5th Congress Autism-Europe
Articulos / Proceeding
Autism-Spain

EXECUTIVE DISFUNCTION AND MEMORY DEFICITS IN AUTISM

Christopher Jarrold & James Russell

OHP 1: Title Sheet

What I hope to do in this presentation is to give an overview of the work which Jim Russell and I have been carrying out over the past couple of years. As I want to go over a reasonable amount of material in the limited time available, I am afraid that I will only be able to give a rather superficial coverage of this work. My hope, however, is that you will come and ask me more about the talk if you find it interesting and want more details. A related point is that I am conscious that at a conference such as this some of the psychological terminology I will use may be unfamiliar to some of you. Again, in the time available I won't be able to make things as clear as I perhaps should, but do come and talk to me later if anything is unclear.

OHP 2: Introduction

Our research investigates the extent to which autism is associated with what are termed executive deficits. These are relatively high-level psychological functions which are thought to be involved in the deliberate and conscious control of behaviour. Ozonoff et al. define executive control as "...the cognitive construct used to describe goal-directed future-oriented behaviors thought to be mediated by the frontal lobes ... including planning, inhibition of prepotent responses, flexibility, organized search and working memory".

Executive function is often tested using formal neuropsychological tasks thought to tap these abilities, such as the 'Wisconsin Card Sort Test' - a measure of inhibition and flexibility, or the 'Tower of London' - a test of planning. Many studies have shown that individuals with autism perform poorly on these tasks; I've only noted a few key ones here. This has led Ozonoff and others to ask whether executive problems might explain many of the symptoms associated with the condition. There are, however, at least two problems with the proposal that autism is essentially an executive disorder. Firstly, executive deficits are not specific to autism, but are seen in some other developmental disorders, and secondly, the notion of executive control is a nebulous one; we clearly need to be more specific about which particular control problems are seen in autism.

To this end we have investigated memory in autism. One reason for this, which is largely a theoretical one, is that, as the quote from Ozonoff et al. indicates, working memory may be required in tests of executive function. The problems seen in autism on these tasks may therefore be due to working memory deficits specifically. A second, more empirical, motivation follows from the fact that executive deficits are also seen in neurological patients who have suffered damage to the frontal lobes of the brain. These patients show a particular pattern of memory problems, and if we can observe the same pattern of deficits in autism then we will have further evidence that frontal dysfunction may be important in the disorder.

OHP 3: Working Memory and Executive Deficits

Working memory can be defined as holding information in mind in order to guide one's behaviour. For example if I am driving on the continent I need, for the first few minutes or so at least, to consciously remind myself to drive on the right, and not on the left as I am used to. This example might also be seen as an executive task; Pennington writes: "... the extent to which a task taps prefrontal function is a joint product of how strong the prepotent response is (driving on the left) and how difficult it is to maintain the internal representation of context (the need to drive on the right) in working memory." Similarly Goldman-Rakic and Diamond would argue for a link between executive tasks and working memory, and would also claim that working memory is mediated by the frontal lobes of the brain.

So an executive task may require the inhibition of an inappropriate response, and working memory. This can be seen in the Wisconsin Card Sort Test, where the player is required to sort cards on the basis of one rule, perhaps into piles of different colours, and then switch to another rule, perhaps sorting on the basis of shape. When told to switch, the player must hold the new rule in mind, and inhibit responses consistent with the previous rule.

The question we were interested to ask then, was whether the poor performance seen on executive tasks in individuals with autism might reflect a problem in the working memory component of these tasks.

OHP 4: Testing Working Memory

We assessed working memory abilities in three groups of children: children with autism, children with moderate learning difficulties (MLD), and normally-developing children. In this study there were 22 children in each group, and children were matched for verbal mental age (VMA) using the British Picture Vocabulary Test. The verbal mental ages of the groups ranged from around 5 to 10 years, with an average of about 7 years.

We gave these children three tasks, all of which had the same structure, thought to tap working memory. In these so-called 'dual tasks' children see a series of cards one after another, and have to work out the solution to a problem shown on each one while remembering the series of solutions already obtained. So, in this example, four cards are seen, and at the end of the trial the child has to respond with the solutions to each one: response one, response two, response three, response four. In the first of our tasks children had to count the number of dots seen on each card, and remember the series of totals. In the second task children had to identify a dot which differed from the others seen, and remember the series of spatial positions in which these dots appeared. And in the third task the children had to work out a sum on each card, and once again remember the series of totals.

Performance on these tasks was measured in terms of the number of cards children could be given and still correctly remember the series of responses. Though there is not time to give proper details of our results, they were extremely clear - the children with autism were unimpaired, and performed as well as controls on all three tasks. So children with autism do not appear to have working memory problems, at least not as measured here. Having shown this we went on to see whether we could find any other positive evidence of 'frontal' patterns in memory performance.

OHP 5: Frontal Patterns Of Memory

The frontal lobes are thought to be involved in at least two other aspects of memory in addition to working memory. One proposal is that they underpin the strategic recall of information. Incisa Della Rocheta and Milner write: "frontal-lobe lesions result in deficits where retrieval requires deliberate and strategic effort". Evidence for this suggestion comes from a number of studies which have demonstrated impaired free-recall and unimpaired cued recall in frontal patients - the argument here being that free-recall requires the subject to generate retrieval strategies for themselves, while cued recall removes the need to behave strategically. Frontal patients also fail to show strategic behaviours during recall, such as clustering and ordering items into categories.

Interestingly, there is reasonable evidence of similar problems in autism. Boucher and Warrington and Tager-Flusberg have shown impaired free-recall and unimpaired cued recall in autism, and some of the work of Hermelin and O'Connor indicates a failure to utilize semantic information to aid recall. Minshew and her colleagues have carried out studies using the California Verbal Learning Test, and argue that the pattern of deficits seen on this task implies a failure to apply organizational strategies in recall in autism.

The third suggestion for the role of the frontal lobes in memory, put forward primarily by Schacter, is that they are involved in the encoding of spatio-temporal contextual information. Evidence for this proposal comes from the problems shown by frontal patients on tasks which require memory for this type of contextual information, such as re-ordering a sequence of events, making judgements about the relative recency of events, and making 'source memory' discriminations. I will give more details about these tasks in a moment.

So, there is already some evidence of a "frontal" pattern of memory performance in autism, as shown by deficits in strategic recall, though we found no evidence of working memory problems. The question which we asked next was whether we could find problems in the third domain memory for 'spatio-temporal context'.

OHP 6: Testing 'Frontal' Memory

These experiments again assessed children with autism, children with MLD and normally developing children. There were 22 children in each group, and individuals were again matched for verbal mental age. The mental ages ranged from around 5 to 9 years, with a mean of around 7 years in each case.

We presented the three tasks thought to tap spatio-temporal memory which I mentioned briefly on the previous overhead. The first of these was a test of the ability to re-order a series of items in their correct temporal sequence. Children were simply shown twelve picture cards, one at a time. Four cards were of different shapes, four of different colours, and four showed pictures of various toys. These three different categories were blocked, so that all four shapes for example were always presented together, but the order of items within a category was randomised. Following a 15 minute delay the children were shown the cards again, and were asked to order the categories into the sequence in which they had been presented, and then to order the four individual cards within each category. We found that the children with autism were no worse than controls in ordering the three categories correctly, or, as the graph shows, in sorting the four items within each set into the order in which they were presented. Note - the graph shows the kendall's T value for ordering of the four cards in each category set

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The second task assessed children's ability to determine which of two cards had been seen more recently. In each trial, twelve picture cards were shown, one at a time. Four cards were presented in one spatial location, the next four in another spatial context, and the final four in a third position. Then children were then shown two of the cards that had been previously presented, and were asked to decide which they had seen more recently. In half the trials the two test items were drawn from within the same spatial context, but in the other cases the two test items were drawn from adjacent contexts. In the later case the child could potentially use contextual information to aid the recency judgement. Eight trials of each kind were presented, and as the graph shows, the children with autism did not differ from the controls in their performance on either type of judgement.

OHP 7: Testing 'Frontal' Memory Cont. - Source Memory

The third test of memory for spatio-temporal context assessed source memory. Johnson et al. provide a definition of this term: "a variety of characteristics that, collectively, specify the conditions under which a memory is acquired (e.g., the spatial, temporal, and social context of the event; the media and modalities through which it was perceived)". In developmental psychology source memory has typically been assessed by asking children to remember which person carried out certain acts, or to decide whether they themselves performed a particular act, or observed someone else doing it.

We assessed source memory by engaging the children in a game in which they took turns with the experimenter to place picture cards onto a central picture board. As well as laying cards for themselves, the children also placed cards on behalf of a doll partner. The experimenter similarly played cards from two sources, for themselves and for their own doll partner. Twenty four cards were played in total, six from each player or source, with each player taking their turn to play a card in order. After all the cards had been laid we asked the children to try to distribute them back to their original player - in other words could children remember which source each card had come from?

The graph shows the average number of cards, out of 24, which children were able to return correctly. Analysis of these data showed the children with autism were impaired on this measure, and on a number of other measures which we took from the task. This suggests that children with autism do have problems with source memory discriminations, at least as measured here, in contrast to their unimpaired performance on the previous two tasks.

OHP 8: Conclusions

This table provides a summary of our results. In contrast to the predictions described initially, we found that children with autism were not impaired on our tests of working memory. They were similarly unimpaired on two tests of memory for spatio-temporal information - carrying out temporal re-ordering, and making relative recency judgements. However they were clearly impaired on our test of source memory.

What do these findings indicate? Firstly, they suggest that executive problems seen in autism cannot be explained solely in terms of the working memory demands of executive tasks. In other words, children with autism's difficulties on tasks like the Wisconsin Card Sort Test would seem to be due to more 'traditional' executive deficits, such as planning, monitoring and inhibiting action.

Secondly, the absence of clear deficits in spatio-temporal memory and in working memory suggests that the memory problems seen in autism do not mirror those observed in frontal patients. However, as I have already mentioned, there is evidence for some 'frontal' memory problems in autism, namely in strategic recall of information. What we might be seeing in autism therefore is a problem which is in fact more executive than frontal. Rather than observing a deficit on all tasks which frontal patients find difficult, we see impairment when strategic memory is required - indeed Schacter would argue that memory for spatio-temporal information is automatic and not strategic. To the extent that strategic recall might require deliberate planning, monitoring and perhaps, inhibition of the most obvious method of recall, it is potentially executive.

Having said this, how does a problem with source memory fit with this proposal? Well, though Schacter would argue that source memory is an automatic process, others would claim that it does in fact require a strategic approach. In particular it seems that monitoring of action plays an important part in source judgements. Work by Bentall has shown that schizophrenic patients who suffer from hallucinations, thought to be indicative of a problem of monitoring, perform poorly on certain source memory discriminations.

In sum then, our results are inconclusive, and the suggestions I have made are consequently tentative. I think however that we would want to argue that our work counts against global 'frontal' problems in autism, and points instead to more narrowly defined deficits, which may well be executive in nature.