.4% of the maximum possible, 61.7% at the last. This compared with a control mean of 94.5% (s.d. 3.4; range 90.9%–98.4%). Initially his drawings of artefacts (e.g., toaster, helicopter, motorcycle) were as competent and detailed as those of the control subjects. At the last testing round, these objects were no longer recognizable for the paucity of detail he was able to produce (see Fig. 7). An additional phenomenon accompanied his delayed copy of animals over time. Although there were inaccuracies, even on the first occasion that the test was administered, all of the six creatures were recognizable. In dramatic contrast, at the final round four of the animals (rhinoceros, swan, goat, crocodile) resembled one another to a remarkable degree, the distinguishing features having been replaced by generic animal heads, bodies, ears, legs and tails (Fig. 8). The crocodile lost the webbing of its feet, the swan acquired extra legs and paws and an animal’s head in place of the bird-like head and beak. The last peacock, from the same testing round (see Fig. 6), lost any remnants of bird-likeness and now had four legs, an animal head and tail. It retained something indeterminate and unusual on its back, the last vestige of knowledge of something special at a peacock’s nether end. The sixth animal tested, the lobster, also became less recognizable over time but, in the same manner as the artefacts, showing loss of detail rather than intrusion of erroneous features. This is hardly surprising, since finally LF had no idea even that a lobster was a living thing. Performance on the object and lexical decision tasks is reported in Fig. 9. Even at the last round LF made too few errors on the former task for any pattern to emerge with respect to frequency. Four of the five errors were, however, of the predicted form; that is, LF selected the more typical, non-real object in preference to the less typical real object (cow without udder, gorilla with tail, frog with paws rather than webbed feet, turtle with ears). There were far more errors in the lexical decision task with an overall decline over time from 93.9% at the second round to 57.8% at the fifth. In general, he did less well with lower than with higher-frequency items but, unexpectedly, there were some errors in all conditions. Fig. 10 displays an additional way of assessing the main question addressed by this study, namely the relative order in which deficits on different ‘non-semantic’ tasks might emerge as the semantic system deteriorates. To be more precise, what Fig. 10 represents is the order in which the predicted form of deficit on these tasks developed over time for LF, namely a disadvantage in dealing with items atypical for the relevant domain. The figure displays – for each testing round and within each task – the relative disadvantage in LF’s scores for atypical relative to typical items. Fig. 10 indicates that, relatively early in his semantic decline (Testing Round 2), LF
Fig. 6 – LF’s delayed copy drawing of a peacock at a) second test round; b) fourth test round; c) final test round. revealed the predicted effect of typicality most markedly in spelling, and to a lesser extent for reading. Over succeeding rounds the effect was present consistently for spelling and increasingly for reading, dramatically so at Round 5. By Round 5, the predicted typicality effect had emerged for the two forced
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Percent correct
a
Object Decision 100 80 60 40 20 0 1st round
2nd round
HF R>NR
Percent correct
b
3rd round
LF R>NR
4th round
HF NR>R
5th round
LF NR>R
Lexical Decision 100 80 60 40 20 0 1st round
2nd round
HF R>NR
Fig. 7 – Delayed copy of a motorcycle at test rounds 2 and 5 showing preserved draughting skill initially but catastrophic loss of detail over time. choice tasks (lexical decision and object decision) as well, such that LF now showed the predicted pattern for all four tasks.
4.
Discussion
This study reports a longitudinal investigation of a patient with semantic dementia in whom several apparently unrelated and apparently ‘non-semantic’ tasks were all compromised in
3rd round
LF R>NR
4th round
HF NR>R
5th round
LF NR>R
Fig. 9 – Scores (% correct) on the object and lexical decision tasks.
concert with the loss of semantic knowledge. The patient was a man whose pre-morbid skills, in terms of both language competence and draughtsmanship, threw into dramatic relief the deterioration of performance on semantic and ‘nonsemantic’ tasks alike. The case demonstrates that not all of these tasks need be affected at the same time, but that over time they all do become compromised. It also demonstrates that impairment on ‘non-semantic’ tasks (here, spelling in particular) can be evident even when the semantic impairment remains relatively mild. The items most likely to be affected,
Fig. 8 – Drawings of a) rhinoceros, b) goat, c) swan and d) crocodile at the final test round.
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Disadvantage for atypical items 50
Size of discrepancy (%)
40 30 20 10 0 -10 -20 2nd round
3rd round
4th round
5th round
Testing Round Object Decision
Reading
Lexical Decision
Spelling
Fig. 10 – For each testing round and task, the relative disadvantage in LF’s scores for atypical relative to typical items.
on the majority of testing occasions and tasks, were those of lower frequency and, importantly, with a less typical form in the relevant modality or mapping. And on all tasks the nature of the errors was most often to render atypical instances (e.g., words with exceptional sound–spelling correspondence) or features (e.g., animals with uncharacteristic appearance) more typical. By virtue of having been ‘caught’ so early in progression, LF displayed an unusually mild semantic deficit at the first round of testing. Patterson et al. (2006) noted that naming is the semantic task most sensitive to mild semantic impairment whereas word–picture matching is more sensitive to moderate or severe impairment. LF’s naming score at the initial assessment was the principal clue to the possibility of a semantic deficit, though there was further evidence in the already impoverished descriptions he gave in response to object names. While this task relies on the subject’s ability to verbalize, the paucity of content on the test was dramatically at odds with his conversational speech which was, until the fourth testing round, fluent, unhesitating and, even up to that point, quite richly detailed. Although this phenomenon has never to our knowledge been formally assessed, the contrast between spontaneous speech – where the patient can largely control the topic and vocabulary – as opposed to ‘responsive mode’ speech in which the experimenter calls the tune, is dramatically apparent to all clinicians and researchers who interact with SD patients. As the disease progressed, of course, LF’s semantic impairment became more noticeable in spontaneous conversation as well as much more pervasive on formal testing. Word–picture matching, in contrast, remained only mildly impaired until the final testing round. The substantial anomia paired with only rather mildly disrupted single-word comprehension (at least on a relatively easy word–picture matching task) that LF displayed over several years is characteristic of SD patients whose
anterior temporal lobe atrophy is strongly lateralised to the left (Lambon Ralph et al., 2001). Notwithstanding relatively mild semantic loss, impaired performance on one ‘non-semantic’ task, spelling, was already evident at LF’s first testing round; and Fig. 10 indicates the order in which the other deficits emerged. Whilst acknowledging the caution appropriate in drawing general conclusions on the basis of data from a single case, we derive two tentative conclusions, or hypotheses, from Fig. 10. The first reinforces and extends the conclusion of Woollams et al. (2007) concerning the association between SD and surface dyslexia: it appears that the question about these associated ‘non-semantic’ deficits in SD is not whether an SD patient will have them but only when. That is, the degree of semantic degradation that will engender impairment in reading or lexical decision or delayed copy drawing seems to vary somewhat from one patient to another (not to mention variability in the sensitivity of different tests designed to assess these cognitive abilities); but where patients have been followed longitudinally, there is as yet no indication that any of these abilities ever remains immune to semantic decline. In this regard, it is important to note that this is not a matter of globally deteriorating cognition in which everything eventually fails. Were that the case, one would have to expect that sometimes SD patients would be unable to do these tasks at all, or that the nature of their impairment would often assume a different pattern. Instead, the patients continue to perform these tasks and consistently fail only in the specific frequency-and-typicality modulated fashion revealed here for LF and for 14 other SD patients studied by Patterson et al. (2006). The second hypothesis to which LF’s data give some credence is this: although there may always remain a degree of unpredictability in the stage of semantic decline at which a particular SD patient will reveal one of these particular deficits on a particular test of the pertinent ability, the order in which the different deficits emerge may be rather more predictable, based on an analysis of the typicality structure relevant to that task. We have only limited support for this hypothesis from LF, because we have not as yet attempted a formal or quantified analysis of the systematicity in these various domains. As a result, our only serious current prediction for LF – and for other SD patients yet to be studied – was that spelling should be vulnerable sooner than reading aloud, because the mappings from sound to spelling in English are substantially less systematic than those from spelling to sound (Barry and Seymour, 1988; Venezky, 1970). There is also a little ‘circumstantial’ support for this prediction from two previous reports on spelling in SD. In the cross-sectional study by Patterson et al. (2006), every single one of the 14 patients was more impaired at spelling words with an atypical sound–spelling correspondence than at reading words with an atypical spelling–sound correspondence. And in the study of spelling and reading by Graham et al. (2000), it was striking that, until the very late stages of the disease, SD patients were substantially impaired at reading only for lower-frequency exception words, but were relatively competent at spelling only for higher-frequency regular words. This again makes good sense in terms of a systematicity comparison between reading and spelling. Take, for example, the English words
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MEET and MEAT. These are both ‘regular’ for reading: that is, despite the occasional neighbour with a different pronunciation (like THREAT), almost all words ending in –EET or –EAT are pronounced ‘‘eet’’. Thus faced with an unfamiliar written word with either of these spelling patterns (say PREET or PREAT), one would be fairly safe in saying ‘‘preet’’. But then how is one to choose between these two orthographic correspondences when given the spoken word ‘‘preet’’ to spell? LF’s performance on the delayed copy task was especially striking in view of his obvious, and highly practiced, skill as a draughtsman. Reflecting this natural talent, his early drawings, especially but not only of artefacts, were even better than those of control subjects, but there was clear decline over time. Initially, drawings of both animals and artefacts were prone to relatively minor omissions. More significant errors appeared at the later rounds. Qualitatively, too, the errors were revealing (see Figs. 6–8). His drawing of all of the objects was characterized by loss of detail to the point of their becoming unrecognizable. In the case of animals especially, there was – in addition to the gradual disappearance of distinctive, atypical features (the peacock’s tail, the webbed feet of the crocodile) – their replacement by elements more typical of the domain. The result is a visual equivalent of regularization errors in reading. Thus, for example, the peacock’s head was highly bird-like on the first occasion but looked much more like the head of a dog at the second; its feet had become paws. Finally, it resembled the other animals, with a generic animal head, four legs and a typical animal tail, and what ought to be the fan-like peacock tail has become a unrecognizable load on its back (see Fig. 6). Bearing in mind that LF had been exposed to line drawings of these objects moments before being asked to draw them, these errors are amongst the most intriguing and point to an unexpectedly prominent role for semantic knowledge in this non-verbal task. Loss of detail in LF’s delayed object copies was mirrored in his scores on the Rey complex figure test: his copy and delayed copy scores for this meaningless figure were both within the normal range on the first occasion of testing, whereas at the last he was still able to produce an elegant rendition if the model remained in view, but his delayed recall was so impoverished that it comprised just the shell of the original figure. This is not, however, to say that LF’s decline in these two delayed copy tasks had the same characteristics, and certainly not that we accord it the same interpretation. SD patients invariably have preserved performance for direct copy of both the meaningless Rey figure and meaningful drawings of real objects; and they often achieve success within the normal range (which is far from perfect: delayed recall of non-sense is difficult even for normal mortals) on delayed copy of the meaningless Rey figure, where the delay is usually on the order of 30–45 min. The one task where their performance is very discrepant from normal is briefly delayed copy of meaningful objects. As discussed at some length by Patterson (2007), this makes sense when one realises that – of the four copy tasks under discussion here (direct vs delayed, meaningful vs meaningless) – the combination of delayed and meaningful is the only one where conceptual knowledge of the content to be reproduced will inevitably affect performance. One does not need to know either that a picture represents a swan or that a swan is a bird and therefore has two legs
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in order to produce two legs in direct copy of the swan: there are the two legs in one’s direct view, demanding to be drawn. And when a normal individual has looked at a picture of a swan and of course classified it as such, he or she does not need to remember those two legs in precise physical detail to reproduce them in the delayed copy: the prior semantic classification demands that the response will have two legs. But when an SD patient like LF looks at a picture of a swan, he can neither name it nor classify it as a swan, only as some sort of generic animal. A short time later, he – just like a normal participant – will have lost substantial memory for the precise visual details of the drawing; and also just like a normal participant, his drawing will be informed (or in his case, misinformed) by his prior conceptual classification. Generic animals have four legs; thus LF’s delayed copy of the swan has four legs. This case adds to the growing body of evidence that a number of cognitive processes, not usually considered to be ‘semantic’ in their demands, nevertheless rely on the integrity of semantic knowledge for successful execution. It is a particularly striking demonstration of the ravages of semantic loss because of the robust early skills and linguistic competence of the patient; we had unusually privileged access to evidence of these, by virtue of his second ‘profession’. As a published cartoonist he had been capable of linguistic virtuosity and skilled draughting, lending particular poignancy to the loss of these talents over time. The case adds to our current understanding in demonstrating that not all tasks are equally vulnerable at the same moment in the course of the disease; and in further characterizing the ways in which degraded semantics disrupt the ability to perform so-called ‘nonsemantic’ tasks.
Acknowledgements Our very warm thanks to LF and his wife, who were unfailingly gracious and cooperative through many hours of testing over a long and, what was for both of them, in different ways, difficult time.
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