Clinical StudyIncreased premotor cortex activation in high functioning autism during action observation
Introduction
Autism spectrum disorders (ASD) are pervasive, neurodevelopmental conditions, with a prevalence of approximately 1–2% of the population [1], [2]. According to the Diagnostic and Statistical Manual V (DSM V) [3], ASD is characterized by anomalies in two key domains: social communication, and repetitive and/or stereotyped patterns of behaviour. At present, the phenotype is broad and ill-defined where diagnosis is made on the basis of behavioural presentation.
In 1999, two research groups independently suggested that a network of visuomotor cells, mirror neurons (MN), might be a potential biomarker to ASD [4], [5]. MN can be distinguished from other motor neurons by discharging both when an individual performs an action (such as reaching for food), and when an individual watches another performing a similar action (such as a friend reaching for some food) [6]. Research using techniques such as functional MRI (fMRI) [7], [8], transcranial magnetic stimulation [9] and electroencephalography (EEG) [10] provide indirect evidence that MN constitute a fronto-parieto network in humans. These regions are the premotor cortex (PMC), the pars opercularis of the inferior frontal gyrus, the inferior parietal lobule and the superior temporal sulcus [11], [12], [13]. More recent depth electrode research on humans suggests neurons with mirror properties are located in supplementary motor areas and medial temporal areas, in addition to non-significant quantities in the anterior cingulate cortex (ACC) [14].
It has been theorized that MN may be a neural substrate to simulation-based theories of how we understand the actions of other people [15]. This theoretical link has prompted research into the potential role of MN in ASD. To date, EEG research has revealed evidence of both typical [16], [17] and atypical [4], [18], [19], [20] MN response in ASD. Regarding fMRI research, findings have been mixed. During observation of emotional stimuli, there is evidence of reduced [21], [22], [23] blood oxygen level dependent (BOLD) response in regions believed to possess MN in ASD compared to typically developing (TD) individuals. In contrast, paradigms requiring observation of non-emotional hand based actions have revealed both increased [24], [25] and equivalent [26], [27] BOLD responses in mirror regions of ASD compared to TD participants. These studies on hand actions have varied considerably in what stimuli are used as a baseline condition, including a non-moving hand [25], a blank screen [26] and geometric patterns [27], which is likely to contribute to the mixed findings.
Using fMRI, the present study will compare BOLD response of participants with high functioning autism and Asperger’s syndrome (HFA/AS) to TD individuals. Videos of goal directed hand actions will be contrasted with still images of a non-moving hand, making the paradigm comparable to previous research which reported a heightened BOLD response in MN regions in ASD [24], [25]. Based upon this limited literature, two hypotheses were generated. Firstly, that both groups would demonstrate significantly increased BOLD response in MN regions during observation of hand actions as compared to baseline. Secondly, when contrasting the groups, the HFA/AS group will demonstrate increased BOLD in frontal, parietal and temporal MN areas as compared to TD participants.
Section snippets
Participants
The present study compared 12 TD participants (mean age = 19.75 years) with 12 individuals who had a previous diagnosis of either autistic disorder or AS (mean age = 18.50 years). Participants with HFA/AS were recruited from various autism support organizations (such as Autism Victoria) and specialist schools (such as Western Autism). In this study, all participants were male, and the age range was from 16–30 years. An experienced clinical psychologist who has worked extensively in the autism field
Within group analysis
For both groups a significant signal increase was observed in all hypothesized MN regions, comprised of pre-frontal (pars opercularis, PMC), parietal (supramarginal gyrus) and temporal (superior temporal sulcus) regions. During the hand observation task, several other voxel clusters demonstrated a similar pattern of activation in both groups, corresponding to visual (middle occipital gyrus) and frontal (inferior and middle frontal gyrus) regions. Participants with HFA/AS demonstrated additional
Discussion
Using fMRI, the present study contrasted BOLD response of participants with HFA/AS to TD participants whilst observing hand actions. The first hypothesis that both groups would demonstrate a significant BOLD increase in MN regions during action observation compared to baseline was supported. Within group analyses demonstrated signal increases in frontal (BA6, BA44), parietal (BA40) and temporal (BA22) MN regions bilaterally in both groups. Activation in these brain regions whilst observing
Conflicts of Interest/Disclosures
The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication.
Acknowledgments
The authors would like to thank all participants in this study and the MRI radiographers at the Brain Research Institute. The authors would also like to acknowledge the assistance of Danny Flanagan throughout this research, and Shawna Farquarson whose patience and technical expertise was greatly appreciated.
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2020, Research in Autism Spectrum DisordersCitation Excerpt :Studies that have reported abnormalities in PMC activation during action observation in ASD are rare. Two studies (Perkins, Bittar, McGillivray, Cox, & Stokes, 2015; Williams et al., 2006) found evidence of increased activation of the right PMC in participants with ASD compared to TD during observation and/or imitation of hand actions. The first study used a finger-tapping task and found greater PMC activation in ASD during imitation than execution of an action in ASD, but not TD.
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2018, Behavioural Brain ResearchCitation Excerpt :Despite both groups activating core regions of the MNS, one of the specific regions of differential activation was the left PMv, with increased activation in ASD participants during intransitive actions, which required individuals to imagine in a more “communicative” context. Increased left PMv activation in ASD is consistent with recent findings of increased activation in imitation tasks in adolescents with ASD in the MNS [45]. Difficulty in intransitive actions in ASD may elicit more brain resources in the MNS.
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2017, NeuroscienceCitation Excerpt :Although participants were instructed to mirror the model’s hand in our study, which could be interpreted as a goal-directed action, the model’s hand portrayed static action poses and not action sequences. For example, in some recent fMRI studies there were action sequences (depicted as videos) involving a hand reaching for an object (Marsh and Hamilton, 2011; Perkins et al., 2015; Pokorny et al., 2015). Some previous paradigms using static and dynamic stimuli have elicited activation in AIN and action observation regions.