Introduction
Besides the well-known difficulties in the areas of social interaction, communication, and flexibility in behaviour (American Psychiatric Association
2013), individuals with Autism Spectrum Disorder (ASD) show a characteristic cognitive profile with strengths and difficulties in areas, such as Theory of Mind (Baron-Cohen et al.
1985; Bowler et al.
2005; Frith and Frith
2003), perception (Frith and Happé
1994; Happé
1999; Mottron and Burack
2001; Mottron et al.
2006; Plaisted et al.
2006,
1998), attention (Allen and Courchesne
2001), executive functions (Hill
2004a,
b), and memory (Boucher and Bowler
2008; Boucher et al.
2012). The present study focuses on the last of these domains, where evidence demonstrates a pattern of relatively preserved memory for single units of information (
item memory), but difficulties in relating these units to one another, or to their spatial and temporal context (
relational memory; see Bowler et al.
2011; Gaigg and Bowler
2012 for reviews). There are some inconsistencies in this literature, however, with some studies suggesting that item memory can be a source of difficulty for individuals with ASD (Cooper et al.
2015; Ring et al.
2016; Solomon et al.
2016), whilst others have shown preserved memory for relational context information (Gras-Vincendon et al.
2007; Lind et al.
2014a; Maister and Plaisted-Grant
2011; Souchay et al.
2013). A number of factors likely contribute to these discrepancies, including the extent to which tasks rely on executive function-related learning strategies (see Solomon et al.
2016), and whether to-be-remembered items are studied in isolation or in the context of other items (e.g., Ring et al.
2016). Another factor that may be involved is the extent to which test performance might be supported by implicit as well as explicit memory for the studied material. Memory difficulties in ASD tend to be more evident in tests of
explicit memory that require the active retrieval of studied information (Tulving
2002), whereas
implicit memory, which operates outside conscious awareness, tends to be preserved (Tulving
2002; Bowler et al.
1997; Gardiner et al.
2003; Renner et al.
2000). It is therefore possible that discrepancies in findings concerning
explicit memory in ASD are partly due to differences in the role that
implicit memory might play in different memory paradigms.
In a study (Ring et al.
2015) that required 25 ASD and 26 age and ability matched typically developing (TD) adults to remember object-locations in pictures of rooms, we have recently found that ASD adults only experienced difficulties in explicitly remembering object-location relations, whereas their implicit memory for the same material was preserved (i.e., they were as likely as TD participants to place objects into studied locations, when explicitly asked to choose new locations). This finding is important because it suggests that relational memory difficulties in ASD arise primarily because of difficulties in retrieving rather than encoding relational information, which has important implications for how memory difficulties might be alleviated in ASD (i.e., by providing support at retrieval; see Bowler et al.
2004). Unfortunately, however, the conclusions drawn from that study were somewhat tempered by ceiling performance in some individuals and floor performance in others. Moreover, the conclusions were at odds with other studies (e.g., Gaigg et al.
2008,
2015), which had suggested that atypical encoding processes do contribute to memory difficulties for relational information in ASD. For instance, Gaigg et al. (
2008) asked participants to study lists of words either with no specific encoding instructions, or with instructions that emphasised item-specific (rate each word on pleasantness) or relational (sort words into categories) information. During subsequent free recall of these lists, the ASD and comparison groups performed similarly following the item-specific encoding instructions but not following the relational or no encoding instructions, where the ASD group performed significantly worse. Since the retrieval conditions were identical across conditions, the authors concluded that the encoding of relational information is a source of difficulty for individuals with ASD.
During our recent object-location memory study referred to above, we had the opportunity to collect eye-movement data for a sub-sample of the participants. These data will be the focus of the current paper because eye-movement data can shed unique light on the encoding and retrieval processes involved in implicit and explicit memory for relational information (e.g., Hannula and Ranganath
2009; Ryan et al.
2000; Ryan and Villate
2009). For example, experiments comparing participants’ eye-movements when looking at scenes that have been manipulated or left unchanged with respect to an earlier study phase demonstrate reliable relational memory effects whereby participants fixate manipulated areas of the scenes more (e.g., Ryan et al.
2000). These
eye-movement-based memory effects operate below the level of awareness (Ryan et al.
2000), and are evident long before participants give an explicit response (Hannula et al.
2007), or even when no explicit response is required (Hannula et al.
2007). Thus, gaze behaviour during retrieval can give insight into implicit memory for relational information. In addition, monitoring gaze behaviour during encoding can reveal how the allocation of attention during study contributes to subsequent relational memory. For example, previous research has shown that the frequency of fixations at encoding is related to overall memory accuracy at test (Molitor et al.
2014; Olsen et al.
2016; Pertzov et al.
2009), and that memory for contextual information is specifically related to a pattern of fixations that is characterised by tightly clustered rather than more evenly spread fixations at encoding (Sharot et al.
2008). Another study has shown that more frequent and longer fixations to objects that are laid out on various surfaces in a three-dimensional space is associated with increased memory for the objects and their specific locations, but not with a more general knowledge about the spatial layout that was presented (Shih et al.
2012). The authors argued that this pattern of results suggests that individuals form a cognitive map of the general layout of their environment within a few fixations and that further fixations aid memory for the specific object-location relations rather than this general layout (Hollingworth and Henderson
2002; Shih et al.
2012). The mechanism of forming cognitive maps has been suspected to function abnormally in autistic individuals (Lind et al.
2013,
2014a; Ring et al.
2017), and to contribute to their memory difficulties (Bigham et al.
2010; Bowler et al.
2004,
2014; Cooper et al.
2015; Gaigg et al.
2014; Lind et al.
2014a,
b; Ni Chuileann and Quigley
2013; Poirier et al.
2011; Ring et al.
2015,
2016; Terrett et al.
2013; Wojcik et al.
2013) and problems with spatial navigation (Lind et al.
2013,
2014a; Pellicano et al.
2011).
Only a few studies to date have examined memory processes in ASD through eye-movement data, with the majority examining memory for faces that is not the focus of the current paper (see Snow et al.
2011; Chawarska and Shic
2009; Hedley et al.
2012). Two studies, however, have focussed on the relation between encoding eye-movements and later memory for non-face stimuli in ASD. Specifically, Loth et al. (
2011) asked participants to read stories and then look at scenes with objects that were either relevant, irrelevant, or neutral in relation to the stories. ASD participants recalled fewer story-relevant objects than TD participants, and eye-movement data pointed to reduced attention to story-relevant information during the initial period of scene viewing. In contrast, Cooper et al. (
2017a) did not find a between-group difference in the number or spatial distribution of fixations at encoding when presenting participants with images of scenes under incidental and intentional learning conditions. When participants were asked to discriminate previously studied from similar lure scenes at test, however, ASD participants’ memory for the scenes was significantly reduced independent of the encoding instruction. Closer examination of the association between gaze data and behavioural performance furthermore showed that while retrieval success was related to the number and spatial distribution of encoding fixations in TD individuals, no such relation was found for persons with ASD. In addition, the extent to which the distribution of fixations at encoding matched the distribution at retrieval was associated with scene memory in TD participants but again not in ASD participants, leading the authors to conclude that scene memory difficulties in ASD arise primarily at the stage of retrieval. These studies show how valuable the measurement of eye-movements can be in the context of memory research in ASD to disentangle the contribution of encoding and retrieval processes.
Given the observations by Loth et al. (
2011) and Cooper et al. (
2017a), the first aim of this study was to examine whether differences in the allocation of attention at encoding may contribute to object-location memory difficulties in ASD. The second aim was to test the prediction that gaze patterns at retrieval would reveal evidence of relational memory difficulties in ASD, with reduced viewing of previously studied compared to non-studied object locations vis-a-vis the comparison group. If this prediction is confirmed, it would indicate that eye-movements could provide a viable method for investigating memory processes in younger and less able individuals with ASD in future studies.
Discussion
Following our recent demonstration of impaired explicit but preserved implicit memory for object–location relations in ASD (Ring et al.
2015), the present study reports on eye-tracking data that we had the opportunity to gather for a sub-sample of the participants involved in that study. Since it is often difficult to disentangle encoding from retrieval processes in behavioural measures of memory, and because it remains unclear to what extent atypical encoding might contribute to atypical retrieval of relational information in ASD, the first aim of this study was to examine how individuals with and without ASD allocate their attention when trying to remember object–locations in complex scenes. The results demonstrated that, ASD and TD participants did not differ overall in how much time they spent looking at the scenes and object locations they were asked to remember. However, when taking subsequent retrieval success into account, it became apparent that encoding-related viewing times differentiated between subsequently remembered versus forgotten object locations only in the TD but not the ASD group. Specifically, TD participants spent more time looking at objects for which they subsequently remembered the scene locations compared to objects for which they forgot the scene locations. This pattern, which replicates the findings of Shih et al. (
2012), was not apparent in the ASD group. Cooper et al. (
2017a) recently reported very similar findings and argued that the absence of a subsequent memory effect in ASD combined with a lack of group differences in overall looking behaviour during encoding suggests that memory retrieval rather than encoding processes are compromised in ASD. This conclusion, however, assumes that ASD participants encode the information they look at in the same way as TD participants, which is at odds with the finding that memory difficulties in ASD vary as a function of encoding condition even when retrieval conditions are held constant (Gaigg et al.
2008,
2015; Toichi and Kamio
2002). The absence of a subsequent memory effect in encoding eye-movements in ASD may therefore also be a reflection of atypical encoding processes such as difficulties in relational binding (e.g., Bowler et al.
2011,
2014) or the use of executive function-related encoding strategies (e.g., Solomon et al.
2016; Southwick et al.
2011). Future studies could shed further light on these issues by systematically examining the effects of various encoding manipulations on eye-movement related subsequent memory effects (see Cooper et al.
2017a).
A second aim of the current study was to establish whether the overt behavioural difficulties individuals with ASD experience in explicitly retrieving relational information might also be revealed in the gaze behaviours of participants. The results suggest that this is indeed the case. Specifically, persons with ASD looked significantly less at the target locations during include trials and less at distracter locations during exclude trials, indicating that reduced memory for object–location relations in ASD can be revealed not only through behavioural tests that require an overt response but also through eye-movement-based data that can be passively recorded (Althoff and Cohen
1999; Ryan et al.
2007). This finding extends evidence of impaired relational memory in ASD to a measure that operates largely outside of conscious awareness and that could therefore be suitable for examining memory functions in under-researched ASD populations, such as individuals with lower intellectual and/or language abilities, or very young individuals with ASD. Expanding research efforts in relation to memory processes to these groups will be critical for the formulation of developmental accounts that try to specify what role atypical memory function might play in the aetiology of ASD in general, and in relation to the heterogeneity of the disorder in particular. For instance, Boucher et al. (
2008) have argued that the patterning of memory strengths and difficulties in different individuals on the autism spectrum might hold the key for understanding the heterogeneity in language development across the spectrum, and eye-tracking methods may prove useful in this context.
The data presented here allow for some speculations about brain regions underlying the memory difficulties observed in ASD. The expression of memory in eye-movements has been found to be related to activity in the hippocampus and prefrontal cortex (PFC; Hannula and Ranganath
2009), and attentional processes underlying differences found in eye-movements during encoding, were found to be related to functions of the medial temporal lobe, PFC, as well as the parietal cortex (Cabeza et al.
2008). Therefore, the current data further support the suggested role of hippocampal–frontal processes in the memory difficulties in ASD (Bowler
2007; Bowler et al.
2011; Minshew and Goldstein
1998). A recent fMRI study by Cooper et al. (
2017b) shows direct evidence for this proposal in presenting reduced connectivity in hippocampal–frontal networks during episodic memory retrieval.
We must acknowledge the modest sample size as a limitation of the present study, and recognise that some caution is warranted in the interpretation of the results, given that the number of analyses across this and the associated Ring et al. (
2015) paper raise concerns over the possibility of Type 1 errors. Another limitation of the current study is the small number of 24 trials for each participant. Splitting up the data by conditions and type of response leaves few trials for the analyses making the results prone to bias. Notwithstanding that further replication will be important, the observations contribute to the literature by extending the recent observations of Cooper et al. (
2017a) in demonstrating that eye-movement data can provide unique insights into the memory difficulties associated with ASD. Moreover, the observations develop the empirical foundations for future studies to examine memory processes in more representative samples, including younger individuals and individuals with language and/or intellectual impairments that remain shamefully underrepresented in the literature.