Compensatory Hippocampal Recruitment Supports Preserved Episodic Memory in Autism Spectrum Disorder

Abstract

Background.-The degree to which individuals with autism spectrum disorder (ASD) evidence impairments in episodic memory relative to their typically developing (TD) counterparts remains unclear. According to a prominent view, ASD is associated with deficits in encoding associations between items and recollecting precise context details. Here, we evaluated behavioral and neural evidence for this impaired relational binding hypothesis using a task involving relational encoding and recollection during fMRI.Methods.-Adolescents and young adults (N ASD =47; N TD =60) performed the Relational and Item-Specific Encoding (RiSE) task during fMRI, including item and associative recognition testing. We modelled functional recruitment within the medial temporal lobes (MTL), and connectivity between MTL and the posterior medial (PM) network thought to underlie relational memory. The impaired relational binding model would predict a behavioral deficit driven by aberrant recruitment and connectivity of MTL and the PM network.Results.-The ASD and TD groups showed indistinguishable item and associative recognition performance. During relational encoding, the ASD group demonstrated increased hippocampal recruitment, and decreased connectivity between MTL and PM regions relative to TD. Within ASD, hippocampal recruitment and MTL-PM connectivity were inversely correlated.Conclusions.-The lack of a behavioral deficit in ASD does not support the impaired relational binding hypothesis. Instead, the current data suggest that increased recruitment of the hippocampus compensates for decreased MTL-PM connectivity to support preserved episodic

Exploring the Event‐Related Potentials' Time Course of Associative Recognition in Autism

“…Analysis of the LPC old/new effect showed similar latency and duration in both groups, with a spatial extension to Midline Parietal ROI in the ASD compared to TD group. First, this additional parietal recruitment may suggest a compensatory process, that is, effortful retrieval of associative information, in some similarly with Hogeveen et al [2019] study showing a hippocampal hyperrecruitment due to lower memory strength for individual items—indexed by the reduced FN400 familiarity signal. Second, the pattern of electrophysiological processes—that is, reduced amplitude of the FN400 familiarity potential, while similar amplitude but parietal extension of the LPC recollective potential—may reflect an immature development of memory processes in ASD.…”

“…Second, the item recognition phase in the Hogeveen et al's [2019] study may have reinforced item memory during the subsequent associative recognition phase, as previously demonstrated in elderly TD participants who show binding difficulties [Fine, Shing, & Naveh‐Benjamin, 2018]. Third, only participants who did not show fatigue were tested on the associative recognition phase of Hogeveen et al's [2019] study, which may limit their conclusion that all participants showed preserved relational memory.…”

“…Rather, Solomon, McCauley, Iosif, Carter, and Ragland [2016] identified that adolescents with ASD performed similarly to TD peers for the associative recognition of picture pairs being interactively encoded, with similar recollection awareness, while performing lower at single‐item recognition. Solomon et al's paradigm has further been tested with functional magnetic resonance imaging (fMRI) in a large cohort of adolescents and young adults with and without ASD by Hogeveen et al [2019], who identified similar item and associative recognition performance in both groups. During associative encoding, authors identified a diminished functional connectivity between the medial temporal lobes and the posterior medial network that are mainly involved in associative memory, and increased hippocampal recruitment that may offset this atypical connectivity to support preserved performance.…”

Short‐Term Memory Span and Cross‐Modality Integration in Younger and Older Adults With and Without Autism Spectrum Disorder

“…To explain these findings, Bowler et al [2011] suggested that ASD is characterized by difficulties in relational binding , which gives rise not only to the patterning of memory difficulties described above, but also to other difficulties experienced by autistic people, such as difficulty in mentalizing and problems in utilizing meaning in support of recall [Bowler, Matthews, & Gardiner, 1997; Cooper & Simons, 2019]. Bowler et al [2011] also drew on current neural models of relational binding in episodic memory [Davachi, 2006; Opitz, 2010] to suggest a possible fronto‐hippocampal basis for these difficulties [see Hogeveen, Krug, Geddert, Ragland, & Solomon, 2020; Cooper et al, 2017; Gaigg, Bowler, Ecker, Calvo‐Merino, & Murphy, 2015 for supporting evidence].…”

Linking the Puzzle Pieces of the Past: A Study of Relational Memory in Children with Autism Spectrum Disorder

“…However, evidence is not consistently in favor of specific difficulties in relational memory since some studies have revealed general difficulties in memory for both features in combination and isolation [Cooper et al, 2015; Ring, Gaigg, & Bowler, 2016; Solomon, McCauley, Iosif, Carter, & Ragland, 2016]. In addition, the results of a recent study of young adults with ASD indicate preserved relational memory and memory for single features in ASD resulting from distinct neural compensatory mechanisms [Hogeveen, Krug, Geddert, Ragland, & Solomon, 2020].…”