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Meta-Analysis
. 2021:31:102700.
doi: 10.1016/j.nicl.2021.102700. Epub 2021 May 28.

The functional neural architecture of dysfunctional reward processing in autism

Hildegard Janouschek  1 , Henry W Chase  2 , Rachel J Sharkey  1 , Zeru J Peterson  1 , Julia A Camilleri  3 , Ted Abel  4 , Simon B Eickhoff  3 , Thomas Nickl-Jockschat  5
Affiliations
Meta-Analysis

The functional neural architecture of dysfunctional reward processing in autism

Hildegard Janouschek et al. Neuroimage Clin. 2021.

Abstract

Functional imaging studies have found differential neural activation patterns during reward-paradigms in patients with autism spectrum disorder (ASD) compared to neurotypical controls. However, publications report conflicting results on the directionality and location of these aberrant activations. We here quantitatively summarized relevant fMRI papers in the field using the anatomical likelihood estimation (ALE) algorithm. Patients with ASD consistently showed hypoactivations in the striatum across studies, mainly in the right putamen and accumbens. These regions are functionally involved in the processing of rewards and are enrolled in extensive neural networks involving limbic, cortical, thalamic and mesencephalic regions. The striatal hypo-activations found in our ALE meta-analysis, which pooled over contrasts derived from the included studies on reward-processing in ASD, highlight the role of the striatum as a key neural correlate of impaired reward processing in autism. These changes were present for studies using social and non-social stimuli alike. The involvement of these regions in extensive networks associated with the processing of both positive and negative emotion alike might hint at broader impairments of emotion processing in the disorder.

Keywords: ASD; Autism; Connectivity modeling; Meta-analysis; Reward; Striatum.

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Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

Fig. 1
Fig. 1
PRISMA diagram describing the study selection for the meta-analysis. 318 of the 347 publications from the literature research had to be excluded because of the following reasons: no fMRI study, no ASD group, no healthy controls, no comparison between ASD and HC for a reward paradigm, review/essay or comment, no humans, no whole-brain analysis, case-reports, or language neither English nor German. Of the 29 publications included in the qualitative analysis, 6 did not yield a significant result in the whole brain analysis. Therefore, only 23 studies were actively contributing coordinates.
Fig. 2
Fig. 2
Differential neural activations in ASD during reward processing. The ALE meta-analysis which only included hypoactivations resulted in two clusters. The larger of these was located in the right hemisphere centering around the right putamen and right accumbens with its fringes extending to the right caudate nucleus, the right fronto-orbital cortex and the subcallosal cortex (MNI peak coordinates: 12, 10, −10; 161 voxel) (A). The smaller of the two comprised the left accumbens, the left caudate nucleus, the pregenual area and the basal forebrain (MNI peak coordinates: −6, 6, −4; 98 voxel) (B). Pooling over all contrasts yielded a cluster which was located in the right putamen and right accumbens with its fringes extending to the right caudate nucleus, the fronto-orbital cortex and the subcallosal cortex (MNI peak coordinates: 12, 10, −10; 110 voxel) (C).
Fig. 3
Fig. 3
Functional changes during reward processing (red) do not overlap with structural alterations in the basal ganglia (blue) in ASD The clusters resulting from our ALE meta-analysis on reward processing in ASD (red) do not overlap with the clusters from a previous ALE meta-analysis on structural alterations in ASD (yellow) (Nickl-Jockschat et al., 2012). However, the cluster in the right caudate nucleus from the ALE on structural changes in ASD was directly adjacent to the right hemispheric putamen-accumbens cluster from the current ALE on reward processing in ASD. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 4
Fig. 4
Overview over the consensus connectivity networks (CCNs) derived from the clusters of our ALE meta-analysis on reward processing in ASD. Fig. 4A shows the CCN which used the right putamen - accumbens cluster from the TDC > ASD ALE as seed region. The CCN shows an extensive coactivation pattern, which is focused on the basal ganglia, thalamus, amygdala and insula, but also extends to the operculum, frontal orbital cortex and midbrain. It also includes the cingulate and paracingulate gyrus and the subcallosal cortex. The CCN which used the left hemispheric cluster in the left caudate, left accumbens and pregenual cortex from the TDC > ASD ALE as a seed region (Fig. 4B) shows a similar co-activation pattern as the former cluster. Fig. 4C depicts the CCN which used the right hemispheric putamen accumbens cluster from the ALE which pooled over all contrasts as a seed region. The CCN shows bilateral connectivity involving the basal ganglia, thalamus, insula, subcallosal, cingulate and paracingulate cortex, the frontal operculum, fronto-orbital cortex and the midbrain.
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