Effects of Related and Unrelated Context on Recall and Recognition by Adults with High-Functioning Autism Spectrum Disorder

Memory in autism spectrum disorder (ASD) is characterised by greater difficulties with recall rather than recognition and with a diminished use of semantic or associative relatedness in the aid of recall. Two experiments are reported that test the effects of item-context relatedness on recall and recognition in adults with highfunctioning ASD (HFA) and matched typical comparison participants. In both experiments, participants studied words presented inside a red rectangle and were told to ignore context words presented outside the rectangle. Context words were either related or unrelated to the study words. The results showed that relatedness of context enhanced recall for the typical group only. However, recognition was enhanced by relatedness in both groups of participants. On a behavioural level, these findings confirm the Task Support Hypothesis (Bowler, Gardiner & Berthollier, 2004), which states that individuals with ASD will show greater difficulty on memory tests that provide little support for retrieval. The findings extend this hypothesis by showing that it operates at the level of relatedness between studied items and incidentally-encoded context. By showing difficulties in memory for associated items, the findings are also consistent with conjectures that implicate medial temporal lobe and frontal lobe dysfunction in the memory difficulties of individuals with ASD. Memory for context in autism 3 It is now generally agreed that autism spectrum disorder (ASD) covers a range of conditions including the categories of autistic disorder and Asperger disorder (DSM-IV TR; American Psychiatric Association, 2000). The first of these conditions is often accompanied by global intellectual disability, whereas the latter is characterised by normal intelligence and an absence of language difficulties. The failure of many attempts to differentiate the two conditions on measures that are not related to those used to classify them in the first place (see Macintosh & Dissanayake, 2004) has led several researchers to divide ASD conditions into those that are accompanied by global cognitive difficulties (low-functioning autism; LFA) from those that are not (high-functioning autism: HFA). Experimental investigations of memory in individuals with LFA and HFA have shown a pattern of findings characterised by relatively diminished performance on tasks such as free recall, where there is little support for memory at test, especially when semantic or associative relations among studied items can be used to aid recall (Bowler, Matthews & Gardiner, 1997; Bowler, Gardiner, Grice & Saavalainen, 2000b, Tager-Flusberg, 1991, but see Lopez and Leekam, 2003). There is also relatively undiminished performance on tasks such as cued recall, where support is present (Boucher & Warrington, 1976; Bowler, Matthews & Gardiner, 1997). Recognition memory, a supported test procedure, has produced more mixed results, with the majority of studies of HFA individuals showing undiminished performance (Bowler, Gardiner & Grice, 2000a; Bowler et al., 2000b; Gardiner, Bowler & Grice, 2003, but see Bowler, Gardiner & Berthollier, 2004). Level of recognition by individuals with LFA tends to depend on the precise procedure used (see Bowler et al., 2004 for review) but the majority of studies show no evidence of reduced performance. The patterning of memory performance across supported and unsupported test procedures led Bowler et al., (1997) to formulate the Task Support Hypothesis (TSH) which states that individuals with ASD will tend to perform at typical levels on any memory task where support is provided at test. When support is absent, then levels of performance will decline relative to typical comparison participants. Memory for context in autism 4 There is also some evidence that individuals with HFA have diminished memory for source or incidentally-encoded context, especially when that context has to be recalled rather than recognised (see Bowler et al., 2004). Diminished ‘remember’ responses have also been documented in this population (Bowler et al., 2000a; Bowler, Gardiner & Gaigg, 2007). ‘Remember’ responses are thought to reflect the operation of the episodic memory system (Tulving, 1985), which Tulving (2001) argues involves the individual mentally travelling back in time to re-create the spatio-temporal context of the recollected episode. The patterning of memory performance in ASD is strongly suggestive of involvement of the medial temporal and the frontal lobes of the brain. Good recognition in the presence of impaired recall has been documented in individuals with damage to the hippocampus (Aggleton, Vann, Denby et al., 2005; Mayes, Holdstock, Isaac et al., 2002). A similar pattern of impaired recall and recollection with spared recognition and semantic memory has been reported in children with early damage to the hippocampus (Brandt, Gardiner, Vargha-Khadem et al., 2006; Vargha-Khadem, Gadian, Watkins et al., 1997). The hippocampus is thought to be responsible for the integration and relation of elements of experience that are stored elsewhere (Aggleton & Brown, 1999). Such integration underlies the creation of episodic memories and the recall of item-context relations. The frontal lobes are another area of the brain that have been implicated in memory function. Damage to the frontal lobes, although often not producing obvious amnesia, does give rise to a patterning of spared and impaired memory functions that is similar to that seen in ASD (Shimamura, 1996; Wheeler & Stuss, 2003), and ASD is characterised by diminished performance on some executive function tasks that are mediated by the frontal lobes (see Hill, 2004). Moreover, when typical ageing is accompanied by a decline on executive function tasks that are thought to measure frontal lobe function, difficulties with source memory and an increasing need for task support are observed (Craik & Anderson, 1999). Although there have been no direct tests of the relation between memory and medial temporal, hippocampal or frontal function in Memory for context in autism 5 individuals with ASD, there is some neuropathological and imaging evidence that shows abnormalities in these structures in this population (Bauman & Kemper, 1994; Boucher, Cowell, Howard et al., 2005; Casanova, Buxoeveden, Switala & Roy, 2002; Salmond, Ashburner, Connelly et al., 2005). In view of the structural findings and the patterning of memory performance, it is reasonable to hypothesise that individuals with ASD will experience difficulties on memory tasks that involve the integration of disparate elements of experience. This hypothesis has been supported by several investigations. Bowler et al. (2004) have shown intact recognition but diminished recall for incidentally-encoded contextual material in adults with HFA. Context in that study was entirely episodically defined, i.e. it consisted of what happened when participants studied individual items. However, context can also be thought of as including semantically or associatively activated representations of a studied item or of such links among studied items. In this respect, Baddeley (1982) makes the distinction between independent context, which does not affect the meaningful interpretation of the studied material and interactive context, which does. Mayes, MacDonald, Donlan, Pears & Meudell (1992) have shown that typical individuals, in contrast to amnesics with extensive medial temporal lobe damage show greater recognition of target words that had been studied in the presence of interactive context words (e.g. ‘grain’ in the presence of ‘crop’) than words that had been studied alone. On the basis of existing findings on memory in ASD as well as on the the consequences for episodic memory of medial temporal and hippocampal damage, it can be argued that diminished episodic memory in ASD is partly the result of a failure of the influence of context on recall of studied material, especially when the context and the studied items are conceptually related. In the two experiments presented here, we adapted the method developed by Mayes et al. and asked participants with and without HFA to study lists of words, each of which was presented together with either a conceptually related or unrelated word. Participants were instructed to pay attention only to the studied word. At test, participants were asked either to recall (Experiment 1) or to recognise Memory for context in autism 6 (Experiment 2) as many words as they could, irrespective of whether the words occurred inside or outside the box at study. We predicted that for comparison participants, recall and recognition would be higher when studied and context words were related than when they were unrelated. For the HFA participants, we predicted a significantly diminished effect of context on recall but, on the basis of the TSH, no diminished effect under recognition. Because of participant overlap across experiments due limited participant availability, the two experiments were carried out 18 months apart. EXPERIMENT 1 Method Participants Twenty individuals with HFA (3 female, 17 male) and twenty typical individuals (4 female, 16 male) participated in this experiment. Participants with and without HFA were individually matched to within 6 points of Verbal IQ as measured by the WAIS-R or WAIS-III (The Psychological Corporation) and as closely as possible in terms of their Performance IQ, Full scale IQ and age. Table 1 summarises these data. All individuals with HFA had been diagnosed by experienced clinicians according to a range of criteria, and a review of records confirmed that all met DSM-IV criteria for Asperger’s disorder apart from the requirement for absence of clinically significant abnormalities in language or communication development. The Comparison group was recruited via local newspaper advertisement and brief interviews ensured that none had any neurological condition or had a family history of ps