Motomi Toichi
Introduction
The superior memory of people with autism has been commented on for over thirty years. Kanner, in his first report on autism, mentioned the ‘excellent rote memory’ of autism children (Kanner, 1943). Clinicians who are familiar with these conditions never fail to come across examples of outstanding memory for particular subjects (such as birthdays, the academic names of fish, and so on). However, early studies that used conventional neuropsychological tests reported impairments on various measures of memory in children with autism. So, for example, Boucher and Warrington (1976; see also Boucher 1978, 1981a) found that per- formance in memory tasks by participants with autism was similar to that of adults with the acquired amnesic syndrome, showing impaired recall from long-term memory (LTM), combined with relatively intact cued recall from LTM as well as intact short-term memory (STM). Thus, there is a discrepancy between the clinical observations and experimental findings.
One possible explanation for this discrepancy is differences between the individuals observed or tested. The participants with autism in early psychological studies were primarily children with varying degrees of intellectual disability (low-functioning autism, or LFA). More recent studies that examined individuals without intellectual disability (high-functioning autism, or HFA) have reported basically unim- paired performance on tasks thought to measure episodic memory (Bennetto, Pennington & Rogers, 1996; Minshew et al., 1992; Minshew & Goldstein, 1993; Renner, Klinger & Klinger, 2000; Summers & Craik, 1994) (but see Bowler, Gardiner & Grice, 2000). This suggests that autism and intellectual disability may have a negative interac- tive influence on the development of episodic memory. Age may also affect episodic memory since performance tends to be less impaired as age advances in people with HFA (e.g. Fein et al., 1996; Beversdorf et al., 1998). Therefore, in addressing the issue of the core
specificity of memory in autism, it seems important to examine adults with HFA.
The nature of memory tasks used in psychological studies appears to be another factor in accounting for the above discrepancy. For example, performance impairment tends to be striking when verbal materials to be remembered have rich semantic cues (Toichi & Kamio, 2003), and when they are semantically or contextually related (O’Connor & Hermelin, 1967; Ramondo & Milech, 1984; Tager-Flusberg, 1991; Wolff & Barlow, 1979), even when participants are those with HFA (Fein et al., 1996; Minshew & Goldstein, 1993) or Asperger syndrome (Bowler, Matthews & Gardiner, 1997). This suggests that individuals with autism may have problems using conceptual relationships in memory. On the other hand, the author’s previous study (Toichi & Kamio, 2002) found that memory performance on tasks not reliant on semantic information was unimpaired or even better than that of age- and ability-matched controls. This leads to the hypothesis that people with autism may be good at remembering stimuli based on sensory information, such as phonological traits or visual characteristics. It follows that in memory tasks it is important to control the type of processing used in encoding to-be-remembered materials.
Also relevant is the role of ‘autonoetic consciousness’, which, accord- ing to Tulving, is necessary for episodic memory (Tulving, 1985; see also Chapter 9, this volume). It has been consistently reported that individuals with autism perform worse than ability-matched comparison participants in remembering what they themselves have done (Boucher, 1981b; Boucher & Lewis, 1989; Millward, Powell & Messer, 2000). A study that directly addressed this issue also reported evidence of reduced autonoetic consciousness in individuals with Asperger syndrome (Bowler, Gardiner & Grice, 2000). These findings suggest that incon- sistent results in previous studies may be partly attributed to the degree to which autonoetic consciouness was involved in the tasks.
The aim of the studies reported here was to examine different aspects of memory in autism taking all of the above points into account. Thus, the participants were adults with HFA; Study 1 re-examined free recall using a conventional memory task; Study 2 examined conceptual relationships in semantic knowledge, using a verbal association task; Study 3 employed a levels-of-processing task to examine the influence of semantic process- ing on episodic memory, as compared to nonsemantic processing; and Study 4 examined the influence of self-related processing on episodic memory. Studies 1 to 4 employed the same autism and comparison participants to exclude confounding factors related to individual differences.
Study 1
In this study, immediate free recall of supraspan unrelated word lists was tested. It is well known that, in this paradigm, typical individuals show superior recall for the first and last few items of a word list, relative to items presented in the middle of the list, phenomena known as the ‘primacy effect’ and ‘recency effect’, respectively. Performance in the primacy and middle regions of the serial position reflects long-term memory (LTM), and performance in the recency region contains both short-term memory (STM) and LTM components (e.g. Craik, 1971). It has also been demon- strated that STM is mediated mainly through auditory or phonological components, and LTM primarily through semantic components (for a review see e.g. Baddeley, 1999). Memory performance was analysed for the three regions (primacy, middle and recency) of word lists.
Methods Participants
The participants were 18 individuals with high-functioning autism (16 men, 2 women) and 18 comparison participants (15 men, 3 women). The autism and comparison groups were matched for age (meanþ SD; 23.0 þ 5.2 and 24.5 þ 7.9, respectively), and for verbal IQ (M¼ 95.3 þ 17.9 and 97.2 þ 19.5) and performance IQ (M ¼ 92.1 þ 14.8 and 91.2þ 19.0) on the Wechsler Adult Intelligence Scale – Revised (Shinagawa et al., 1990). The diagnosis of ‘autism disorder’ was made according to Diagnostic and Statistical Manual of Mental Disorders, 4th edition (DSM-IV; American Psychiatric Association, 1994) criteria by a child psychiatrist, and the experimental participants’ scores on the Childhood Autism Rating Scale (Schopler, Reichler & Renner, 1986) (modified for adult use) ranged between 31 and 46.5 (M¼ 37.4), as assessed by the parents or professional psychologists. None of the partic- ipants had neurological problems or were taking medication, as con- firmed by physical examination and interviews. All participants gave written informed consent prior to participation.
Materials
Two types of word lists (Type A and Type B) were used. Type A lists consisted of abstract nouns such as ‘convenience’ and ‘satisfaction’, and Type B lists consisted of concrete nouns such as ‘orange’ and ‘blackboard’ (see Table 1 of Toichi & Kamio, 2003). Two lists were prepared for each list type, producing four different lists (A-1, A-2, B-1, B-2), and each list contained fifteen words of three or four syllables (mean 3.47 syllables for
Type A, 3.6 for Type B). List items were selected to avoid a phonological or semantic relationship between any two items in the same list. The average word frequency (the occurrence in ninety magazines) was higher for the abstract lists (82.7 and 63.2 for A-1 and A-2, respectively) than for the concrete lists (18.9 and 22.7 for B-1 and B-2, respectively), with no signifi- cant differences between lists of the same type. The average ‘meaningfulness’ (the number of associated words within ten seconds to a stimulus word) was 3.22 and 2.17 per word for the concrete and abstract word lists respectively, with the difference being significant (t¼ 8.2, p <0.0001). All the items in these lists were common words among Japanese adolescents and adults.
Procedure
Participants were tested individually. Words were spoken by an experi- menter at the rate of one per two seconds, and the participant was instructed to write down all the items recalled within two minutes imme- diately following the learning phase. Two free-recall trials were con- ducted successively with a one-minute inter-trial interval. Half the participants in each group were tested using lists A-1 and B-1, and half using lists A-2 and B-2. The order of presentation of list-type was coun- terbalanced. The word order of the list was chosen from three random- izations, counterbalanced across participants.
Analysis
The primacy and recency regions were defined as the first three and the last six items (e.g. Craik, 1971 for review) in the serial positions, respectively. The area between the two regions, which included six items, was called the middle region. The mean probability of correct recall was calculated for each region in each participant. Statistical analyses were conducted using a Group (autism, comparison) Type (concrete, abstract) Position (primacy, middle, recency) analysis of variance (ANOVA).
Results
Figure 8.1 shows correct performance in the two groups in the three regions of interest. The number of recall errors (including intrusions) was small in both groups. The mean (SD) number of errors (per list) was 0.33 (0.59) and 0.22 (0.48) in the autism and comparison groups, res- pectively, with no significant difference between groups (t < 1, df¼ 34). Concerning correct recall, ANOVA revealed a significant main effect of Group (F¼ 4.2, df ¼ 1, 204, p < 0.05), Position (F ¼ 46.6, df ¼ 2, 204, p < 0.0001) and Type (F ¼ 4.1, df ¼ 1, 204, p ¼ < 0.05). There was a significant Group Type interaction (F ¼ 4.2, df ¼ 1, 204, p ¼ 0.04),
with no other significant interactions or double interactions. Post hoc comparisons (Fisher’s PLSD) showed that the recall performances of the primacy region and recency region were better than that of the middle region (p < 0.0001), with better recognition in the recency than primacy region (p¼ 0.005). This indicates that the two groups showed similar serial position effects (i.e. primacy and recency effects) across list types.
The Group Type interaction was attributable to a difference between the two groups in the superiority of recall of concrete as compared to abstract nouns. Post hoc comparisons (Fisher’s PLSD) revealed that con- crete noun recall in the comparison group was significantly better than abstract noun recall in the same group (p < 0.02), and concrete and abstract noun recall in the autism group (p¼ 0.02 and p ¼ 0.02, respectively). On the other hand, there was no significant difference between abstract noun recall in the comparison group and either type of noun recall in the autism group, or between recall of the two word types in the autism group. This indicates that the significant main effect of Type was attributable primarily to the superior recall of concrete over abstract nouns in the comparison group. In summary, performance was better for concrete than abstract nouns in the comparison group, but the two types in the autism group were comparable, and similar to abstract nouns in the comparison group.
Discussion
The main findings of Study 1 replicated those of the author’s previous study (Toichi & Kamio, 2003) which examined individuals with autism
Primacy Middle Recency
0 10 20 30 40 50 60 70 80 90 100 CTL (conc) CTL (abst) HFA (conc) HFA (abst)
Figure 8.1 Correct recall (%) in the three regions. CTL: comparison participants; HFA: participants with high-functioning autism; conc, abst: concrete and abstract word lists, respectively
with a lower IQ than the participants in this study. In the present study, the main effect of Type and that of Group, as well as the Group Type interaction, reached significance. For concrete nouns, the experimental group performed worse than the comparison group in all three serial positions (primacy, middle and recency). Considering that the primacy and middle regions exclusively reflect LTM, with the recency region including STM plus LTM components, the result suggests an impaired LTM for concrete nouns in the autism group. Abstract noun recall in both groups, however, was comparable, suggesting unimpaired memory for abstract nouns in the autism group. It is of interest that abstract noun recall in the two groups was similar to concrete noun recall in the autism group. As explained in the introduction, the nouns in the concrete word lists had higher ‘meaningfulness’ (i.e. they elicited more semantic associations) than those in the abstract word lists. Furthermore, in our previous study (Toichi & Kamio, 2003), the meaningfulness of words was found to correlate with the LTM performance of words in comparison participants but not in those with autism. Considering these findings, along with the semantic nature of LTM described in the introduction, a lack of superiority in the recall of concrete over abstract nouns in the autism group appears to suggest a problem using semantic knowledge at encoding. The next study examined the basic structure of semantic memory knowledge in autism.
Study 2
This study investigated semantic knowledge with a focus on semantic relationships between common words, using an indirect priming techni- que. Semantic priming refers to a phenomenon in which a preceding stimulus (prime) facilitates the processing of a subsequent target stimulus when the prime and target are semantically related (such as ‘robin’ and ‘swallow’). It is believed that this phenomenon is mediated through the associative processing of concepts in semantic memory (Collins & Loftus, 1975). Two components of associative processing have been identified: fast automatic (unconscious) association, which occurs within a few hundred milliseconds, and slow voluntary (conscious) association (Neeley, 1977; Posner & Snyder, 1975). Of the two components of association, this study examined the slow component, using a semantic priming task with a word completion paradigm requiring participants to generate words to fit the word fragments. In the paradigm, targets were word fragments that were difficult to complete without semantic cues. If the semantic relationships between concepts were underdeveloped, the effect of semantic cues to facilitate correct responses (i.e. semantic pri- ming effect) should be small.
The advantage of using a priming task is that it requires little explicit memory ability. Thus it is possible to examine semantic abilities inde- pendent of explicit memory function.
Methods Materials
Single words and word fragments (36 points in size) were presented on a computer display approximately 70 cm from the participant. Letters appeared in black in the centre of the display against a white background. The prime and target words were written in Katakana, which is a set of phonograms used in written Japanese. Each ‘character’ in this syllabary conveys one syllable corresponding to one vowel or a consonant–vowel pair in English. The priming words were nouns and verbs, consisting of three to five letters. The target words were nouns and adjectives, consist- ing of three to five letters with the first letter always presented, and each missing letter replaced by a circle. Two letters were missing from four- letter words, and two or three from five-letter words, with two successive letters never presented. Only one word could be made from each target. Therefore errors, if present, would be due to producing nonwords or incorrect words that did not match the word fragments. College students found it difficult to complete the word fragments without seman- tic cues. Thirty pairs of primesþ targets were used for the test trial. Twenty pairs were semantically related (e.g. ‘bus’–‘train’, ‘war’–‘army’, ‘ice’–‘cold’ and ‘tear’–‘sad’); and ten pairs were semantically unrelated (e.g. ‘television’–‘necktie’). A preparatory study confirmed that the correct response for related and unrelated target words without primes and that for unrelated target words with primes did not differ significantly. Priming effects were therefore evaluated in terms of the ability of related primes, as compared with unrelated primes, to facilitate correct word completion.
Procedure
Participants were tested individually. Prior to test trials, three practice pairs which did not appear in the test trials were presented so that the partic- ipants could understand the test procedure. In the test trials, a prime word was presented for two seconds, during which time the participant was asked to read it aloud to confirm that the prime word had been correctly recognized. The target word fragment was then presented and the partic- ipant was asked to complete it orally. After fifteen seconds, the next prime word was presented, and the same process continued until the last word pair of primesþ targets had been presented. Thus, the stimulus onset asynchrony (SOA) between the prime and target words was two seconds,
with no inter-stimulus interval (ISI). The same (pseudo-random) order was used for all participants, that is, thirty pairs appeared randomly with the restriction that similar semantic relationships (e.g. ‘laugh’–‘funny’ and ‘play’–‘amusing’) did not appear in successive trials.
Results
Percentages of correctly completed word fragments following semanti- cally related and semantically unrelated primes are shown for both groups in Figure 8.2. In both groups, performance for the related items was much better than that for the unrelated items. Relationship (unrelated, related) Group (autism, comparison) repeated-measures analysis of variance (ANOVA) revealed a significant main effect of Relationship (F¼ 244.0, df ¼ 1, 34, p < 0.0001), but neither the main effect of Group (F¼ 2.6, df¼ 1, 34) nor the Relationship Group interaction (F¼ 1.2, df ¼ 1, 34) was significant, indicating that both groups showed similar semantic priming effects.
Discussion
The priming task used in this study examined the associative organization of verbal material in semantic memory. The results of Study 2 replicated those of a previous study of individuals with HFA (Toichi & Kamio, 2001). The findings are also similar to a conceptual priming task by Gardiner, Bowler & Grice (2003). These results suggest that the
Unrelated Related 0 10 20 30 40 50 60 70 80 90 100 Control HFA
Figure 8.2 Correct completion (%) of unrelated and related word fragments. HFA: participants with high-functioning autism
associative organization of concepts underlying simple common words is unimpaired in individuals with autism spectrum disorders. Unimpaired semantic organization has been suggested in studies using word fluency tasks in which participants are asked to generate words in association with a given semantic category (such as ‘animal’ or ‘vehicle’) (e.g. Boucher, 1988); also in a card-sorting task using semantic categories (Tager- Flusberg, 1985a, b) and a Stroop task (Bryson, 1983; Eskes, Bryson & McCormick, 1990). However, a few studies have reported impaired semantic abilities even in individuals with high-functioning autism. In those studies, participants with HFA showed less categorical clustering (Minshew & Goldstein, 1993) or less contextual organization (Fein et al., 1996) than ability-matched comparison groups. These last two studies, however, employed tasks that involved explicit memory components. Such discrepancy in the results suggests that people with HFA may have problems in the relationship between semantic and episodic memory, rather than the structure of semantic knowledge. Study 3 addressed this issue.
Study 3
Semantic processing, or the use of semantic knowledge in encoding words, facilitates recall better than ‘shallow’ (phonological or perceptual) processing. This phenomenon is known as the levels-of-processing effect (Craik & Tulving, 1975). The phenomenon is robust, and has been confirmed in first- and second-grade children (Geis & Hall, 1976, 1978; Owings & Baumeister, 1979) as well as in healthy adults, and even in patients with amnesia (Cermak & Reale, 1978; Cermak, 1979).
The levels-of-processing effect is important in that it provides evidence concerning the relationship between semantic and episodic memory. It is significant, therefore, that a previous study by the author (Toichi & Kamio, 2002) found reduced levels-of-processing effects in young people with autism whose average IQ was around 80. Study 3, reported here, investigated the relationship between episodic memory and semantic memory in adults with HFA using the levels-of-processing task used in the earlier study, which was in turn based on a task originally developed by Craik and Tulving (1975).
Methods Materials
A word list was developed from a pool of common words. Thirty nouns were drawn from the list as targets to be studied. A set of questions about each target was also prepared. There were three ‘levels’ of questions for
each target: graphic, phonological and semantic (see Table 8.1). Graphic questions concerned the type of character (Katakana or Hiragana, both syllabaries for writing Japanese) in which a target word was written. Phonological and semantic questions concerned the pronunciation and meaning of a target word, respectively. The words used in phonological questions were closely similar in pronunciation to the targets (such as ‘attitude’ and ‘altitude’), inducing an intensive phonological encoding. There were two answer types (‘yes’ and ‘no’) for each level of questioning, producing six (3 levels 2 answer types) different questions for each target. Six lists, each consisting of 30 questions, were developed by pairing each of the 30 targets with one question from each of the six alternative questions. Of the 30 questions about the targets to be learned, 10 questions were graphic, 10 phonological, and the remaining 10 were semantic. Half the questions in each set of 10 were the ‘yes’ type, and half the ‘no’ type.
Three word lists were prepared for the recognition test, each containing 30 targets and 60 distractors. The three lists each contained the same 90 words printed on one side of a sheet of paper; however, their arrangement differed.
In addition to the materials to be used at study, as described above, six further target-question pairs were prepared, to be presented before (3 pairs) and after (3 pairs) the 30 pairs on which the participants would be tested. The target words used in these additional target-question pairs did