Abstract
Background
Autism spectrum disorder (ASD) affects many aspects of life, from social interactions
to (multi)sensory processing. Similarly, the condition expresses at a variety of levels
of description, from genetics to neural circuits and interpersonal behavior. We attempt
to bridge between domains and levels of description by detailing the behavioral, electrophysiological,
and putative neural network basis of peripersonal space (PPS) updating in ASD during
a social context, given that the encoding of this space relies on appropriate multisensory
integration, is malleable by social context, and is thought to delineate the boundary
between the self and others.
Methods
Fifty (20 male/30 female) young adults, either diagnosed with ASD or age- and sex-matched
individuals, took part in a visuotactile reaction time task indexing PPS, while high-density
electroencephalography was continuously recorded. Neural network modeling was performed
in silico.
Results
Multisensory psychophysics demonstrates that while PPS in neurotypical individuals
shrinks in the presence of others—as to “give space”—this does not occur in ASD. Likewise,
electroencephalography recordings suggest that multisensory integration is altered
by social context in neurotypical individuals but not in individuals with ASD. Finally,
a biologically plausible neural network model shows, as a proof of principle, that
PPS updating may be inflexible in ASD owing to the altered excitatory/inhibitory balance
that characterizes neural circuits in animal models of ASD.
Conclusions
Findings are conceptually in line with recent statistical inference accounts, suggesting
diminished flexibility in ASD, and further these observations by suggesting within
an example relevant for social cognition that such inflexibility may be due to excitatory/inhibitory
imbalances.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Biological Psychiatry: Cognitive Neuroscience and NeuroimagingAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Prevalence and treatment patterns of autism spectrum disorder in the United States, 2016.JAMA Pediatr. 2019; 173: 153-159
- Sensory perception in autism.Nat Rev Neurosci. 2017; 18: 671-684
- Circuit level defects in the developing neocortex of fragile X mice.Nat Neurosci. 2013; 16: 903-909
- Peripheral mechanosensory neuron dysfunction underlies tactile and behavioral deficits in mouse models of ASDs.Cell. 2016; 166: 299-313
- Dysfunction of cortical GABAergic neurons leads to sensory hyper-reactivity in a Shank3 mouse model of ASD.Nat Neurosci. 2020; 23: 520-532
- Model of autism: Increased ratio of excitation/inhibition in key neural systems.Genes Brain Behav. 2003; 2: 255-267
- Excitation/inhibition imbalance in animal models of autism spectrum disorders.Biol Psychiatry. 2017; 81: 838-847
- Why is visual search superior in autism spectrum disorder?.Dev Sci. 2009; 12: 1083-1096
- The weak coherence account: Detail-focused cognitive style in autism spectrum disorders.J Autism Dev Disord. 2006; 36: 5-25
- Behavioral, perceptual, and neural alterations in sensory and multisensory function in autism spectrum disorder.Prog Neurobiol. 2015; 134: 140-160
- Multisensory integration as a window into orderly and disrupted cognition and communication.Annu Rev Psychol. 2020; 71: 193-219
- Self-motion perception in autism is compromised by visual noise but integrated optimally across multiple senses.Proc Natl Acad Sci U S A. 2015; 112: 6461-6466
- Personal space regulation by the human amygdala.Nat Neurosci. 2009; 12: 1226-1227
- Violations of personal space by individuals with autism spectrum disorder.PLoS One. 2014; 9e103369
- Peripersonal space (PPS) as a multisensory interface between the individual and the environment, defining the space of the self.Neurosci Biobehav Rev. 2019; 99: 138-159
- Multisensory brain mechanisms of bodily self-consciousness.Nat Rev Neurosci. 2012; 13: 556-571
- Peripersonal space as the space of the bodily self?.Cognition. 2015; 144: 49-57
- Unconscious integration of multisensory bodily inputs in the peripersonal space shapes bodily self-consciousness.Cognition. 2017; 166: 174-183
- Shared mapping of own and others’ bodies in visuotactile bimodal area of monkey parietal cortex.J Cogn Neurosci. 2010; 22: 83-96
- Social modulation of peripersonal space boundaries.Curr Biol. 2013; 23: 406-411
- Social perception of others shapes one’s own multisensory peripersonal space.Cortex. 2018; 104: 163-179
- Neural bases of perihand space plasticity through tool-use: Insights from a combined computational-experimental approach.Neuropsychologia. 2010; 48: 812-830
- Visuotactile representation of peripersonal space: A neural network study.Neural Comput. 2010; 22: 190-243
- Extending peripersonal space representation without tool-use: Evidence from a combined behavioral-computational approach.Front Behav Neurosci. 2015; 9: 4
- Altered bodily self-consciousness and peripersonal space in autism.Autism. 2019; 23: 2055-2067
- Visual-tactile spatial multisensory interaction in adults with autism and schizophrenia.Front Psychiatry. 2020; 11: 578401
- Assessing duration discrimination: Psychophysical methods and psychometric function analysis.in: Di Luca M. Vatakis A. Balcı F. Correa Á. Timing and Time Perception: Procedures, Measures, & Applications. Brill, Leiden, the Netherlands2018: 52-78
- The spatial self in schizophrenia and autism spectrum disorder.Schizophr Res. 2017; 179: 8-12
- On the contribution of overt tactile expectations to visuo-tactile interactions within the peripersonal space.Exp Brain Res. 2017; 235: 2511-2522
- Capturing the dynamics of peripersonal space by integrating expectancy effects and sound propagation properties.J Neurosci Methods. 2020; 332: 108534
- Divided attention: Evidence for coactivation with redundant signals.Cogn Psychol. 1982; 14: 247-279
- Optimal multisensory decision-making in a reaction-time task.eLife. 2014; 3e03005
- Multisensory integration: Current issues from the perspective of the single neuron.Nat Rev Neurosci. 2008; 9: 255-266
- Audio-tactile and peripersonal space processing around the trunk in human parietal and temporal cortex: An intracranial EEG study.Cereb Cortex. 2018; 28: 3385-3397
- Peri-personal space encoding in patients with disorders of consciousness and cognitive-motor dissociation.Neuroimage Clin. 2019; 24: 101940
- Superadditivity in multisensory integration: Putting the computation in context.Neuroreport. 2007; 18: 787-792
- On the use of superadditivity as a metric for characterizing multisensory integration in functional neuroimaging studies.Exp Brain Res. 2005; 166: 289-297
- From statistical regularities in multisensory inputs to peripersonal space representation and body ownership: Insights from a neural network model.Eur J Neurosci. 2021; 53: 611-636
- Parameterization of connectionist models.Behav Res Methods Instrum Comput. 2004; 36: 732-741
- Rapid recalibration of peri-personal space: Psychophysical, electrophysiological, and neural network modeling evidence.Cereb Cortex. 2020; 30: 5088-5106
- Neuronal bases of peripersonal and extrapersonal spaces, their plasticity and their dynamics: Knowns and unknowns.Neuropsychologia. 2015; 70: 313-326
- An action field theory of peripersonal space.Trends Cogn Sci. 2018; 22: 1076-1090
- Increased variability but intact integration during visual navigation in autism spectrum disorder.Proc Natl Acad Sci U S A. 2020; 117: 11158-11166
- Multisensory temporal integration in autism spectrum disorders.J Neurosci. 2014; 34: 691-697
- Multisensory speech perception in children with autism spectrum disorders.J Autism Dev Disord. 2013; 43: 2891-2902
- Atypical audiovisual temporal function in autism and schizophrenia: Similar phenotype, different cause.Eur J Neurosci. 2018; 47: 1230-1241
- A computational perspective on autism.Proc Natl Acad Sci U S A. 2015; 112: 9158-9165
- Normalization as a canonical neural computation.Nat Rev Neurosci. 2011; 13: 51-62
- Perceptual bias reveals slow-updating in autism and fast-forgetting in dyslexia.Nat Neurosci. 2019; 22: 256-264
- Adults with autism overestimate the volatility of the sensory environment.Nat Neurosci. 2017; 20: 1293-1299
- Peri-personal space as a prior in coupling visual and proprioceptive signals.Sci Rep. 2018; 8: 15819
- Autistic disturbances of affective contact.Nerv Child. 1943; 2: 217-250
Article Info
Publication History
Published online: April 09, 2021
Accepted:
March 29,
2021
Received in revised form:
March 8,
2021
Received:
December 19,
2020
Identification
Copyright
© 2021 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
