BRAIN
AND COGNITION
18,
12-33 (1992)
Short-Term Memory and Verbal Learning with Auditory PhonologicalCoding Defect: A Neuropsychological Case Study LUIGI TROJANO Fondazione
Clinica
de1 Lavoro,
Centro Medico di Campoli Monte Taburno (BN), Italy
M. T., I. R.C.C.S.,
Campoli
AND MARIA I and II Clinica
STANZIONE
Neurologica,
AND DARIO GROSSI
II Facolta’
di Medicina,
Napoli,
Italy
A patient is described with a rarely reported linguistic syndrome: he could repeat words but not nonwords. The patient produced semantic paraphasias in repetition and could read both words and nonwords flawlessly. His basic difficulties were localized in auditory phonological coding, identifying a clinical picture called “phonemic deafness.” Short-term memory and verbal learning results suggested that a standard, selective short-term memory defect can be induced by auditory phonological coding deficits as well as by “pure” short-term memory capacity limitation and other phonological deficits. Findings also provided evidence that lexical-semantic code can allow normal verbal learning. 0 1992 Academic Press. Inc.
Selective impairment of repetition and in particular of meaningless verbal material is found in syndromes such as “reproduction” conduction aphasia and “pure” STM defect (see Berndt, 1988 for a review). The inability to repeat nonsense words is occasionally associated with semantic errors in word repetition, but not with semantic paralexias and nonword reading deficits. This pattern makes up the linguistic syndrome that Morton (1980) termed “auditory parallel to deep dyslexia.” Morton, commenting on two patients with the features described above, (described by Cruse, unpublished, and by Michel, 1979), stated that similar cases could We thank Dr. G. Vallar for his helpful comments. Reprint requests should be addressed to Luigi Trojano, Fondazione Clinica del Lavoro, Centro Medico di Campoli M.T., I.R.C.C.S., 82030 Campoli M.T. (BN), Italy. 12 0278-2626192 $3.00 Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.
VERBAL
MEMORY
IN PHONEMIC
DEAFNESS
13
be found in the literature under the headings of word deafness or conduction aphasia. However, the distinctive feature of this syndrome is the coexistence of a dissociation between repetition and reading (as highlighted by Michel, 1979) and of that between word and nonword repetition, in the presence of semantic errors in repetition. Only a few such patients have been described in the literature. Goldblum (1981) described two patients using the term “auditory parallel to deep dyslexia,” and Newcombe and Marshall (1984) described a patient with the two dissociations and semantic paraphasias in repetition in the context of “modalityspecific” aphasias. Another patient was classified as a “pure word deaf” by Metz-Lutz and Dahl (1984), who localized the damage at the “prephonetic” stage of auditory input analysis and claimed that their patient improved his comprehension through lexical semantic processing. Two patients with similar features were described by Duhamel and Poncet (1986) and Katz and Goodglass (1990) under the label “deep dysphasia,” proposed by Michel and Andreewsky (1983) in a second study on the patient described by Michel in 1979. Duhamel and Poncet (1986) stated that the main linguistic deficit was in oral language decoding, specifically in phonemic perception, while nonphonological mechanisms were considered intact and probably localized in the right hemisphere. Katz and Goodglass (1990) stated that their patient had impaired nonlexical repetition and semantic processing. In this paper we describe a patient with “deep dysphasia” and discuss the possible functional impairment, assessing verbal short-term memory, which is reported to be impaired in such patients (Michel & Andreewsky, 1983; Duhamel & Poncet, 1986; Katz & Goodglass, 1990), and verbal learning. Theoretical implications will be also presented. CASE DESCRIPTION
SC. is a 33-year-old, right handed male, an electrician with 8 years of schooling. He suddenly experienced severe aphasia and right hemiparesis in July 1984. A CT scan performed 2 months later showed a hypodense area in the left temporal and parietal regions. When admitted to Clinica Neurologica, Napoli, in January 85, he had recovered motor functions but still presented language disabilities. His spontaneous speech was characterized by neologisms and phonemic paraphasias, without articulatory disturbances. His Token test score was 5/36, but he comprehended all orally presented concrete nouns. Reading comprehension was relatively spared (20/36 at Token test with written presentation, no time constraint). He was unable to read aloud, write spontaneously, or take dictation. On readmission to the clinic, in February 1987, he showed clear improvement in both spontaneous speech and comprehension. He was able to make normal conversation with few difficulties, perform written cal-
14
TROJANO,
STANZIONE TABLE
STANDARD
LANGUAGE
AND GROSS1 1
EXAMINATION
(Basso et al., 1979)
Spontaneous speech was fluent, sufficiently communicative, Naming Comprehension Words Sem. related words Simple commands Repetition Letters Syllables Words Nonwords Sentences
with some anomias.
Reading aloud (letters, syllables, words, nonwords, and sentences) Written naming Reading comprehension Words Sem. related words Sentences Writing to dictation Letters Syllables Words Nonwords Sentences Copying
85% 100% 85% 80% 20% 40% 80% 0 0 100% 85% 100% 95% 80% 30% 40% 80% 0 0 100%
culations without mistakes, and copy complex geometric shapes flawlessly. He scored 31/36 on Raven’s Coloured Progressive Matrices. The data presented in this paper were collected from February to April 1987. Language Examination
S.C.‘s spontaneous speech had became sufficiently communicative, although he presented some anomias and rare phonemic paraphasias. His performance on the Standard Language Examination (Basso, Capitani, & Vignolo, 1979) is shown in Table 1. He could comprehend all orally presented concrete nouns, but had difficulty pointing to objects named by the examiner when semantically related alternatives were given. He could cope with simple verbal commands and scored 19/36 on the Token test (De Renzi & Faglioni, 1978) with oral presentation and only marginally below cutoff score with visual presentation (28/36). He was able to read aloud both words and nonwords without errors; word repetition
VERBAL
MEMORY
IN PHONEMIC
DEAFNESS
1.5
was quite good but repetition of nonwords and sentences was impossible. His results from taking dictation showed a similar pattern and he made a few literal paraphasias in written naming. Phonemic skills and lexical decision were further investigated. Auditory
phonemic
discrimination
(Caramazza,
Miceli & Villa, 1986).
The patient was presented with 120 pairs of CCVC syllables in which the first consonant was varied. The task consisted of deciding whether two successive phonemes read aloud by the examiner were identical. S.C. performed 70% correct (85/120); errors were randomly distributed between identical and different pairs, and between markedly different (/p//g/) and phonetically similar (/t/-/d/) initial consonants (Caramazza et al.‘s normal controls made up to 10 errors). Matching task. The patient was asked to point to the stimulus read by the examiner on a list comprising three written items differing from the target by one CV syllable. Thirty four- to six-letter high-frequency words and nonwords were used. He scored 100% with words and 66% with nonwords, with nonsignificantly better performance with short items. Spelling. The patient could correctly spell orally presented words that he had understood (high-frequency bisyllabic words: 12/12) and could copy written words (20/20) and nonwords (20/20). Visual confrontation task. The patient was presented with 40 pairs of nonwords, in which each letter was printed in a different format, style, and font. The patient, when asked whether items of each pair were identical or not, scored 100%. Nonword delayed copy. The patient was presented with 30 four- to sixletter nonwords. He read each and after 10 set had to write it. He performed 86% and made six literal substitutions. Auditory lexical decision. The patient was presented with 108 words balanced for frequency, length, and grammatical class and 108 nonwords balanced for length, derived from words with one to four phonemic substitutions. Lip reading was avoided to exclude his relying on mechanisms other than auditory perception, as might a pure word deaf patient. He succeeded in recognizing 97% of nonwords as nonfamiliar stimuli, a performance significantly better than that achieved for words (56% correct; x2 = 39.6, df = 1; p = .OOOl). G rammatical class (x2 = 10.8, df = 4; p = .Ol) and word frequency (x2 = 7.4, df = 1; p = .006) significantly affected the performance, the highest error rate being for low-frequency function words and verbs. Length effect was not significant (x” = 4.9, df = 4; p = .29). Visual lexical decision. The same stimuli were presented visually. He
scored 95% for nonwords and 88% for words. As for words, visual lexical decision was significantly better than auditory task (x2 = 12.2, df = 1; p = .OOOS).Word frequency effect (x2 = 2.7, df = 1; p = .l) and length
16
TROJANO,
STANZIONE TABLE
REPETITION
OF WORDS
AND GROSS1 2
AND NONWORDS
(LIST
A)
Words N: Correct repetitions Semantic paraphasias Unrecognizable Refusals
HF 15
LF 15
13 2 0 0
10 3 0 2
Nonwords 30 0 0 12 18
Length class Errors
4 0
5 1
6 3
7 2
8 1
effect (x” = 1.5, df = 4; p = 23) were not significant, while grammatical class effect resulted in a great number of errors (8 of 13: 61%) on verbal forms. Repetition Tasks
In a standard language examination the patient was able to repeat words but not nonwords. In order to specify the repetition deficit and to ascertain whether stimulus length, word frequency, grammatical class, and concreteness could affect performance, S.C. was asked to repeat three lists of items. Material and Method Items were read one at a time by the examiner and responses were tape recorded for subsequent evaluation. Lip reading was avoided. Lists consisted of the following items: (A) Thirty words balanced for length and frequency and 30 nonwords balanced for length. (B) Ninety-eight words balanced for length, frequency, and grammatical class. (C) Forty bisyllabic words balanced for concreteness and frequency. Errors were classified as: (i) verbal paraphasia (word without a clear relation to the stimulus); (ii) semantic paraphasia (response semantically related to the stimulus); (iii) literal paraphasia (response with one or two letter substitutions); (iv) unrecognizable (response with three or more letter substitutions or a nonsense cluster of phonemes without relation to the stimulus); (v) refusal (no attempt to reproduce the item). In the case of refusal, the patient was asked to convey everything he could about the item, e.g., its length, its semantic field in the case of a word.
Results
Results are shown in Tables 2 through 4. The patient did not repeat any nonword correctly and his responses were classified as unrecognizable. He said that he could not repeat this kind of stimuli. By contrast, he repeated a high percentage of words correctly, with significant effects of
VERBAL
REPETITION
OF WORDS
MEMORY
BALANCED
IN
PHONEMIC
TABLE
3
FOR FREQUENCY, (LIST B)
Nouns
N: Correct repetitions Literal paraphasias Verbal paraphasias Semantic paraphasias Refusals
LENGTH,
AND GRAMMATICAL
Adjectives
Verbs
CLASS
Function
HF 20
LF 20
HF 10
LF 10
HF 10
LF 10
HF 9
LF 9
18 0 0 0 2
16 2 0 0 2
9 0 0 0 1
1 0 0 0 9
6 0 1 0 3
5 0 0 0 5
5 0 2 0 2
1 0 1 0 7
Length 4 5
Errors
17
DEAFNESS
5 11
class 6 6
7 7
8 9
word frequency (x2 = 27.2, df = 1; p = .OOOl) and grammatical class (x2 = 15.8, df = 1; p = .OOl). Th e influence of the concrete/abstract factor approached significance (x’ = 3.5, df = 1; p = .056). Length effect was not evident. Errors consisted mainly of refusals: 3 of 7 errors in the first list, 31/37 in the second, and 14/17 in the third one. The formalized questionnaire showed that in most cases (80%) the patient stated that he had not understood the stimulus at all. In the remaining cases he could vaguely relate the item’s semantic field. Apart from refusals, most errors were semantic paraphasias: 4 of 7 errors in the first list and 3/37 in the second (for instance: “braccio” arm instead of “mano” hand). Moreover, he made four verbal paraphasias in the second list: one derivational error (“serviti” served instead of “servire” to serve) and three function word substitutions. Finally, there were only two literal paraphasias, both in lowfrequency nouns in the second list.
TABLE REPETITION
OF BISYLLABIC
WORDS
BALANCED
4 FOR FREQUENCY
AND CONCRETENESS
Concrete
N: Correct repetitions Semantic paraphasias Refusals
(LIST
C)
Abstract
HF 10
LF 10
HF 10
LF 10
9 1 0
5 0 5
8 0 2
1 0 9
18
TROJANO,
STANZIONE
AND GROSS1
Comment on Case Description
S.C. showed semantic paraphasias in repetition and the selective impairment of nonword repetition in the absence of written language deficits, typical of “deep dysphasia. ” The dissociation between word and nonword repetition can also be found in patients with phonological disturbances, in whom the damage is thought to lead to the selective disruption of the automatic nonlexical recoding of verbal input into an articulatory code (Friedrich, Glenn, & Marin, 1984). S.C. differed from such patients in being fully capable of reading words and nonwords, of written and oral spelling, of visual confrontation of nonwords, and of writing nonwords he had read after a lo-set delay. His functional impairment seemed to be restricted to the perceptual analysis of auditory verbal input, with spared grapheme-to-phoneme conversion and phonological manipulations. Basic difficulties were observed in phonemic discrimination and identification (nonword matching task). S.C.‘s auditory comprehension, and the successive oral or written reproduction of auditory stimuli, seemed to be based on his relatively preserved lexical access. S.C. clearly stated that he could repeat only those stimuli that he could understand, i.e., which had access to the lexicon. Furthermore, in auditory lexical decision the patient tended to reject all stimuli that he could not recognize quickly and certainly. Overall “no” responses, i.e., correct rejections and misses (69%), were significantly more frequent than “yes” ones, i.e., correct word identifications and false alarms (x2 = 29.9, df = 1; p = .OOOl), and he had a high rate for nonwords. On the other hand, the hypothesis that the repetition performance was mainly determined by lexical access in the absence of auditory phonological coding is supported by the observation that both lexical decision and repetition were significantly affected by word frequency, part of speech, and concreteness. The most parsimonious interpretation of S.C.‘s linguistic features and repetition would be a selective deficit in auditory phonological coding or, in other words, the inability to perceive elementary speech sounds and to associate adequate phonological representations with them. This picture was called “phonemic deafness” by Duhamel and Poncet. A deficit in phonemic discrimination was suggested to be due to unilateral left temporal lesions in word deaf patients (Auerbach, Allard, Naeser, Alexander, & Albert, 1982), but this observation referred to the general impairment of speech sound analysis at a prephonetic stage. Here “phonemic deafness” refers to the selective inability to analyze step-by-step auditory input and to associate sounds with phonemic representations, while “global” lexical processing of auditory stimuli is spared. In synthesis, “phonemic deafness” appears to be a specific deficit of auditory phonological analysis, in patients whose internal phonological representations and processes are
VERBAL
MEMORY
IN PHONEMIC
DEAFNESS
19
spared, and in whom the direct access to the auditory lexicon is preserved. In this sense the “phonemic deafness” appears distinct both from “reproduction” conduction aphasia, in which a disruption of internal phonology is found, and from pure word deafness, in which analysis of auditory speech sounds is generally defective and in which auditory comprehension is not affected by the grammatical category or the concrete/abstract dimension (Michel & Andreewsky, 1983). SHORT-TERM
MEMORY TASKS
S.C. offers the opportunity of studying verbal memory in the context of a very selective impairment of auditory phonological input analysis without a general disruption of phonological skills. In this sense, patients with “phonemic deafness” represent a different source of information from patients with different language disorders whose short-term memory has been widely studied in the literature (“absence of phonological coding,” i.e., impaired phonemic skills, Martin & Caramazza, 1982; selective “nonword processing impairment” despite good phonological skills, Bisiacchi, Cipolotti, & Denes, 1989; conduction aphasia in its classical definition, Friedrich et al., 1984; Martin, 1987; verbal short-term memory deficit, Saffran & Marin, 1975; Caramazza, Basili, Koller, & Berndt, 1981). This study will focus on conventional memory span for verbal and visuospatial material, immediate serial recall for visual versus oral presentation of verbal material, rate of forgetting, and primacy and recency effects. Spatial and Verbal Span
The first assessment of short-term memory was the measure of spatial and verbal span. Material and Method Spatial span was assessed on Corsi’s block tapping task, given according to standard criteria (Orsini, Grossi, Capitani, Laiacona, Papagno, & Vallar, 1987). Verbal span was assessed as a function of modality of presentation and type of material. The patient was auditorily presented with lists increasing in length from one to six items. Lists were made up from five sets of high-frequency nouns: digits (from W.A.1.S); bisyllabic concrete words; trisyllabic concrete words; bisyllabic abstract words; CV syllables. For visual presentation, only digits, bisyllabic concrete words, and CV syllables were used. The patient attempted immediate serial recall of three lists at each level and proceeded to the next level if he could recall correctly one of the three lists.
Results
S.C. showed a selective deficit of verbal short-term memory and had a spatial span well within the normal range (Table 5). On auditory presentation he showed a slight facilitation with digits and concrete words,
20
TROJANO,
STANZIONE TABLE
IMMEDIATE
AND GROSS1 5
MEMORY
SPAN
Corsi’s block tapping task
6
Auditory verbal span for Digits Concrete bisyllabic words Concrete trisyllabic words Abstract bisyllabic words Visual verbal span for Digits Concrete bisyllabic words Graphemes
2 2 1
regardless of their length. Fewer orally presented abstract words and CV syllables were recalled as expected given the patient’s repetition ability. S.C.‘s impression of relative ease with visual presentation was not supported by span data: his recall rate was similar for orally and visually presented digits, concrete words, and CV syllables. Verbal Immediate
Serial Recall
To further investigate the effects of visual versus oral presentation, and the influence of part of speech effect, the patient was given a serial recall task of supraspan sequences. This task was devised to obtain more precise measures of immediate verbal memory independent of the repetition deficit . Material and Method Twenty three-item series from each of three sets of words (bisyllabic high-frequency concrete nouns, abstract nouns, and function words) were visually presented. Twenty series of three concrete nouns from a pool of nouns the patient was able to repeat were then presented orally. The number of sequences correctly recalled, the number of items recalled in correct serial position, and the overall number of items recalled were scored separately. TABLE IMMEDIATE
N: Auditory concrete nouns Visual concrete nouns Visual abstract nouns Visual function words
SERIAL
RECALL
6
OF THREE-ITEM
SEQUENCES
Sequences 20
Items in correct order 60
Overall correct items 60
1 14 10 10
15 48 36 40
39 52 47 46
VERBAL
MEMORY
IN PHONEMIC TABLE
RATE
OF FORGETTING
RESULTS
Words
7 (THREE-WORD
in correct
order
Position correct
Delay
(set)
N:
Sequences 20
0 3 6
1 2 0
21
DEAFNESS
LISTS)
Overall
correct
Serial
position
words
1 20
2 20
3 20
Total 60
1 20
2 20
3 20
Total 60
7 10 3
8 7 6
3 2 0
18 19 9
12 15 8
13 12 10
15 9 10
40 37 28
Results Results are shown in Table 6. This time, a clear-cut advantage of visual presentation appeared for concrete nouns, and the overall score was also significantly higher for visual modality (x2 = 38.7, df = 1; p = .OOOl). In visual modality, the type of material did not influence the number of sequences correctly recalled (x’ = 2.7, df = 2; p = 0.2) nor the overall number of items recalled (x2 = 2.2, df = 2; p = 0.3). Rate of Forgetting The patient’s immediate memory for auditory stimuli with articulatory suppression was further examined by means of serial recall with two different delay conditions. Material and Method Sixty series of three items were made up from the same set of concrete nouns as in the previous task. The patient had to repeat 20 series immediately after the presentation, 20 after an interval of 3 set, and 20 after an interval of 6 sec. During intervals the patient was requested to articulate irrelevant material. The number of sequences correctly recalled, the number of items recalled in correct serial position, and the overall number of items recalled were scored separately. Furthermore, item recall as a function of serial position was considered.
Results As seen in Table 7, short-term memory impairment was confirmed by the first task (without delay): The score was similar to that obtained in the previous task. The patient’s recall rate was similar in the task with the 3-set delay but was lower with the 6-set delay. In all conditions a high discrepancy was observed between the number of items recalled in correct serial position and the overall number of items recalled: Summing results over delay conditions, the patient was able to recall 44 items in correct serial position versus 104 total recalls. This discrepancy was more
22
TROJANO,
4oo
STANZIONE
1
2
3
1
AND GROSS1
5
6
7
0
9 10
Serialposition FIG. 1. Immediate free-recall curve. Patient S.C. could recall only some items from first serial positions and did not showed recency effect at all.
pronounced than that observed for visual modality in the previous task (124 items in correct position of 144 total recalls). Across serial positions, no marked effect was found but the relevant drop for the last position, when items recalled in the correct order were considered. Verbal Free-Recall Curve
In the previous task, final items tended to be recalled less accurately. This finding can be taken as an index of lack of recency effect (Vallar, Basso, & Bottini, 1990). However, the most appropriate method for studying primacy and recency effects is the free-recall curve for supraspan sequences, in which no order-recall constraint could influence the performance. Material and Method Ten series of 10 bisyllabic concrete nouns were presented orally, and the patient was asked to recall as many words as he could, in whatever order, immediately after each presentation.
Results
Results are shown in Fig. 1. Overall performance was poor, as could be expected in view of previous test results: only 1.7 items per list. Almost all items recalled were presented in the first three serial positions (82%), while no item was recalled from the final three positions. Comment on Short-Term
Memory
Task Results
The patient showed an impairment of verbal short-term memory. Immediate serial recall showed a clear advantage for written over oral presentation and a significant effect of grammatical class for the latter, even with items the patient could repeat flawlessly. With oral presentation the patient was unable to retain order information and did not present recency effect. Visual superiority and lack of recency effect for auditory presentation are considered typical of pure STM patients (Warrington & Shallice,
VERBAL
MEMORY
IN PHONEMIC
DEAFNESS
23
1969; Warrington, Logue, and Pratt, 1972; Shallice and Butterworth, 1977; Basso, Spinnler, Vallar, & Zanobio, 1982). The impairment of auditory phonological coding could thus induce a typical short-term memory defect. On the other hand, short-term memory results suggest that S.C. did not use a phonological code in auditory modality. First, part-of-speech effect in serial recall is somewhat inconsistent with phonological coding. Furthermore, rate of forgetting results suggested that the performance relied on a code: (i) sufficient to maintain verbal items only up to 3 set without decrement, (ii) not capable of retaining order information, and (iii) not related to recency. Correct serial recall has been thought to reflect efficient input phonological coding (Martin & Caramazza, 1982). On the other hand, recency effect has been thought to reflect an STM component of verbal memory (Glanzer, 1972) and was recently interpreted as the output of a phonological buffer (Bisiacchi et al., 1989). Therefore, the lack of recency found in immediate serial recall, and especially in the free-recall curve, together with all the other results, suggests that S.C. was using a nonphonological code, probably related to lexical-semantic processes, rapidly fading and insufficient to retain order information. It should be noted that features of auditory memory tasks did not parallel those observed in the visual modality, where grammatical class effect was not found, and order information and recency effect were better maintained. These data suggest that the patient was relying on a code different from that used in auditory memory tasks. However, it is not possible to specify whether it was visual in nature, as hypothesized in patients with selective immediate memory deficit (Basso et al., 1982) and in those with phonological disabilities (Campbell & Butterworth, 1985). As S.C. was able to read items and manipulate phonological representations, better preserved order information for visual presentation might be related to the generation of phonological representations of written items. VERBAL LEARNING TASKS
The assessment of verbal learning in patients with selective deficits of auditory phonological coding is of interest for two reasons. It could provide additional evidence for the above hypothesis that the “phonemic deafness” induced an STM defect similar to that of pure STM patients. An auditory verbal learning task could also explore the effect of lexical-semantic coding and strategies in entering new material into LTM. The patient was given a verbal learning test with four conditions differing in memory load and semantic content. Material and Method Four lists of 10 high-frequency (A) Bisyllabic concrete nouns;
items
comprised:
24
TROJANO,
STANZIONE
AND GROSS1
TABLE 8 NUMBEROF TRIALS TO REACH LEARNING CRITERION Controls
Bisyllabic Trisyllabic Bisyllabic Bisyllabic
Patient S.C.
Mean
Range
6 7 10 14
4.2 4.5 7.2 9.1
3-6 3-7 5-9 6-13
concrete nouns concrete nouns abstract nouns function words
(B) Trisyllabic concrete nouns; (C) Bisyllabic abstract nouns; (D) Bisyllabic function words. The examiner read each list, one per session, in the order above and at the standard rate of one item/set, and the patient was asked to recall as many words as possible immediately after the presentation, without any order constraint. Each list was repeated until the patient was able to recall all 10 items two consecutive times. The number of trials S.C. needed to do so was compared to that of five normal subjects matched for age and education.
Results As it can be seen in Table 8, S.C. reached learning criterion for concrete bi- and trisyllabic nouns at a comparable rate and well within the normal range (Fig. 2). He was slightly slower with abstract nouns, although still in the normal range. However, S.C. was slower than all normal subjects in learning function words and he was able to recall 9 of 10 items correctly and consistently only after 14 trials (Fig. 3). He could not recall the 10th item, but gave some related responses (“maniera” manner, “mode” way, instead of “come” how). In all four tasks he started with fewer items recalled than control and rapidly improved his performance. BISYLLABK CONCRElENOUNS
‘IXISYLLABICaNCRETE NOUNS
FIG. 2. Learning of auditorily presented lo-item lists of concrete nouns of different length. Patient S.C. could recall less items than controls in early trials, but he reached learning criterion at a normal rate.
VERBAL
MEMORY
IN PHONEMIC
DEAFNESS
25
FUNCTION WORDS
ABStRACTNOUNS
,I
12
TlidS
TlidS
Learning of auditorily presented lo-item lists of words with different semantic content. Patient S.C. was less efficient than controls throughout the task, particularly with function words. FIG.
3.
Comment on Verbal Learning
Task Results
S.C.‘s normal learning ability was affected by semantic content but not by word length. These features paralleled those found in auditory lexical decisions and repetition and suggest that verbal learning also relied on a nonphonological code. This does not only mean that the patient could not phonologically analyze speech sounds, but also that the lexical-semantic code has some properties inherent in verbal learning tasks. This lexical-semantic code allowed memorization of words with high semantic content, but reached full efficiency only after several repetitions. On the other hand, verbal learning results add further support to the hypothesis that in this patient “phonemic deafness” induced a classical picture of short-term memory defect. DISCUSSION
This paper reports on a patient with the linguistic picture of “deep dysphasia.” His specific functional impairment was restricted to auditory phonological coding, in a way that closely resembles so-called “phonemic deafness” (Duhamel & Poncet, 1986). We will not discuss whether phonemic deafness is present in all deep dysphasics. However, it is likely in Metz-Lutz and Dahl’s (1984) patient and possible in Michel and Andreewsky’s (1983) and Katz and Goodglass’ (1990) patients, whose auditory phonological coding processes were not specifically investigated. “Phonemic deafness” is selective functional damage not exclusively related to this syndrome. Vallar et al. (1990) report the case of E.R., a patient with deficit of auditory phonological analysis but without deficit of auditory processing of speech input. That report includes no quantitative data about the patient’s repetition of words and nonwords, but phonological discrimination of stop-consonants was defective, while the patient could repeat series of two to four words, with clear effects of
26
TROJANO,
STANZIONE
AND GROSS1
lexical-semantic factors. The only qualitative difference between that case and ours seems to be that our patient made semantic paraphasias in repetition. The source of our patient’s semantic paraphasias is not clear. The above case and that described by Beauvois, Derousne’, and Bastard (1980) suggest that the lack of phonological coding is not sufficient to produce semantic paraphasias in repetition; accessory lexical disorders could be postulated (Katz & Goodglass, 1990; Caramazza & Hillis, 1990). However, we have only weak evidence of lexical difficulties in S.C. (some semantic confusions in auditory word comprehension). From a theoretical point of view, the selective impairment of nonword repetition is consistent with models implying at least two distinct pathways of repetition. One such model has been proposed by Friedrich et al. (1984). On the basis of the double dissociation of auditory comprehension and repetition found in conduction aphasics confronted with echolalic aphasic patients, Friedrich et al. postulated a “direct auditory-articulatory link” for repetition of meaningless verbal stimuli, distinct from the lexical route. The existence of “phonemic deafness” throws a different light on the matter. It implies that auditory input is processed by functionally separated routes: two processing routes also present at the input stages. This idea is not consistent with Friedrich et al.3 model (1984) or with other two- or three-route models of repetition and speech production (McCarthy & Warrington, 1984; Katz & Goodglass, 1990), in which routes separate after input analysis. By contrast, parallel processing of auditory input is supported by experimental studies on speech perception: recently, Wioland, Metz-Lutz, and Brock (in press) have demonstrated the interaction of on-line phonemic and lexical analyses in tasks of CV syllable monitoring. To address the issue of a general model of speech perception, more detailed investigations are needed and they would also have to account for related findings, such as the possible dissociation between accurate auditory phonological information and semantic access (wordmeaning deafness: Ellis, 1984; Kohn & Friedman, 1986). Our findings can only reveal a selective damage of auditory phonological analysis and infer that in normal subjects this works in parallel with lexical processes. “Phonemic
Deafness” and Verbal Memory
Our findings have relevant implications for memory models. S.C. had a verbal immediate memory defect identical to that of pure STM patients, supported by normal verbal learning. Indeed, the inversion of the usual modality effect in immediate verbal memory found in S.C. and STM patients has also been described in patients with “phonological disabilities” (Martin & Caramazza, 1982; Butterworth, Campbell, & Howard, 1986) and conduction aphasia (Freidreich et al., 1984; Martin, 1987). Furthermore, lack of recency effect has been found in patients with phonological impairment (Martin & Caramazza, 1982; Bisiacchi et al.,
VERBAL
MEMORY
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1989). In other words, two main features of S.C.‘s short-term memory, visual superiority and lack of recency effect for auditory presentation, are shared with patients whose functional impairment has been considered different. To summarize, (i) the selective damage to auditory phonological analysis, as in the present case and in Vallar et al.‘s patient E.R.; (ii) disorders of internal phonological representations (“absence of phonological codconduction aphasia: ing”: Martin & Caramazza, 1982; “reproduction” Friedrich et al., 1984; Martin, 1987), even with preserved phonological awareness (Bisiacchi et al., 1989); (ii) selective STM deficit without phonological impairment (Warrington & Shallice, 1969; Saffran & Marin, 1975; Basso et al., 1982; but also Caramazza et al., 1981); all these different linguistic syndromes converge into a similar STM deficit with consistent features. One wonders whether these syndromes can really be considered different. Apart from difficulties in classifying patients (see for example the distinction between “reproduction” conduction aphasia and “pure” STM defect; Shallice & Warrington, 1970), most case reports differ in historical and theoretical perspectives, so that results are not easily comparable. For example, phonemic discrimination and internal manipulation of phonemic representations were not investigated in all patients, and only indirect evidence can be collected. Nonetheless, it seems possible to group patients according to the sketchy, functional distinction suggested above: patients with a selective impairment of auditory phonological analysis (like S.C.); patients with difficulties at some level of internal phonological processes; and patients without such perceptual or “inner” phonological defects but with a pure capacity limitation of STM. A second question is whether S.C.‘s impaired phonemic discrimination and nonword repetition and writing could be caused by the memory defect. Pure STM patients also had some difficulty in repeating and writing nonwords to dictation (cited by Bisiacchi et al., 1989). However, the immediate memory defect does not necessarily produce errors in repeating even single letters or trigrams (Vallar & Baddeley, 1984a; Baddeley, Vallar, & Wilson, 1987), and our tasks were devised to minimize memory load (auditory phonetic discrimination and nonword matching). Therefore the answer to this question is no. Furthermore, visual superiority and lack of recency found in the three classes of patients mentioned above cannot be thought of as nonspecific consequences of an STM defect. Actually, opposite patterns of STM defect do exist in nonfluent aphasic patients (preserved recency and superiority of auditory over visual modality; Martin, 1987) and in sensory transcortical aphasics (preserved recency and no primacy; Martin & Saffran, 1990). Consequently, and also on the basis of De Renzi and Nichelh’s (1975) claims, we think that STM is better conceived as an independent area, whose structure and processes can be specifically and differentially damaged.
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To address this issue, one must accommodate the consistent performance of different types of patients within a coherent STM theoretical framework. An elaborated framework of STM is working memory, which is composed of a limited-capacity supervisory system (central executive) and a number of “slave” systems (Baddeley & Hitch, 1974; Baddeley, 1986). The “slave” system which processes verbal material is called the “articulatory loop,” and it has been divided into two components: a passive input store (phonological store, PS), in which phonologically coded phonemes are held, and an active rehearsal process (articulatory rehearsal, AR), which continually refreshes traces contained in PS. The distinction between AR and PS received primary neuropsychological support from Vallar and Baddeley (1984b) in a study on a patient with a pure STM deficit. They claimed that this deficit was restricted to the impairment of only one component, the phonological store, and thus characterized a clinical syndrome on the basis of a psychological model. The hypothesis of a selective PS impairment in this STM patient accounted for the superiority of visual versus auditory presentation and also for the lack of recency effect (Vallar & Papagno, 1986). Visual superiority and lack of recency effect have been considered the hallmark of a selective PS impairment in further studies, as well as in that conducted by Martin (1987). Martin studied a conduction aphasic and contrasted his performance with that of six nonfluent aphasics. On the basis of visual superiority and lack of recency effect, and in keeping with other related data, Martin claimed that the conduction aphasic showed the same PS impairment as Vallar et al.% patient (1984b), while the nonfluent aphasics showed an opposite pattern and were diagnosed as affected by AR damage (Martin, 1987). In this light, S.C. can also be said to show a PS impairment, even though data about phonological similarity effect in immediate memory (considered as specific to PS functioning) are not available. This common functional damage seems to be shared by patients showing both “inner” phonological problems and pure STM capacity limitation, but also by patients with auditory phonological analysis defect such as S.C. and Vallar et al’s patient E.R. If they all have a PS defect, it would follow that PS can be selectively damaged by different mechanisms. The first, and best known, is the so-called capacity limitation (pure STM defect); another, found in S.C., is the impossibility of generating from auditory input the representations which PS is able to hold; a third mechanism is due to a deficit in operating upon phonological representations held in PS. The hypothesis of alternative mechanisms of PS damage, entirely based on the working memory model, would explain the STM defect in the three types of patients. A similar hypothesis is expressed by Vallar et al. (1990), who identify primary deficits of PS, due to capacity limitations, and secondary PS deficits, due to phonological processing disorders. S.C. could be included in this “secondary” type of PS deficit, with the observation that
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his deficit is caused by impairment of auditory phonological analysis, different from a “secondary” deficit due to “inner” phonological disorders. In terms of working memory, the possibility of AR damage could also be explored, but necessary data (phonological similarity with visual presentation and length effect on immediate memory tasks) are not available for our patient, and a “secondary” PS deficit could entirely account for his performance. PS and phonological analysis impairments could presumably occur independently or be associated in one patient. In other words, auditory phonological analysis defect may not necessarily entail a PS impairment. This possibility could only be ruled out by further observations of phonological analysis skills and STM in terms of working memory, showing opposite patterns of impairment. Data available on Vallar et al.‘s patient and our patient suggest that these necessary relationships do exist and imply a serial organization in which “the output of phonological analysis is the input to PS” (Vallar et al., 1990). As stated above, S.C.‘s normal learning capacities support the idea that “phonemic deafness” implies a memory defect very similar to the selective verbal STM impairment first described by Warrington and Shallice (1969)) notwithstanding the different functional impairment and the distinctive features identified in this study. The STM patient described by Basso et al. (1982) and subsequently by Vallar and Baddeley (1984b) and by Vallar and Papagno (1986) could learn 10 familiar bisyllabic words after five attempts, but was unable to learn nonsense words in a paradigm of pairedassociate learning (Baddeley, Papagno, & Vallar, 1988). The patient could learn material which could be lexically or semantically coded, but failed when accurate phonological representations of stimuli were requested. These findings showed that phonological store was not necessary in learning familiar words, but became crucial with new material. Our findings are entirely consistent with these observations: auditory analysis of nonsense material was impossible, but the use of words with different semantic content verified lexical-semantic effects on verbal learning, in keeping with Baddeley et al.3 findings (1988). In conclusion, verbal learning results suggested that S.C.‘s linguistic damage apparently caused a true STM defect, which can be conceptualized in terms of the working memory model, but not as the well-known capacity limitation. However, it must be remembered that S.C.‘s residual STM performance, which was characterized as mainly based on a lexical-semantic code, is difficult to explain in terms of this model, which assumes that verbal STM relies almost exclusively on phonological coding. As for S.C.‘s normal learning abilities, we suggest that they relied on a lexical-semantic code which allowed normal, albeit slower, learning of words with high semantic content. Although S.C. was unable to make an adequate auditory phonological analysis, his slower acquisition of items in first trials could be the result of “slower” lexical-semantic coding, which on its own can allow verbal
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learning in the absence of other cognitive deficits. This provisional explanation cannot be supported by other studies of patients with phonological disabilities and STM defect, because verbal learning has rarely been studied in such cases. However, it is consistent with findings of normal verbal learning in Vallar et al.‘s patient E.R., who showed similar deficits in auditory phonological analysis, and in Bisiacchi et al.‘s patient (in press), who had a phonological deficit not clearly localized at input or output stages of language processes. From another point of view, Baddeley (1966) found that acoustical similarity significantly affected verbal learning in normal subjects, but that its detrimental effect declined over consecutive trials. Baddeley interpreted these findings as reflecting the role of auditorily based short-term memory in verbal learning. Findings in S.C., who had an auditory phonological analysis defect, confirm that long-term memory relies extensively but not exclusively on lexical-semantic coding and that phonological shortterm memory has a definite role in the early stages of learning. CONCLUSION
The patient reported here was affected by a rarely reported repetition disorder due to a highly selective impairment of auditory phonological coding. Our findings suggest that auditory phonological analysis and auditory lexical-semantic analysis are parallel processes and can be selectively impaired. A comprehensive model of speech perception could not be formulated on the basis of this case study, but our hypothesis finds support in other clinical neuropsychological and experimental findings, although it is not considered in many recent linguistic models (for example Hillis & Caramazza, 1989). We suggest that different mechanisms can produce a similar specific defect in different types of patients. In particular, we interpret our findings on the basis of a working memory model, whose precise characterization has allowed identification of the defect of a subcomponent (PS) in the patient reported here. On the other hand, these findings corroborated the idea that phonological STM plays a definite role in the first stages of verbal learning, interacting with the slower lexical-semantic processes. Specific theoretical inferences have been allowed by the progressive specification of cognitive models, in which every structure is put in close relation with certain behavioral manifestations. On this basis, the investigation of relationships among processes and structures of different cognitive areas appears to be a very fruitful perspective. REFERENCES Auerbach, word
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