Differential mirror neuron system (MNS) activation during action observation with and without social-emotional components in autism: a meta-analysis of neuroimaging studies

Abstract

Background Impaired imitation has been found to be an important factor contributing to social communication deficits in individuals with autism spectrum disorder (ASD). It has been hypothesized that the neural correlate of imitation, the mirror neuron system (MNS), is dysfunctional in ASD, resulting in imitation impairment as one of the key behavioral manifestations in ASD. Previous MNS studies produced inconsistent results, leaving the debate of whether “broken” mirror neurons in ASD are unresolved. Methods This meta-analysis aimed to explore the differences in MNS activation patterns between typically developing (TD) and ASD individuals when they observe biological motions with or without social-emotional components. Effect size signed differential mapping (ES-SDM) was adopted to synthesize the available fMRI data. Results ES-SDM analysis revealed hyperactivation in the right inferior frontal gyrus and left supplementary motor area in ASD during observation of biological motions. Subgroup analysis of experiments involving the observation of stimuli with or without emotional component revealed hyperactivation in the left inferior parietal lobule and left supplementary motor during action observation without emotional components, whereas hyperactivation of the right inferior frontal gyrus was found during action observation with emotional components in ASD. Subgroup analyses of age showed hyperactivation of the bilateral inferior frontal gyrus in ASD adolescents, while hyperactivation in the right inferior frontal gyrus was noted in ASD adults. Meta-regression within ASD individuals indicated that the right cerebellum crus I activation increased with age, while the left inferior temporal gyrus activation decreased with age. Limitations This meta-analysis is limited in its generalization of the findings to individuals with ASD by the restricted age range, heterogeneous study sample, and the large within-group variation in MNS activation patterns during object observation. Furthermore, we only included action observation studies which might limit the generalization of our results to the imitation deficits in ASD. In addition, the relatively small sample size for individual studies might also potentially overestimate the effect sizes. Conclusion The MNS is impaired in ASD. The abnormal activation patterns were found to be modulated by the nature of stimuli and age, which might explain the contradictory results from earlier studies on the “broken mirror neuron” debate.

The mirror neuron system compensates for amygdala dysfunction-associated social deficits in individuals with higher autistic traits

“…Similar to an amygdala-damaged patient with intact fear recognition and social network size (Becker et al, 2012;Mihov et al, 2013), healthy individuals with higher autistic traits showed MNS hyperactivity in the same location of the left STS. Although consistent with previous findings in ASD patients (Chan & Han, 2020;Yang & Hofmann, 2016), the current finding of increased STS activation in individuals with subclinical autistic characteristics but intact social interaction indicates the possibility of functional MNS compensation for amygdala pathology in autistic individuals.…”

“…While studies have reported decreased (Dapretto et al, 2006;Ramachandran & Oberman, 2006), or increased (Martineau, Andersson, Barthélémy, Cottier, & Destrieux, 2010;Wadsworth, Maximo, Donnelly, & Kana, 2018) or normal (Dinstein et al, 2010;Marsh & Hamilton, 2011) MNS activity in ASD, two meta-analyses have concluded that MNS hyperactivity is most consistently found (Chan & Han, 2020;Yang & Hofmann, 2016). It has been proposed that MNS dysfunction in ASD is mainly due to abnormal functional connectivity either within the MNS itself, such as in the IFG-STS automatic mimicry route (Hamilton, 2008), or between the MNS and other brain networks that regulate top-down control or social cognitive functions (Hamilton, 2013;Yates & Hobson, 2020).…”

The Atypical Effective Connectivity of Right Temporoparietal Junction in Autism Spectrum Disorder: A Multi-Site Study

“…Next, we performed a mean analysis, i.e., the main meta-analysis method. The main threshold of a p -value < 0.0005 (Chan and Han, 2020 ) and an additional z -based threshold of z > 1 were adopted to reduce the possibility of false-positive results. Then, the recommended extent threshold of 10 voxels was applied to exclude smaller clusters (Radua et al, 2012 ).…”

Neural responses to biological motion distinguish autistic and schizotypal traits in the general population

“…Differential patterns of neural magnitude and synchronization in response to social stimuli may provide important insights into individual differences in social behaviours that are associated with autism and schizophrenia. Those with autism and schizophrenia consistently exhibit atypical neural activity in the network of regions implicated in social perception (Chan & Han, 2020;Glerean et al, 2016;Jáni & Kašpárek, 2017;Mehta, Thirthalli, Aneelraj, Jadhav, Gangadhar, & Keshavan, 2014;Philip, Dauvermann, Whalley, Baynham, Lawrie, & Stanfield, 2012;Yang & Hofmann, 2016). Direct comparisons between those with autism and schizophrenia have revealed comparably atypical neural activity when perceiving a range of social stimuli (Abdi & Sharma, 2014;King & Lord, 2011;Sasson, Pinkham, Carpenter, & Belger, 2011).…”