Reduced Hippocampal Functional Connectivity During Episodic Memory Retrieval in Autism

Abstract

Increasing recent research has sought to understand the recollection impairments experienced by individuals with autism spectrum disorder (ASD). Here, we tested whether these memory deficits reflect a reduction in the probability of retrieval success or in the precision of memory representations. We also used functional magnetic resonance imaging (fMRI) to study the neural mechanisms underlying memory encoding and retrieval in ASD, focusing particularly on the functional connectivity of core episodic memory networks. Adults with ASD and typical control participants completed a memory task that involved studying visual displays and subsequently using a continuous dial to recreate their appearance. The ASD group exhibited reduced retrieval success, but there was no evidence of a difference in retrieval precision. fMRI data revealed similar patterns of brain activity and functional connectivity during memory encoding in the 2 groups, though encoding-related lateral frontal activity predicted subsequent retrieval success only in the control group. During memory retrieval, the ASD group exhibited attenuated lateral frontal activity and substantially reduced hippocampal connectivity, particularly between hippocampus and regions of the fronto-parietal control network. These findings demonstrate notable differences in brain function during episodic memory retrieval in ASD and highlight the importance of functional connectivity to understanding recollection-related retrieval deficits in this population.

Keywords: autism; connectivity; fronto-parietal control network; hippocampus; memory retrieval.

Figure 1.

An illustration of the task design, showing a series of displays learnt during encoding and the subsequent memory test on an individual display during the retrieval phase.

Figure 2.

Error distributions across all participants (and all features) within the control and the ASD groups. The number of responses that are distributed uniformly from −180 to 180° (shaded area) is indicative of increased guessing (and lower retrieval success rate) in the ASD group, but the concentration parameter k (describing the response variability) of the von Mises component is similar across the 2 groups.

Figure 3.

(A) Subsequent memory effects in the control and ASD groups, where the ASD group shows an attenuated relationship between LPFC activity and subsequent retrieval success (0–6 features recalled). (B) Activity during the memory retrieval task, where the ASD group shows attenuated LPFC activity relative to the control group. Effects are displayed using bspmviewer at a threshold of P < 0.01 uncorrected for visualization, with the scale reflecting t values.

Figure 4.

(A) The summary node strength measure for each of the 4 seed regions during the memory encoding and retrieval tasks in the control and ASD groups where the ASD group shows significantly reduced HC node strength, only during memory retrieval. (B) Smoothed heat maps illustrating each group's mean correlation between activity of each seed region during the memory retrieval task and regions across the whole brain (summarized as “node strength” for each seed). These images illustrate the general similarity between groups in whole-brain connectivity for the LPFC, MPFC, and PPC seeds, but a marked reduction in HC connectivity strength in the ASD group during memory retrieval. Effects are displayed using SurfIce.

Figure 5.

(A) Images depict connections (mean r > 0.25), with the width of the connection lines weighted by the mean correlation strength, between the HC (node in red) and the DMN (top) and FPCN (bottom) nodes during the memory encoding and retrieval tasks in both the ASD and control groups. The connections between the HC node and the network nodes illustrate the similarity in connectivity during memory encoding but a reduction in HC-network connectivity during memory retrieval in the ASD group, with substantial reductions in connectivity between the HC and FPCN. Images were generated using BrainNet Viewer. (B) Regions showing significantly higher HC connectivity in the control group compared with the ASD group during memory retrieval. Effects are displayed using bspmviewer at a threshold of P < 0.01 uncorrected for visualization, with the scale reflecting t values.