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Auditory-verbal short-term memory impairment and conduction aphasia
BRAIN
AND
LANGUAGE
4, 479-491 (1977)
Auditory-Verbal Short-Term and Conduction TIM SHALLICEAND
Memory Aphasia
Impairment
ELIZABETH K. WARRINGTON
National Hospital, London The specific impairment of performance on repetition tasks has classically been identified with conduction aphasia. It is argued that this impairment can be subdivided and a deficit in span performance distinguished from that of the reproduction of single words. An explanation of the span deficit in terms of auditory-verbal short-term memory is preferred to hypotheses involving disconnections or damage to order retention systems. It is shown that a short-term memory component is present in many patients previously classified as conduction aphasics.
It is now widely believed that conduction aphasia exists as a syndrome, distinct from both sensory and motor aphasia. It is a syndrome in which verbal repetition is selectively impaired with spontaneous speech being relatively preserved and comprehension apparently intact.’ While it is held by some that conduction aphasia is a form of expressive aphasia (Dubois, HCcaen, Angelergues, Maufras, Du Chatelier, & Marcie, 1964), in fact patients classified as conduction aphasic have had a variety of different deficients of spontaneous speech (Benson, Sheremata, Bouchard, Segarra, Price, & Geschwind, 1973). The most commonly accepted cardinal symptom is a gross defect of repetition. However, the term “repetition” has been used relatively loosely in the literature to cover repetition of individual words, of individual nonsense syllables, of meaningless polysyllables, of unconnected sets of words (word span including digit span), of more than one nonsense syllable, and of phrases and of sentences. For theoretical reasons, to be discussed later, we will distinguish between repetition of a single relatively infrequent multisyllabic word (to be called “reproduction”) and of a number of unconnected short familiar words (to be called “repetition”). We will argue that the former task imposes stress on a different process from the latter. Theoretically, the distinction may be conceptualized terms of the distinction between the ability to produce and the ability retain an ordered set of verbal units.
in to
We should like to thank Dr. R. T. C. Pratt for his helpful suggestions on the manuscript. Requests for reprints should be addressed to Dr. Tim Shallice, National Hospital, Queen’s Square, London, W.C. 1. England. I The term syndrome is used in the sense of a collection together.
479
of symptoms regularly
occurring
480
SHALLICE
AND WARRINGTON
Most clinical investigations of conduction aphasia have not separately assessed production and retention of verbal units. Experimental studies have, however, recently tended to be of “repetition” as defined above and have provided a much more systematic body of data on conduction aphasia than was previously available. However, this greater uniformity of method has not led to any uniformity of theoretical position. Indeed, from investigations of repetition, four different theories of conduction aphasia have recently been supported. In a series of investigations of a patient, KF (Warrington & Shallice, 1969, 1972; Shallice & Warrington, 1970, 1974), we argued that a specific failure on repetition tasks exists which arises from a difficulty of auditory-verbal short-term memory. Further research showed that the deficit of three other patients could be interpreted in the same terms (Warrington, Logue, & Pratt, 1971; Saffran & Marin, 1975). Our position has been questioned by Kinsbourne (1972), Tzortzis and Albert (1974), and Strub and Gardner (1974), who have studied forms of conduction aphasia which they argued do not arise from a deficit of auditory-verbal short-term memory (STM). Kinsbourne argues in favor of a modern version of Wernicke’s (1874) disconnection hypothesis [also supported by Geschwind (1965)] in terms of a pathologically limited channel between the auditory-verbal STM system and the “imitative response program.” He considers that this pathological limitation can arise in two different ways. It can result from the use of a damaged left arcuate bundle (which connects Wernicke’s area with Broca’s area); alternatively, extensive left hemisphere damage can, in his view, lead to a release of the language mechanisms of the right hemisphere from inhibition. Following Kleist’s (1916) suggestion, he proposes that “the right temporal lobe compensates for the left but then has to utilize the imperfect speech programming mechanism of the right hemisphere having no ready access to the intact Broca’s area on the left.” Tzortzis and Albert hold that the basic disorder of conduction aphasic patients lies in the “disorganization of the execution of a particular encoded programme” in the speech production process, which Dubois et al. (1964), the originators of the theory, term “an aphasia of the first articulation, i.e., groups defined by the plans of the morpheme or the phrase.” Tzortzis and Albert argue that “essential to this hypothesis is the implied contention that there is a marked deficiency in the memory for the specific sequential order of the items to be repeated.” The final approach is that of Strub and Gardner (1974). They assume that the difficulty arises after phonological analysis of the auditory input has been performed and some trace held for further processing. At this point they argue that the conduction aphasic “can proceed to extract its meaning and/or synthesize its phonemic components for eventual articulation,” but these processes are performed with reduced efficiency and
SHORT-TERM
MEMORY
AND CONDUCTION
APHASIA
481
may be mutually interfering. In particular, the repetition difficulty arises from “an impairment in proceeding from a phonological analysis to the selection and combination of target phonemes.” One problem with assessing these theories is that it is unclear how far they are reformulations or actually substantively different. Thus, Strub and Gardner’s explanation of repetition difficulty, depending on the emphasis one gives to their wording, could be equivalent to either Kinsbourne’s or Tzortzis and Albert’s position. Furthermore, while Kinsbourne’s theory seems to be in conflict with that of Tzortzis and Albert, it does not appear to be necessarily incompatible with the theory of Dubois et al., of which Tzortzis and Albert’s theory is supposed to be a reformulation! However, we will assume that the theory of Dubois et al. refers to a deficit in a system which receives input from the conduction pathway or pathways that Kinsbourne argues are damaged. A similar point concerns Strub and Gardner’s attempt to contrast linguistic and mnestic theories. We have argued that the function of auditory-verbal short-term memory is specific to speech processing (Shallice & Warrington, 1970, 1974; Shallice, 1975). In fact, on a theory such as Morton’s (1970) in which the main auditory verbal short-term memory store is a Response Buffer, the auditory-verbal STM theory could become equivalent to the theory of Dubois et al. We, however, will argue that the auditory-verbal STM is an input store. A second problem is that there is considerable doubt in the literature over whether all of the patients labeled as conduction aphasic have the same functional deficit. We, ourselves, for instance, have modified our position on this matter (see Warrington & Shallice, 1969; Warrington et al., 1971). In this paper we will argue that there are at least two theoretically separable functional deficits corresponding to specific difficulties on the repetition and reproduction tasks, respectively, the former involving auditory-verbal STM and the latter involving the speech production process. This view might seem to resolve much of the conflict in the literature since it could be argued that the different explanations could be referring to different types of patient. However, the situation is, in fact, more complex. Most of the tests performed in all of the recent investigations have involved repetition (which would be the STM type of test) and from this Kinsbourne, Tzortzis, and Albert, and Strub and Gardner have all concluded that their patients do not have STM difficulties. Moreover, two (Kinsbourne and Strub & Gardner) suggest that their theories would explain the repetition defects of our patients. We consider that both of these types of argument are incorrect and that in only one (or possibly two) of these patients is there evidence that their repetition (as opposed to reproduction) deficits do not arise from an STM deficit. As these authors tend to produce evidence which they consider supports their theory and is in
482
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AND WARRINGTON
conflict with a STM approach, we will present our arguments similarly. After reviewing the evidence on repetition tasks for the non-STM theories, we will consider the deficits of reproduction. We begin, however, with a brief discussion of the STM theory. THE STM APPROACH
By the late 196Os,it was widely accepted by cognitive psychologists that memory systems exist which only hold information over short intervals of time and, in particular, that performance on verbal memory tasks involved at least one STM system as well as a long-term memory (LTM) system (Waugh & Norman, 1965; Atkinson & Shiffrin, 1968). Evidence for this conclusion was derived from a number of different sources (see Baddeley, 1976). For instance, material retained over different periods of time seems more affected by different sources of interference: acoustic over short intervals, semantic over long (Baddeley, 1966; Kintsch & Buschke, 1969). In addition, a number of different tasks were found in which the STM and LTM components could be manipulated independently (Glanzer, 1972). On free recall, one such task, amnesics are found to perform very poorly on the LTM component, but satisfactorily on the STM component (e.g., Baddeley & Warrington, 1970). Three other patients, in contrast, were found to have the complementary difficulty: performing normally on the LTM component and very poorly on the STM one (Shallice & Warrington, 1970; Warrington et al., 1971). These patients also showed very much reduced spans and very rapid forgetting using the Brown-Peterson procedure (Warrington & Shallice, 1969, 1972; Warrington et al., 1971). Moreover, in two cases (the third patient was not so tested), the patients were also found to have severe deficits in shortterm memory tasks using recognition techniques (Shallice & Warrington, 1970, 1974), indicating that the deficit was of STM storage, not simply retrieval from STM. This dichotomy between long- and short-term verbal memory has been quite widely criticized recently (Shulman, 1970; Craik & Lockhart, 1972). However, recent papers have presented evidence which shows that these criticisms can be adequately countered (Shallice, 1975; Levy & Craik, 1975). For convenience, we will use the terms STM and LTM for the two systems, without intending to suggest that this is an exclusive classification. For instance, we believe that a visual STM system exists which can be spared when the auditory-verbal STM system is damaged (Warrington & Shallice, 1972; Saffran & Marin, 1975). It would seem plausible that a system which holds phonological information for short periods of time could be part of either the input or the output speech system. We will discuss in a later section why we do not think that it is involved in the speech production process. If it is part of the speech comprehension process as suggested by Shallice and Warring-
SHORT-TERM
MEMORY
AND CONDUCTION
APHASIA
483
ton (1970), Shallice (1973, Marin, Saffran, and Schwartz (1973, and Baddeley (1976), then the finding of seemingly intact comprehension of such conduction aphasics on clinical testing is paradoxical. In fact, Warrington et al. (1971) showed that such patients had moderate to severe difficulties on De Renzi’s test, even though they performed much better on identifying words from description, a task that involves comprehension of a sentence of similar length. The latter sentences, though, like most in normal conversation, are semantically overdetermined. The former are not, as each requires the interpretation of three or four disparate pieces of information. Moreover, further testing suggests that these patients may have difficulty in comprehending sentences which are syntactically complex or which cannot be easily disambiguated, so a subtle comprehension defect may well result from auditory-verbal STM loss. As pointed out by Marin et al., it may be that only in the comprehension of such sentences is the preservation of surface structure necessary. KINSBOURNE’S
DISCONNECTION
APPROACH
Kinsbourne (1972) studied the performance of two patients, JT and JO. In common with the patients we studied, his patients have a drastically reduced auditory-verbal span and a somewhat better visual-verbal span. One patient, JO, is clearly different from the other conduction aphasics under consideration. His performance was considerably improved by being able to point to written numbers or write them instead of having to repeat them, which suggests involvement of the articulatory control system. This patient was not able to repeat most single words and therefore the defect appears to be one not of repetition but of reproduction, which we would not wish to encompass by the STM model. We will discuss this issue more fully later. Kinsbourne argues that his more fully studied patient, JT, does not have a STM defect on three grounds: his rate of responding, his ability to match strings of digits, and his improved recall performance when output requirements are reduced. He suggests instead, as we discussed before, that the patient’s defect arises from a pathologically limited channel from STM to the speech response program. When two digits are presented to JT, not only is there an increased error rate when compared with the one-digit situation, but there is also a gross slowing of the response. Kinsbourne argues that this is because information must be transmitted along the critical channel at a “pathologically slow rate.” However, once it is recognized that retrieval in a span task can have at least two components, some retrieval from LTM being possible in addition to STM, the result becomes entirely compatible with the STM interpretation. In the two-digit case (above JT’s span) one digit may frequently have to be retrieved from LTM, which is known to be a much slower process (Waugh, 1970). This argument is supported by our
484
SHALLICE
AND WARRINGTON
finding that KF, who has a comparable span (see Table I), uses LTM as well as STM in a two-digit span situation as judged by his susceptibility to proactive interference in that situation (Shallice & Warrington, 1970). In addition, Saffran and Marin (1975) have shown that the effect of material on span performance for their patient has accepted LTM characteristics rather than STM ones, as with KF. Kinsbourne also shows that if the two digits are the same or if only one must be recalled, performance is improved and he claims that this shows that the impairment is subsequent to the short-term store. However, Waugh and Norman (1968) have shown that in certain circumstances a repeated digit may require no more STM capacity than a single digit. On part-responding to one of a two-digit string, Kinsbourne says: “Although a few errors crept in, as long as only one item need be repeated, the error rate approximates that when one item only is presented.” In fact, on this task, JT performed at 86% accuracy; in normal recall with one item he was 100% correct and with two items he was 75% correct. STM theory predicts just this intermediate type of figure, whereas conduction theory predicts 100% performance, as with one digit. Moreover, on STM theory, performance on the second digit should be better than the first since there is less retroactive interference; even with the relatively small amount of data Kinsbourne reported that retention of the second item is marginally significantly better (Fisher exact test, p < .l). Kinsbourne’s most compelling argument stems from the seemingly good performance of conduction aphasics on matching tasks. When JT has to match two strings of digits for sameness/difference, he scores far more highly than in recall of a string of comparable length. Moreover, his performance on this task is not very different from that of KF (see Table 1). Kinsbourne interprets this as showing that, if output requirements are reduced to a mere Yes or No response, performance is much improved and that this would not be expected if the deficit is one of STM storage. However, it might be expected that performance on a matching task would be better than on a recall task even for normal subjects. In signal detection theory terms, one needs a much greater signal strength to decide TABLE 1 COMPARISON OF JT AND KF’s PRE-OP PERFORMANCE ON RECALL AND MATCHING DIGITS~
1
2
3
4
Recall (strings correct)
JT KF
40140 20120
30/40 12120
o/10 6120
o/10 l/20
Matching
JT KF
20120 20120
20120 19/20
18120 20120
19/20 17120
n From Kinsboume (1972) and Warrington and Shallice (1969).
SHORT-TERM
MEMORY
AND CONDUCTION
APHASIA
485
with a given accuracy between 10 alternatives than between 2 alternatives. To assess whether the recognition performance of these patients is in fact qualitatively better than their recall performance, as Kinsbourne claims, one would need a satisfactory theory of the interrelation between recall and recognition in short-term memory, but no such theory exists. Available evidence suggests that, in normals, STM recognition scores are superior to recall scores even when allowance is made for the greater response load of the recall task (Norman, 1966). Comparison of the recognition and recall performance in conduction aphasics is an inadequate way of assessing whether a recognition defect exists. Only roughly comparable performance between conduction aphasics and appropriate controls on recognition tasks could substantiate that no such deficit exists. The only relevant data for the matching task are provided by the work of Tzortzis and Albert; their conduction aphasics were “much worse” on the matching task than were two control subjects who were (non-conduction) aphasics. When considering whether, in general, a disconnection theory can account for all of the repetition results found with conduction aphasic patients, data from more satisfactory retrieval tasks need to be considered. On a probe digit task in which the subject has to say whether a probe item was included in the presented set, a recognition task which is not only “cleaner” than the matching task but also has the advantage of reducing intonation cues, our two conduction aphasics (KF and JB) both performed at a level that must be regarded as well below normal. A high percentage of errors on strings shorter than the normal span occurred. KF made 35% errors on a five-item string and JB made 37% errors on a six-item string (Shallice & Warrington, 1970, 1974). Furthermore, on the missing scan task devised by Buschke (1963), where subjects only have to produce the one missing digit, KF showed the same order of deficit as on a recall task (Shallice & Warrington, 1970). (JB was not tested on this task.) Experiments using types of retrieval other than recall therefore support the STM interpretation and greatly weaken the conduction hypothesis. One final type of evidence which is extremely difficult for a disconnection hypothesis to explain is the poor performance of our conduction aphasic patients on Brown-Peterson tasks (Warrington et al., 1971). KF even showed a striking decrement over time in the retention of a single item (Warrington & Shallice, 1972). In this situation the retrieval demands of the task remain constant and minimal, yet an abnormally great STM decrement occurs. Unfortunately, this critical experiment has not been reported for any of the other conduction aphasic patients. In conclusion, we would argue that Kinsbourne’s findings with JT are more easily explained as a STM defect than as a conduction defect, but as no specifically STM experiments were performed this interpretation must be provisional. In any case, there is no reason to suppose that JT’s
486
SHALLICE
AND WARRINGTON
syndrome differs significantly from KF’s, for whom a STM interpretation is clearly better. TZORTZIS
AND ALBERT’S
ORDERING
DEFICIENCY
APPROACH
Tzortzis and Albert (1974) present data on three conduction aphasic patients. Their results on digit, letter, and word spans, on the superiority with visual input, and on the absence of any advantage in using a pointing response are very similar to ours. They argue that their patients are, in fact, different from ours, as they differ in three respects: long-term memory, short-term memory for nonverbal sounds, and, most important, sequencing. They consider that the difficulty arises from an inability to retain order information about sounds to be produced. Their conduction aphasics performed more poorly on long-term memory tasks than did the three controls. However, the three controls were younger student volunteers, so this is hardly surprising. On the Wechsler paired-associate learning task, two of the conduction aphasics (C2, C3) obtained an above-average score for their age and, on the IO-word learning test (Stevenson, 1968), one (C3) was satisfactory. Thus, there appears to be no consistent relation in Tzortzis and Albert’s patients between their conduction aphasia and poor LTM performance. On short-term memory for nonverbal sounds, the conduction aphasics performed less well than did the other two non-conduction aphasics. Our two patients (KF and JB) performed as well as normals on this task (Shallice & Warrington, 1974). However, we required our subjects to perform a concurrent counting task to prevent them from verbalizing the names of the sounds and so remembering them through verbal mediation, a strategy which is only of use if the patient has a reasonable word span. Since Tzortzis and Albert did not use such a concurrent task, it is likely that their conduction asphasics were handicapped by their inability to use a verbal mediation strategy. Their patients’ seemingly inferior performance on rhythm reproduction could be explained in a similar way. Clearly, a possible way of performing this task is by covertly naming to oneself the number of taps in successive groups. Tzortzis and Albert present a detailed analysis to show that their subjects make more order errors than item errors and argue that order errors occur more frequently as strings become longer. The data they present are not relevant, as they compared the number of items correct in totally correct sequences with the number of items correct in all erroneous sequences (see their Table 5a). The relevant comparison is between totally correct sequences and sequences having all items correct and order incorrect. Even accepting that some order errors are made by their subjects in span tasks, this does not distinguish them from our subjects. It would only refute a STM interpretation if, by ignoring order, performance became near normal: This is far from the case. Table 2 shows the order errors for our
SHORT-TERM
MEMORY
AND CONDUCTION TABLE
FREQUENCY
OF ORDER
2
ERRORS IN STRINGS
WITH
ALL
ITEMS
Digits 2
KF (pre-op) KF (post-op) JB WH
NA
0120 Oil0 0124
487
APHASIA
CORRECT Letters
3
4
2
3
4
016 0114 119 5114
Ill 317 il.5 313
NA 0118 019 1122
o/3 l/8 O/5 318
012 O/l Oil
patients on the span tasks previously reported (Warrington & Shallice, 1969; Warrington et al., 1971). It can be seen that for our patients, too, there is an increasing chance of an order error as the length of the strings increases toward the maximum ever attained by the patient. However, normal subjects actually make more transposition errors (order errors) than item errors when they reach the limit of their span (Ryan, 1969). Yet normal performance breaks down when STM capacity, not just order capacity, is reached since both item errors and transposition errors occur. In any case, it is widely held that there is an intimate link between item and order information in STM. If, as suggested, it is a store which maintains a record of phonological processing in case an initial attempt by semantic mechanisms to interpret the sentence fails, then it is vital for it to be an order-based store. Moreover, LTM, which we know the conduction aphasics also use in a span situation, is likely not to be order based, given findings such as those of Morton (1968) and Fozard (1970). Thus, when STM fails, order errors as well as item errors are to be expected. We therefore conclude that the repetition difficulties of the patients reported by Tzortzis and Albert are not different from those of the patients we studied. Furthermore, their explanation is not as radically different from ours as they claim. (The existence of order errors is, of course, yet another argument against the disconnection theory.) However, as in both Tzortzis and Albert’s work and ours there is evidence of defects involving the retention of item information as well as order information, we also consider the STM hypothesis to be more parsimonious than a hypothesis which postulates just a serial order deficit. For instance, in both their work and ours, a sizable loss of item information is present in the repetition of letter, digit, and word strings. It might be objected that in these experiments the patient who has to retain both order and item information does not reproduce the item information, even though it is available, because order information has been lost. Apart from its intrinsic inplausibility, such a notion would not explain the difficulties our patients have with probe recognition (Shallice & Warrington, 1970, 1974), free recall (Shallice &
488
SHALLICE
AND WARRINGTON
Warrington, 1970; Warrington et al., 1971), and one-item Brown-Peterson retention (Warrington & Shallice, 1972), where order information is irrelevant. Until it is shown that a conduction aphasic is relatively normal on such order-irrelevant experiments, it is unnecessary to postulate a special memory for order. STRUB AND GARDNER’S
MULTICOMPONENT
THEORY
Strub and Gardner (1974) describe a patient (LS) who has many difficulties in common with KF, but who they argue has further deficits which make the syndrome difficult to interpret on the STM theory. They put forward a number of arguments including two which have already been discussed, namely, the existence of sequencing effects and the increase in span when it is tested by matching. In their case, the argument against a STM interpretation is made even weaker by the use of highly meaningful material (words or objects), which allow LTM to play a more important role in span tasks than when material such as letters or digits is used (see Baddeley, 1976). They raise a number of other points which we will discuss briefly. “The patient’s ability to repeat familiar materials was dramatically superior to his repetition of unfamiliar or nonsense materials.” Saffran and Marin (1975) have already pointed out that the effect of familiarity is exactly what one would expect on STM theory, since the performance of these patients on span tasks relies to a considerable extent on LTM. A similar argument applied to their point covering the rate of presentation variable: “The patient retained more information when stimuli were presented at a slower rate.” LTM is greatly affected by rate of presentation (Glanzer, 1972). None of these points appears to us to be at all critical for the STM theory. Strub and Gardner suggest that in conduction aphasia after perception of “a word as a word,” “decoding for meaning” and “selection and arrangement of phonemes in the correct sequence” may both be performed with reduced efficiency, especially when both need to be undertaken simultaneously. The complexities of this notion make it a priori difficult to falsify. All of these difficulties may well occur in their patient, but unless it can be shown that one of the other three single-factor explanations is unsatisfactory there is no justification for accepting theirs as a general explanation of conduction aphasia. It is also unclear why on this theory one test of comprehension, the Token Test, should be so much more affected in our patients than another, the Words from Description Test (Warrington et al., 1971). Both, in their terms, require “decoding for meaning.” Nor on their theory is it clear why short-term memory tested by recognition techniques should produce deficits with conduction aphasic patients. We, therefore, do not consider that their theory can provide a general explanation of repetition deficits in conduction aphasic patients.
SHORT-TERM
HIGH-LEVEL
MEMORY
AND CONDUCTION
SPONTANEOUS
APHASIA
489
SPEECH DEFECTS
There is, however, one major difference between Strub and Gardner’s patient LS and our patients. LS made very frequent paraphasic responses, either semantic or literal. This was not the case for our patients, whose errors were mainly omissions, or indeed for Saffran and Marin’s (1977) patient IL. Yet paraphasic errors are often considered characteristic of conduction aphasia (e.g. Dubois et al., 1964). The question is therefore raised of whether some form of high-level deficit of spontaneous speech is functionally contingent upon the repetition defect or is a distinct anatomically related difficulty. To pose the problem more generally: Is auditory-verbal short-term memory involved in speech output, as suggested, among others, by Hintzman (1967) and Morton (1970)? Benson et al. (1973) report a variety of types of speech disorder in a series of conduction aphasic patients for whom autopsy data were available: “fluent, paraphasic” (six cases), “fluent, paraphasic, and paragrammatic” (two cases), “grammatical defect” (one case), “disturbed, much paraphasia” (one case), “jargon” (one case), “essentially normal, occasional paraphasia” (one case), “fluent, no paraphasia” (one case). This wide distribution of spontaneous speech symptoms together with the latter two cases of near normality in spontaneous speech suggests that this defect is anatomically rather than functionally related to the STM defect. This conclusion is strongly supported by the finding that one of our STM cases, JB, has no detectable spontaneous speech defect other than a slight increase in function word errors (Shallice & Butterworth, 1977). Moreover, Saffran and Marin describe their patient IL as having only a “minimal” expressive difficulty. If this conclusion is correct, namely, that the connection between the repetition and reproduction difficulties is anatomical rather than functional, then the syndrome conduction aphasia can arise in two ways. The following hypothethical simplified scheme is presented to highlight the difference between them. Conduction aphasia derived from reproductive difficulties, the type stressed by Dubois et al., would be the inability to reproduce on request individual words, being exacerbated by using longer less-frequent words. In such cases, the severity of the reproductive defect would be closely related to the severity of the literal paraphasic disturbance in their expressive speech and, probably, as Yamadori and Ikumura (1975) have argued, to difficulty on object naming and reading aloud as well. Conduction aphasia derived from repetition difficulties (a deficit of STM) would not, in its pure form, give rise to reproductive difficulties, but instead to impairment on verbal span tasks; spontaneous speech would not be affected. In our view, there is a STM component contributing to the deficits on repetition tasks of all experimentally studied conduction aphasic patients with the exception of Kinsbourne’s patient, JO.
SHALLICE
490
AND WARRINGTON
Granted this theoretical distinction, practical differentiation between the two types would be facilitated by systematic use of more appropriate techniques. As pointed out in the introduction, many clinical tests of repetition, e.g., repetition of a phrase, involve both functions. However, it appears that many conduction aphasics have sustained both types of defect, which suggests that there may be a close anatomical relation between the critical lesion sites. If this theoretical distinction is accepted, then there need be no functional relationship between the systems involved in repetition and reproduction and so their respective functions could more conveniently be discussed independently. In our view, the term “conduction aphasia” should be restricted to the usage stressed by Dubois et al. (1964) and Benson et al. (1973), namely, the disorder of reproduction. The disorder of repetition could then be called a deficit of auditory-verbal STM. REFERENCES Atkinson, R. C., & Shiffrin, R. M. 1968. Human memory: A proposed system and its control processes. In K. W. Spence & J. T. Spence (Eds.), The psychology of learning and motivation: Advances in research and theory. New York: Academic Press. Vol. 2. Baddeley, A. D. 1966. Short-term memory for word sequences as a function of acoustic, semantic and formal similarity. Quarterly Journal of Experimental Psychology, 18, 362-365. Baddeley, A. D. 1976. The psychology of memory. New York: Harper. Baddeley, A. D., & Warrington, E. K. 1970. Amnesia and the distinction between long- and short-term memory. Journal of Verbal Learning and Verbal Behavior, 9, 176-189. Benson, D. F., Sheremata, W. A., Bouchard, R., Segarra, J. M. Price, D., & Geschwind, N. 1973. Conduction aphasia: A clinicopathological study. Archives of Neurology, 28, 339-346. Buschke, H. 1963. Retention in immediate memory estimated without retrieval. Science, 140, 56-57. Craik, F. I. M. & Lockhart, R. S. 1972. Levels of processing: A framework for memory research. Journal of Verbal Learning and Verbal Behavior, 11, 671-684. Dubois, J., Hecaen, H., Angelergues, R., Maufras, Du Chatelier, A., & Marcie, P. 1964. Etude neurolinguistique de I’aphasie du conduction. Neuropsychologia, 2, 9-44. Fozard, J. L. 1970. Apparent recency of unrelated pictures and nouns presented in the same sequence. Journal of Experimental Psychology, 86, 137-143. Geschwind, N. 1965. Disconnexion syndromes in animal and man. Brain, 88, 237-294, 585-644. Glanzer, M. 1972. Storage mechanisms in recall. In G. H. Bower (Ed.), The psychology of learning and motivation: Advances in research and theory. New York: Academic Press. Vol. 5. Hintzman. D. L. 1967.Articulatory coding in short-term memory. Journal of Verbal Learning and Verbal Behavior, 6, 312-316. Kinsbourne, M. 1972. Behavioral analysis of the repetition deficit in conduction aphasia. Neurology, 22, l126- 1132. Kintsch, W., & Buschke, H. 1969. Homophones and synonyms in short-term memory. Journal
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Kleist, K. 1916. Uber Leitungsaphasie und grammatische Storungen. Monatsschrift Psychiatric
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fur
SHORT-TERM Levy, Marin,
MEMORY
AND CONDUCTION
APHASIA
B. A., & Craik, F. I. M. 1975. The co-ordination of codes in short-term Quarterly Journal qf’ Experimental Psychology. 27, 33-46.
491 retention.
0. S. M., Saffran, E. M., & Schwartz, M. F. 1975. Dissociations oflangrrage in aphasia: Implications for normal functions. Paper presented at The New York Academy of Sciences Conference on Origins and Evolution of Language and Speech, September. Morton, .I. 1968. Repeated items and decay in memory. Psychonomic Science, 10, 219-220. Morton, .I. 1970. A functional model for memory. In D. A. Norman (Ed.). Models of humau ,rtemory. New York: Academic Press. Norman, D. A. 1966. Acquisition and retention in short-term memory. Jorrrnul qf Erperimental Psychology, 72, 369-381. Ryan, J. 1969. Grouping and short-term memory: Different means and patterns of grouping. Quarterly Journal of Experimental Psychology, 21, 137- 147. Saffran, E. M., & Marin. 0. S. M. 1975. Immediate memory for word lists and sentences in a patient with deficient auditory short-term memory. Brain and Language, 2, 420-433. Shallice. T. 1975. On the contents of primary memory. In S. Dornic & P. Rabbitt (Eds.). Attention and performance V. New York: Academic Press. Shallice, T., & Butterworth, B. B. 1977. Short-term memory and impairment und spontaneous speech. Neuropsychologia (in press). Shallice. T., & Warrington, E. K. 1970. Independent functioning of the verbal memory stores: A neuropsychological study. Quarterly Journul qf Experimental Psychology, 22, 261-273. Shallice, T.. & Warrington, E. K. 1974. The dissociation between short-term retention of meaningful sounds and verbal material. Neuropsychologia. 12, 553-555. Shulman. H. G. 1970. Encoding and retention of semantic and phonemic information in short-term memory. Journal of Verbal Leurning and Verbal Beharlior. 9, 499-508. Stevenson, J. 196X. Some psychological ejfects offrontal lobe lesions in man. M.Sc. thesis (unpublished), University of Cambridge. Strub, R. L.. & Gardner, H. 1974. The repetition defect in conduction aphasia: Mnestic or linguistic? Brain and Language. 1, 241-255. Tzortzis, C.. & Albert, M. L. 1974. Impairment of memory for sequences in conduction aphasia. Neuropsychoiogiu, 12, 355-366. Warrington, E. K., Logue, V., & Pratt, R. T. C. 1971. The anatomical localisation of auditory-verbal short-term memory. Neurc~psychologia, 9, 377-387. Warrington, E. K., & Shallice, T. 1969. The selective impairment of auditory-verbal short term memory. Brain, 92, 885-896. Warrington. E. K., & Shallice, T. 1972. Neuropsychological evidence of visual storage in short-term memory tasks. Quarter/y Joarnal of‘ Experimental Psychology, 24, 30-40. Waugh, N. C. 1970. Retrieval time in short-term memory, British Journal ofPsycho&y, 61, l-12. Waugh, N. C., & Norman, D. A. 1965. Primary memory. Psycho/ogica/ Rel,ielc,, 72, g9- 104. Waugh, N. C., & Norman, D. A. 1968. The measure of interference in primary memory. Journal of Verbal Learning and Verbal Behavior, 7, 617-626. Wernicke. C. 1874. Der Aphasische Symptomenkomplex. Breslau: Taschen. Yamadori, A., & Ikumura, G. 1975. Central (or conduction) aphasia in a Japanese patient. Cortex, 11, 73-82.
AND
LANGUAGE
4, 479-491 (1977)
Auditory-Verbal Short-Term and Conduction TIM SHALLICEAND
Memory Aphasia
Impairment
ELIZABETH K. WARRINGTON
National Hospital, London The specific impairment of performance on repetition tasks has classically been identified with conduction aphasia. It is argued that this impairment can be subdivided and a deficit in span performance distinguished from that of the reproduction of single words. An explanation of the span deficit in terms of auditory-verbal short-term memory is preferred to hypotheses involving disconnections or damage to order retention systems. It is shown that a short-term memory component is present in many patients previously classified as conduction aphasics.
It is now widely believed that conduction aphasia exists as a syndrome, distinct from both sensory and motor aphasia. It is a syndrome in which verbal repetition is selectively impaired with spontaneous speech being relatively preserved and comprehension apparently intact.’ While it is held by some that conduction aphasia is a form of expressive aphasia (Dubois, HCcaen, Angelergues, Maufras, Du Chatelier, & Marcie, 1964), in fact patients classified as conduction aphasic have had a variety of different deficients of spontaneous speech (Benson, Sheremata, Bouchard, Segarra, Price, & Geschwind, 1973). The most commonly accepted cardinal symptom is a gross defect of repetition. However, the term “repetition” has been used relatively loosely in the literature to cover repetition of individual words, of individual nonsense syllables, of meaningless polysyllables, of unconnected sets of words (word span including digit span), of more than one nonsense syllable, and of phrases and of sentences. For theoretical reasons, to be discussed later, we will distinguish between repetition of a single relatively infrequent multisyllabic word (to be called “reproduction”) and of a number of unconnected short familiar words (to be called “repetition”). We will argue that the former task imposes stress on a different process from the latter. Theoretically, the distinction may be conceptualized terms of the distinction between the ability to produce and the ability retain an ordered set of verbal units.
in to
We should like to thank Dr. R. T. C. Pratt for his helpful suggestions on the manuscript. Requests for reprints should be addressed to Dr. Tim Shallice, National Hospital, Queen’s Square, London, W.C. 1. England. I The term syndrome is used in the sense of a collection together.
479
of symptoms regularly
occurring
480
SHALLICE
AND WARRINGTON
Most clinical investigations of conduction aphasia have not separately assessed production and retention of verbal units. Experimental studies have, however, recently tended to be of “repetition” as defined above and have provided a much more systematic body of data on conduction aphasia than was previously available. However, this greater uniformity of method has not led to any uniformity of theoretical position. Indeed, from investigations of repetition, four different theories of conduction aphasia have recently been supported. In a series of investigations of a patient, KF (Warrington & Shallice, 1969, 1972; Shallice & Warrington, 1970, 1974), we argued that a specific failure on repetition tasks exists which arises from a difficulty of auditory-verbal short-term memory. Further research showed that the deficit of three other patients could be interpreted in the same terms (Warrington, Logue, & Pratt, 1971; Saffran & Marin, 1975). Our position has been questioned by Kinsbourne (1972), Tzortzis and Albert (1974), and Strub and Gardner (1974), who have studied forms of conduction aphasia which they argued do not arise from a deficit of auditory-verbal short-term memory (STM). Kinsbourne argues in favor of a modern version of Wernicke’s (1874) disconnection hypothesis [also supported by Geschwind (1965)] in terms of a pathologically limited channel between the auditory-verbal STM system and the “imitative response program.” He considers that this pathological limitation can arise in two different ways. It can result from the use of a damaged left arcuate bundle (which connects Wernicke’s area with Broca’s area); alternatively, extensive left hemisphere damage can, in his view, lead to a release of the language mechanisms of the right hemisphere from inhibition. Following Kleist’s (1916) suggestion, he proposes that “the right temporal lobe compensates for the left but then has to utilize the imperfect speech programming mechanism of the right hemisphere having no ready access to the intact Broca’s area on the left.” Tzortzis and Albert hold that the basic disorder of conduction aphasic patients lies in the “disorganization of the execution of a particular encoded programme” in the speech production process, which Dubois et al. (1964), the originators of the theory, term “an aphasia of the first articulation, i.e., groups defined by the plans of the morpheme or the phrase.” Tzortzis and Albert argue that “essential to this hypothesis is the implied contention that there is a marked deficiency in the memory for the specific sequential order of the items to be repeated.” The final approach is that of Strub and Gardner (1974). They assume that the difficulty arises after phonological analysis of the auditory input has been performed and some trace held for further processing. At this point they argue that the conduction aphasic “can proceed to extract its meaning and/or synthesize its phonemic components for eventual articulation,” but these processes are performed with reduced efficiency and
SHORT-TERM
MEMORY
AND CONDUCTION
APHASIA
481
may be mutually interfering. In particular, the repetition difficulty arises from “an impairment in proceeding from a phonological analysis to the selection and combination of target phonemes.” One problem with assessing these theories is that it is unclear how far they are reformulations or actually substantively different. Thus, Strub and Gardner’s explanation of repetition difficulty, depending on the emphasis one gives to their wording, could be equivalent to either Kinsbourne’s or Tzortzis and Albert’s position. Furthermore, while Kinsbourne’s theory seems to be in conflict with that of Tzortzis and Albert, it does not appear to be necessarily incompatible with the theory of Dubois et al., of which Tzortzis and Albert’s theory is supposed to be a reformulation! However, we will assume that the theory of Dubois et al. refers to a deficit in a system which receives input from the conduction pathway or pathways that Kinsbourne argues are damaged. A similar point concerns Strub and Gardner’s attempt to contrast linguistic and mnestic theories. We have argued that the function of auditory-verbal short-term memory is specific to speech processing (Shallice & Warrington, 1970, 1974; Shallice, 1975). In fact, on a theory such as Morton’s (1970) in which the main auditory verbal short-term memory store is a Response Buffer, the auditory-verbal STM theory could become equivalent to the theory of Dubois et al. We, however, will argue that the auditory-verbal STM is an input store. A second problem is that there is considerable doubt in the literature over whether all of the patients labeled as conduction aphasic have the same functional deficit. We, ourselves, for instance, have modified our position on this matter (see Warrington & Shallice, 1969; Warrington et al., 1971). In this paper we will argue that there are at least two theoretically separable functional deficits corresponding to specific difficulties on the repetition and reproduction tasks, respectively, the former involving auditory-verbal STM and the latter involving the speech production process. This view might seem to resolve much of the conflict in the literature since it could be argued that the different explanations could be referring to different types of patient. However, the situation is, in fact, more complex. Most of the tests performed in all of the recent investigations have involved repetition (which would be the STM type of test) and from this Kinsbourne, Tzortzis, and Albert, and Strub and Gardner have all concluded that their patients do not have STM difficulties. Moreover, two (Kinsbourne and Strub & Gardner) suggest that their theories would explain the repetition defects of our patients. We consider that both of these types of argument are incorrect and that in only one (or possibly two) of these patients is there evidence that their repetition (as opposed to reproduction) deficits do not arise from an STM deficit. As these authors tend to produce evidence which they consider supports their theory and is in
482
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AND WARRINGTON
conflict with a STM approach, we will present our arguments similarly. After reviewing the evidence on repetition tasks for the non-STM theories, we will consider the deficits of reproduction. We begin, however, with a brief discussion of the STM theory. THE STM APPROACH
By the late 196Os,it was widely accepted by cognitive psychologists that memory systems exist which only hold information over short intervals of time and, in particular, that performance on verbal memory tasks involved at least one STM system as well as a long-term memory (LTM) system (Waugh & Norman, 1965; Atkinson & Shiffrin, 1968). Evidence for this conclusion was derived from a number of different sources (see Baddeley, 1976). For instance, material retained over different periods of time seems more affected by different sources of interference: acoustic over short intervals, semantic over long (Baddeley, 1966; Kintsch & Buschke, 1969). In addition, a number of different tasks were found in which the STM and LTM components could be manipulated independently (Glanzer, 1972). On free recall, one such task, amnesics are found to perform very poorly on the LTM component, but satisfactorily on the STM component (e.g., Baddeley & Warrington, 1970). Three other patients, in contrast, were found to have the complementary difficulty: performing normally on the LTM component and very poorly on the STM one (Shallice & Warrington, 1970; Warrington et al., 1971). These patients also showed very much reduced spans and very rapid forgetting using the Brown-Peterson procedure (Warrington & Shallice, 1969, 1972; Warrington et al., 1971). Moreover, in two cases (the third patient was not so tested), the patients were also found to have severe deficits in shortterm memory tasks using recognition techniques (Shallice & Warrington, 1970, 1974), indicating that the deficit was of STM storage, not simply retrieval from STM. This dichotomy between long- and short-term verbal memory has been quite widely criticized recently (Shulman, 1970; Craik & Lockhart, 1972). However, recent papers have presented evidence which shows that these criticisms can be adequately countered (Shallice, 1975; Levy & Craik, 1975). For convenience, we will use the terms STM and LTM for the two systems, without intending to suggest that this is an exclusive classification. For instance, we believe that a visual STM system exists which can be spared when the auditory-verbal STM system is damaged (Warrington & Shallice, 1972; Saffran & Marin, 1975). It would seem plausible that a system which holds phonological information for short periods of time could be part of either the input or the output speech system. We will discuss in a later section why we do not think that it is involved in the speech production process. If it is part of the speech comprehension process as suggested by Shallice and Warring-
SHORT-TERM
MEMORY
AND CONDUCTION
APHASIA
483
ton (1970), Shallice (1973, Marin, Saffran, and Schwartz (1973, and Baddeley (1976), then the finding of seemingly intact comprehension of such conduction aphasics on clinical testing is paradoxical. In fact, Warrington et al. (1971) showed that such patients had moderate to severe difficulties on De Renzi’s test, even though they performed much better on identifying words from description, a task that involves comprehension of a sentence of similar length. The latter sentences, though, like most in normal conversation, are semantically overdetermined. The former are not, as each requires the interpretation of three or four disparate pieces of information. Moreover, further testing suggests that these patients may have difficulty in comprehending sentences which are syntactically complex or which cannot be easily disambiguated, so a subtle comprehension defect may well result from auditory-verbal STM loss. As pointed out by Marin et al., it may be that only in the comprehension of such sentences is the preservation of surface structure necessary. KINSBOURNE’S
DISCONNECTION
APPROACH
Kinsbourne (1972) studied the performance of two patients, JT and JO. In common with the patients we studied, his patients have a drastically reduced auditory-verbal span and a somewhat better visual-verbal span. One patient, JO, is clearly different from the other conduction aphasics under consideration. His performance was considerably improved by being able to point to written numbers or write them instead of having to repeat them, which suggests involvement of the articulatory control system. This patient was not able to repeat most single words and therefore the defect appears to be one not of repetition but of reproduction, which we would not wish to encompass by the STM model. We will discuss this issue more fully later. Kinsbourne argues that his more fully studied patient, JT, does not have a STM defect on three grounds: his rate of responding, his ability to match strings of digits, and his improved recall performance when output requirements are reduced. He suggests instead, as we discussed before, that the patient’s defect arises from a pathologically limited channel from STM to the speech response program. When two digits are presented to JT, not only is there an increased error rate when compared with the one-digit situation, but there is also a gross slowing of the response. Kinsbourne argues that this is because information must be transmitted along the critical channel at a “pathologically slow rate.” However, once it is recognized that retrieval in a span task can have at least two components, some retrieval from LTM being possible in addition to STM, the result becomes entirely compatible with the STM interpretation. In the two-digit case (above JT’s span) one digit may frequently have to be retrieved from LTM, which is known to be a much slower process (Waugh, 1970). This argument is supported by our
484
SHALLICE
AND WARRINGTON
finding that KF, who has a comparable span (see Table I), uses LTM as well as STM in a two-digit span situation as judged by his susceptibility to proactive interference in that situation (Shallice & Warrington, 1970). In addition, Saffran and Marin (1975) have shown that the effect of material on span performance for their patient has accepted LTM characteristics rather than STM ones, as with KF. Kinsbourne also shows that if the two digits are the same or if only one must be recalled, performance is improved and he claims that this shows that the impairment is subsequent to the short-term store. However, Waugh and Norman (1968) have shown that in certain circumstances a repeated digit may require no more STM capacity than a single digit. On part-responding to one of a two-digit string, Kinsbourne says: “Although a few errors crept in, as long as only one item need be repeated, the error rate approximates that when one item only is presented.” In fact, on this task, JT performed at 86% accuracy; in normal recall with one item he was 100% correct and with two items he was 75% correct. STM theory predicts just this intermediate type of figure, whereas conduction theory predicts 100% performance, as with one digit. Moreover, on STM theory, performance on the second digit should be better than the first since there is less retroactive interference; even with the relatively small amount of data Kinsbourne reported that retention of the second item is marginally significantly better (Fisher exact test, p < .l). Kinsbourne’s most compelling argument stems from the seemingly good performance of conduction aphasics on matching tasks. When JT has to match two strings of digits for sameness/difference, he scores far more highly than in recall of a string of comparable length. Moreover, his performance on this task is not very different from that of KF (see Table 1). Kinsbourne interprets this as showing that, if output requirements are reduced to a mere Yes or No response, performance is much improved and that this would not be expected if the deficit is one of STM storage. However, it might be expected that performance on a matching task would be better than on a recall task even for normal subjects. In signal detection theory terms, one needs a much greater signal strength to decide TABLE 1 COMPARISON OF JT AND KF’s PRE-OP PERFORMANCE ON RECALL AND MATCHING DIGITS~
1
2
3
4
Recall (strings correct)
JT KF
40140 20120
30/40 12120
o/10 6120
o/10 l/20
Matching
JT KF
20120 20120
20120 19/20
18120 20120
19/20 17120
n From Kinsboume (1972) and Warrington and Shallice (1969).
SHORT-TERM
MEMORY
AND CONDUCTION
APHASIA
485
with a given accuracy between 10 alternatives than between 2 alternatives. To assess whether the recognition performance of these patients is in fact qualitatively better than their recall performance, as Kinsbourne claims, one would need a satisfactory theory of the interrelation between recall and recognition in short-term memory, but no such theory exists. Available evidence suggests that, in normals, STM recognition scores are superior to recall scores even when allowance is made for the greater response load of the recall task (Norman, 1966). Comparison of the recognition and recall performance in conduction aphasics is an inadequate way of assessing whether a recognition defect exists. Only roughly comparable performance between conduction aphasics and appropriate controls on recognition tasks could substantiate that no such deficit exists. The only relevant data for the matching task are provided by the work of Tzortzis and Albert; their conduction aphasics were “much worse” on the matching task than were two control subjects who were (non-conduction) aphasics. When considering whether, in general, a disconnection theory can account for all of the repetition results found with conduction aphasic patients, data from more satisfactory retrieval tasks need to be considered. On a probe digit task in which the subject has to say whether a probe item was included in the presented set, a recognition task which is not only “cleaner” than the matching task but also has the advantage of reducing intonation cues, our two conduction aphasics (KF and JB) both performed at a level that must be regarded as well below normal. A high percentage of errors on strings shorter than the normal span occurred. KF made 35% errors on a five-item string and JB made 37% errors on a six-item string (Shallice & Warrington, 1970, 1974). Furthermore, on the missing scan task devised by Buschke (1963), where subjects only have to produce the one missing digit, KF showed the same order of deficit as on a recall task (Shallice & Warrington, 1970). (JB was not tested on this task.) Experiments using types of retrieval other than recall therefore support the STM interpretation and greatly weaken the conduction hypothesis. One final type of evidence which is extremely difficult for a disconnection hypothesis to explain is the poor performance of our conduction aphasic patients on Brown-Peterson tasks (Warrington et al., 1971). KF even showed a striking decrement over time in the retention of a single item (Warrington & Shallice, 1972). In this situation the retrieval demands of the task remain constant and minimal, yet an abnormally great STM decrement occurs. Unfortunately, this critical experiment has not been reported for any of the other conduction aphasic patients. In conclusion, we would argue that Kinsbourne’s findings with JT are more easily explained as a STM defect than as a conduction defect, but as no specifically STM experiments were performed this interpretation must be provisional. In any case, there is no reason to suppose that JT’s
486
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AND WARRINGTON
syndrome differs significantly from KF’s, for whom a STM interpretation is clearly better. TZORTZIS
AND ALBERT’S
ORDERING
DEFICIENCY
APPROACH
Tzortzis and Albert (1974) present data on three conduction aphasic patients. Their results on digit, letter, and word spans, on the superiority with visual input, and on the absence of any advantage in using a pointing response are very similar to ours. They argue that their patients are, in fact, different from ours, as they differ in three respects: long-term memory, short-term memory for nonverbal sounds, and, most important, sequencing. They consider that the difficulty arises from an inability to retain order information about sounds to be produced. Their conduction aphasics performed more poorly on long-term memory tasks than did the three controls. However, the three controls were younger student volunteers, so this is hardly surprising. On the Wechsler paired-associate learning task, two of the conduction aphasics (C2, C3) obtained an above-average score for their age and, on the IO-word learning test (Stevenson, 1968), one (C3) was satisfactory. Thus, there appears to be no consistent relation in Tzortzis and Albert’s patients between their conduction aphasia and poor LTM performance. On short-term memory for nonverbal sounds, the conduction aphasics performed less well than did the other two non-conduction aphasics. Our two patients (KF and JB) performed as well as normals on this task (Shallice & Warrington, 1974). However, we required our subjects to perform a concurrent counting task to prevent them from verbalizing the names of the sounds and so remembering them through verbal mediation, a strategy which is only of use if the patient has a reasonable word span. Since Tzortzis and Albert did not use such a concurrent task, it is likely that their conduction asphasics were handicapped by their inability to use a verbal mediation strategy. Their patients’ seemingly inferior performance on rhythm reproduction could be explained in a similar way. Clearly, a possible way of performing this task is by covertly naming to oneself the number of taps in successive groups. Tzortzis and Albert present a detailed analysis to show that their subjects make more order errors than item errors and argue that order errors occur more frequently as strings become longer. The data they present are not relevant, as they compared the number of items correct in totally correct sequences with the number of items correct in all erroneous sequences (see their Table 5a). The relevant comparison is between totally correct sequences and sequences having all items correct and order incorrect. Even accepting that some order errors are made by their subjects in span tasks, this does not distinguish them from our subjects. It would only refute a STM interpretation if, by ignoring order, performance became near normal: This is far from the case. Table 2 shows the order errors for our
SHORT-TERM
MEMORY
AND CONDUCTION TABLE
FREQUENCY
OF ORDER
2
ERRORS IN STRINGS
WITH
ALL
ITEMS
Digits 2
KF (pre-op) KF (post-op) JB WH
NA
0120 Oil0 0124
487
APHASIA
CORRECT Letters
3
4
2
3
4
016 0114 119 5114
Ill 317 il.5 313
NA 0118 019 1122
o/3 l/8 O/5 318
012 O/l Oil
patients on the span tasks previously reported (Warrington & Shallice, 1969; Warrington et al., 1971). It can be seen that for our patients, too, there is an increasing chance of an order error as the length of the strings increases toward the maximum ever attained by the patient. However, normal subjects actually make more transposition errors (order errors) than item errors when they reach the limit of their span (Ryan, 1969). Yet normal performance breaks down when STM capacity, not just order capacity, is reached since both item errors and transposition errors occur. In any case, it is widely held that there is an intimate link between item and order information in STM. If, as suggested, it is a store which maintains a record of phonological processing in case an initial attempt by semantic mechanisms to interpret the sentence fails, then it is vital for it to be an order-based store. Moreover, LTM, which we know the conduction aphasics also use in a span situation, is likely not to be order based, given findings such as those of Morton (1968) and Fozard (1970). Thus, when STM fails, order errors as well as item errors are to be expected. We therefore conclude that the repetition difficulties of the patients reported by Tzortzis and Albert are not different from those of the patients we studied. Furthermore, their explanation is not as radically different from ours as they claim. (The existence of order errors is, of course, yet another argument against the disconnection theory.) However, as in both Tzortzis and Albert’s work and ours there is evidence of defects involving the retention of item information as well as order information, we also consider the STM hypothesis to be more parsimonious than a hypothesis which postulates just a serial order deficit. For instance, in both their work and ours, a sizable loss of item information is present in the repetition of letter, digit, and word strings. It might be objected that in these experiments the patient who has to retain both order and item information does not reproduce the item information, even though it is available, because order information has been lost. Apart from its intrinsic inplausibility, such a notion would not explain the difficulties our patients have with probe recognition (Shallice & Warrington, 1970, 1974), free recall (Shallice &
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AND WARRINGTON
Warrington, 1970; Warrington et al., 1971), and one-item Brown-Peterson retention (Warrington & Shallice, 1972), where order information is irrelevant. Until it is shown that a conduction aphasic is relatively normal on such order-irrelevant experiments, it is unnecessary to postulate a special memory for order. STRUB AND GARDNER’S
MULTICOMPONENT
THEORY
Strub and Gardner (1974) describe a patient (LS) who has many difficulties in common with KF, but who they argue has further deficits which make the syndrome difficult to interpret on the STM theory. They put forward a number of arguments including two which have already been discussed, namely, the existence of sequencing effects and the increase in span when it is tested by matching. In their case, the argument against a STM interpretation is made even weaker by the use of highly meaningful material (words or objects), which allow LTM to play a more important role in span tasks than when material such as letters or digits is used (see Baddeley, 1976). They raise a number of other points which we will discuss briefly. “The patient’s ability to repeat familiar materials was dramatically superior to his repetition of unfamiliar or nonsense materials.” Saffran and Marin (1975) have already pointed out that the effect of familiarity is exactly what one would expect on STM theory, since the performance of these patients on span tasks relies to a considerable extent on LTM. A similar argument applied to their point covering the rate of presentation variable: “The patient retained more information when stimuli were presented at a slower rate.” LTM is greatly affected by rate of presentation (Glanzer, 1972). None of these points appears to us to be at all critical for the STM theory. Strub and Gardner suggest that in conduction aphasia after perception of “a word as a word,” “decoding for meaning” and “selection and arrangement of phonemes in the correct sequence” may both be performed with reduced efficiency, especially when both need to be undertaken simultaneously. The complexities of this notion make it a priori difficult to falsify. All of these difficulties may well occur in their patient, but unless it can be shown that one of the other three single-factor explanations is unsatisfactory there is no justification for accepting theirs as a general explanation of conduction aphasia. It is also unclear why on this theory one test of comprehension, the Token Test, should be so much more affected in our patients than another, the Words from Description Test (Warrington et al., 1971). Both, in their terms, require “decoding for meaning.” Nor on their theory is it clear why short-term memory tested by recognition techniques should produce deficits with conduction aphasic patients. We, therefore, do not consider that their theory can provide a general explanation of repetition deficits in conduction aphasic patients.
SHORT-TERM
HIGH-LEVEL
MEMORY
AND CONDUCTION
SPONTANEOUS
APHASIA
489
SPEECH DEFECTS
There is, however, one major difference between Strub and Gardner’s patient LS and our patients. LS made very frequent paraphasic responses, either semantic or literal. This was not the case for our patients, whose errors were mainly omissions, or indeed for Saffran and Marin’s (1977) patient IL. Yet paraphasic errors are often considered characteristic of conduction aphasia (e.g. Dubois et al., 1964). The question is therefore raised of whether some form of high-level deficit of spontaneous speech is functionally contingent upon the repetition defect or is a distinct anatomically related difficulty. To pose the problem more generally: Is auditory-verbal short-term memory involved in speech output, as suggested, among others, by Hintzman (1967) and Morton (1970)? Benson et al. (1973) report a variety of types of speech disorder in a series of conduction aphasic patients for whom autopsy data were available: “fluent, paraphasic” (six cases), “fluent, paraphasic, and paragrammatic” (two cases), “grammatical defect” (one case), “disturbed, much paraphasia” (one case), “jargon” (one case), “essentially normal, occasional paraphasia” (one case), “fluent, no paraphasia” (one case). This wide distribution of spontaneous speech symptoms together with the latter two cases of near normality in spontaneous speech suggests that this defect is anatomically rather than functionally related to the STM defect. This conclusion is strongly supported by the finding that one of our STM cases, JB, has no detectable spontaneous speech defect other than a slight increase in function word errors (Shallice & Butterworth, 1977). Moreover, Saffran and Marin describe their patient IL as having only a “minimal” expressive difficulty. If this conclusion is correct, namely, that the connection between the repetition and reproduction difficulties is anatomical rather than functional, then the syndrome conduction aphasia can arise in two ways. The following hypothethical simplified scheme is presented to highlight the difference between them. Conduction aphasia derived from reproductive difficulties, the type stressed by Dubois et al., would be the inability to reproduce on request individual words, being exacerbated by using longer less-frequent words. In such cases, the severity of the reproductive defect would be closely related to the severity of the literal paraphasic disturbance in their expressive speech and, probably, as Yamadori and Ikumura (1975) have argued, to difficulty on object naming and reading aloud as well. Conduction aphasia derived from repetition difficulties (a deficit of STM) would not, in its pure form, give rise to reproductive difficulties, but instead to impairment on verbal span tasks; spontaneous speech would not be affected. In our view, there is a STM component contributing to the deficits on repetition tasks of all experimentally studied conduction aphasic patients with the exception of Kinsbourne’s patient, JO.
SHALLICE
490
AND WARRINGTON
Granted this theoretical distinction, practical differentiation between the two types would be facilitated by systematic use of more appropriate techniques. As pointed out in the introduction, many clinical tests of repetition, e.g., repetition of a phrase, involve both functions. However, it appears that many conduction aphasics have sustained both types of defect, which suggests that there may be a close anatomical relation between the critical lesion sites. If this theoretical distinction is accepted, then there need be no functional relationship between the systems involved in repetition and reproduction and so their respective functions could more conveniently be discussed independently. In our view, the term “conduction aphasia” should be restricted to the usage stressed by Dubois et al. (1964) and Benson et al. (1973), namely, the disorder of reproduction. The disorder of repetition could then be called a deficit of auditory-verbal STM. REFERENCES Atkinson, R. C., & Shiffrin, R. M. 1968. Human memory: A proposed system and its control processes. In K. W. Spence & J. T. Spence (Eds.), The psychology of learning and motivation: Advances in research and theory. New York: Academic Press. Vol. 2. Baddeley, A. D. 1966. Short-term memory for word sequences as a function of acoustic, semantic and formal similarity. Quarterly Journal of Experimental Psychology, 18, 362-365. Baddeley, A. D. 1976. The psychology of memory. New York: Harper. Baddeley, A. D., & Warrington, E. K. 1970. Amnesia and the distinction between long- and short-term memory. Journal of Verbal Learning and Verbal Behavior, 9, 176-189. Benson, D. F., Sheremata, W. A., Bouchard, R., Segarra, J. M. Price, D., & Geschwind, N. 1973. Conduction aphasia: A clinicopathological study. Archives of Neurology, 28, 339-346. Buschke, H. 1963. Retention in immediate memory estimated without retrieval. Science, 140, 56-57. Craik, F. I. M. & Lockhart, R. S. 1972. Levels of processing: A framework for memory research. Journal of Verbal Learning and Verbal Behavior, 11, 671-684. Dubois, J., Hecaen, H., Angelergues, R., Maufras, Du Chatelier, A., & Marcie, P. 1964. Etude neurolinguistique de I’aphasie du conduction. Neuropsychologia, 2, 9-44. Fozard, J. L. 1970. Apparent recency of unrelated pictures and nouns presented in the same sequence. Journal of Experimental Psychology, 86, 137-143. Geschwind, N. 1965. Disconnexion syndromes in animal and man. Brain, 88, 237-294, 585-644. Glanzer, M. 1972. Storage mechanisms in recall. In G. H. Bower (Ed.), The psychology of learning and motivation: Advances in research and theory. New York: Academic Press. Vol. 5. Hintzman. D. L. 1967.Articulatory coding in short-term memory. Journal of Verbal Learning and Verbal Behavior, 6, 312-316. Kinsbourne, M. 1972. Behavioral analysis of the repetition deficit in conduction aphasia. Neurology, 22, l126- 1132. Kintsch, W., & Buschke, H. 1969. Homophones and synonyms in short-term memory. Journal
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