Dysregulated Oscillatory Connectivity in the Visual System in Autism Spectrum Disorder

AbstractAutism Spectrum Disorder is increasingly associated with atypical perceptual and sensory symptoms. Here we explore the hypothesis that aberrant sensory processing in Autism Spectrum Disorder could be linked to atypical intra- (local) and inter-regional (global) brain connectivity. To elucidate oscillatory dynamics and connectivity in the visual domain we used magnetoencephalography and a simple visual grating paradigm with a group of 18 adolescent autistic participants and 18 typically developing controls. Both groups showed similar increases in gamma (40-80Hz) and decreases in alpha (8-13Hz) frequency power in occipital cortex. However, systematic group differences emerged when analysing intra- and inter-regional connectivity in detail. Firstly, directed connectivity was estimated using non-parametric Granger causality between visual areas V1 and V4. Feedforward V1-to-V4 connectivity, mediated by gamma oscillations, was equivalent between Autism Spectrum Disorder and control groups, but importantly, feedback V4-to-V1 connectivity, mediated by alpha (8-13Hz) oscillations, was significantly reduced in the Autism Spectrum Disorder group. This reduction was positively correlated with autistic quotient scores, consistent with an atypical visual hierarchy in autism, characterised by reduced top-down modulation of visual input via alpha-band oscillations. Secondly, at the local level in V1, coupling of alpha-phase to gamma amplitude (alpha-gamma phase amplitude coupling, PAC) was reduced in the Autism Spectrum Disorder group. This implies dysregulated local visual processing, with gamma oscillations decoupled from patterns of wider alpha-band phase synchrony (i.e. reduced PAC), possibly due to an excitation-inhibition imbalance. More generally, these results are in agreement with predictive coding accounts of neurotypical perception and indicate that visual processes in autism are less modulated by contextual feedback information.

Download Full-text

Atypical cortical connectivity in autism spectrum disorder (ASD) as measured by magnetoencephalography (MEG)

10.31237/osf.io/42ghu ◽

2019 ◽

Author(s):

Robert A. Seymour ◽

Paul Sowman ◽

Klaus Kessler

Keyword(s):

Autism Spectrum Disorder ◽

Sensory Processing ◽

Perspective Taking ◽

Predictive Coding ◽

Gamma Oscillations ◽

Autism Spectrum ◽

Spectrum Disorder ◽

Alpha Oscillations ◽

Oscillatory Power ◽

Phase Amplitude

Autism Spectrum Disorder (ASD) is a neurodevelopmental condition, characterised by impairments in social interaction and communication, the presence of repetitive behaviours, and multisensory hyper- and hypo-sensitives. This thesis utilised magnetoencephalography, in combination with robust analysis techniques, to investigate the neural basis of ASD. Based on previous research, it was hypothesised that cortical activity in ASD would be associated with disruptions to oscillatory synchronisation during sensory processing, as well as during high-level perspective-taking. More specifically, a novel framework was introduced, based on local gamma-band dysregulation, global hypoconnectivity and deficient predictive-coding. To test this framework, data were collected from adolescents diagnosed with ASD and age-matched controls.Using a visual grating stimulus, it was found that in primary visual cortex, ASD participants had reduced coupling between the phase of alpha oscillations and the amplitude of gamma oscillations (i.e. phase amplitude coupling), suggesting dysregulated visual gamma in ASD. These findings were based on a robust analysis pipeline outlined in Chapter 2. Next, directed connectivity in the visual system was quantified using Granger causality. Compared with controls, ASD participants showed reductions in feedback connectivity, mediated by alpha oscillations, but no differences in inter-regional feedforward connectivity, mediated by gamma oscillations. In the auditory domain, it was found that ASD participants had reduced steady-state responses at 40Hz, in terms of oscillatory power and inter-trial coherence, again suggesting dysregulated gamma. Investigating predictive-coding theories of ASD using an auditory oddball paradigm, it was found that evoked responses to the omission of an expected tone were reduced for ASD participants. Finally, we found reductions in theta-band oscillatory power and connectivity for ASD participants, during embodied perspective-taking. Overall, these findings fit the proposed framework, and demonstrate that cortical activity in ASD is characterised by disruptions to oscillatory synchronisation, at the local and global scales, during both sensory processing and higher-level perspective-taking.Keywords: Autism Spectrum Disorder; Magnetoencephalography; Oscillations; Phase Amplitude Coupling; Connectivity.

Download Full-text

Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions

Autism ◽

10.1177/1362361320926061 ◽

2020 ◽

Vol 24 (7) ◽

pp. 1849-1859

Author(s):

Thijs van Laarhoven ◽

Jeroen J Stekelenburg ◽

Mart LJM Eussen ◽

Jean Vroomen

Keyword(s):

Autism Spectrum Disorder ◽

Brain Activity ◽

Predictive Coding ◽

Sensory Information ◽

Sensory Stimulation ◽

Autism Spectrum ◽

Spectrum Disorder ◽

Prediction Errors ◽

Typical Development ◽

Autism Spectrum Disorder Group

Autism spectrum disorder is a pervasive neurodevelopmental disorder that has been linked to a range of perceptual processing alterations, including hypo- and hyperresponsiveness to sensory stimulation. A recently proposed theory that attempts to account for these symptoms, states that autistic individuals have a decreased ability to anticipate upcoming sensory stimulation due to overly precise internal prediction models. Here, we tested this hypothesis by comparing the electrophysiological markers of prediction errors in auditory prediction by vision between a group of autistic individuals and a group of age-matched individuals with typical development. Between-group differences in prediction error signaling were assessed by comparing event-related potentials evoked by unexpected auditory omissions in a sequence of audiovisual recordings of a handclap in which the visual motion reliably predicted the onset and content of the sound. Unexpected auditory omissions induced an increased early negative omission response in the autism spectrum disorder group, indicating that violations of the prediction model produced larger prediction errors in the autism spectrum disorder group compared to the typical development group. The current results show that autistic individuals have alterations in visual-auditory predictive coding, and support the notion of impaired predictive coding as a core deficit underlying atypical sensory perception in autism spectrum disorder. Lay abstract Many autistic individuals experience difficulties in processing sensory information (e.g. increased sensitivity to sound). Here we show that these difficulties may be related to an inability to process unexpected sensory stimulation. In this study, 29 older adolescents and young adults with autism and 29 age-matched individuals with typical development participated in an electroencephalography study. The electroencephalography study measured the participants’ brain activity during unexpected silences in a sequence of videos of a handclap. The results showed that the brain activity of autistic individuals during these silences was increased compared to individuals with typical development. This increased activity indicates that autistic individuals may have difficulties in processing unexpected incoming sensory information, and might explain why autistic individuals are often overwhelmed by sensory stimulation. Our findings contribute to a better understanding of the neural mechanisms underlying the different sensory perception experienced by autistic individuals.

Download Full-text

Ringing Decay of Gamma Oscillations and Transcranial Magnetic Stimulation Therapy in Autism Spectrum Disorder

Applied Psychophysiology and Biofeedback ◽

10.1007/s10484-021-09509-z ◽

2021 ◽

Author(s):

Manuel F. Casanova ◽

Mohamed Shaban ◽

Mohammed Ghazal ◽

Ayman S. El-Baz ◽

Emily L. Casanova ◽

...

Keyword(s):

Autism Spectrum Disorder ◽

Transcranial Magnetic Stimulation ◽

Magnetic Stimulation ◽

Gamma Oscillations ◽

Autism Spectrum ◽

Spectrum Disorder ◽

Magnetic Stimulation Therapy

Download Full-text

Decreased homotopic interhemispheric functional connectivity in children with autism spectrum disorder

10.1101/2020.11.08.373126 ◽

2020 ◽

Author(s):

Shuxia Yao ◽

Menghan Zhou ◽

Yuan Zhang ◽

Feng Zhou ◽

Qianqian Zhang ◽

...

Keyword(s):

Autism Spectrum Disorder ◽

Functional Connectivity ◽

Symptom Severity ◽

Visual Processing ◽

Brain Networks ◽

Cingulate Cortex ◽

Autism Spectrum ◽

Spectrum Disorder ◽

Volume Changes ◽

Processing Network

AbstractWhile a number of functional and structural changes occur in large-scale brain networks in autism spectrum disorder (ASD), reduced interhemispheric resting state functional connectivity (rsFC) between homotopic regions may be of particular importance as a biomarker. ASD is an early-onset developmental disorder and neural alterations are often age-dependent, reflecting dysregulated developmental trajectories, although no studies have investigated whether homotopic interhemispheric rsFC alterations occur in ASD children. The present study conducted a voxel-based homotopic interhemispheric rsFC analysis in 146 SD and 175 typically developing children under age 10 and examined associations with symptom severity in the Autism Brain Imaging Data Exchange datasets. Given the role of corpus callosum (CC) in interhemispheric connectivity and reported CC volume changes in ASD we additionally examined whether there were parallel volumetric changes in ASD children. Results demonstrated decreased homotopic rsFC in ASD children in the medial prefrontal cortex, precuneus and posterior cingulate cortex of the default mode network (DMN), the dorsal anterior cingulate cortex of the salience network, the precentral gyrus and inferior parietal lobule of the mirror neuron system, the lingual, fusiform and inferior occipital gyri of the visual processing network and thalamus. Symptom severity was associated with homotopic rsFC in regions in the DMN and visual processing network. There were no significant CC volume changes in ASD children. The present study shows that reduced homotopic interhemispheric rsFC in brain networks in ASD adults/adolescents is already present in children of 5-10 years old and further supports their potential use as a general ASD biomarker.

Download Full-text

Interhemispheric alpha-band hypoconnectivity in children with autism spectrum disorder

Behavioural Brain Research ◽

10.1016/j.bbr.2018.04.026 ◽

2018 ◽

Vol 348 ◽

pp. 227-234 ◽

Cited By ~ 8

Author(s):

Abigail Dickinson ◽

Charlotte DiStefano ◽

Yin-Ying Lin ◽

Aaron Wolfe Scheffler ◽

Damla Senturk ◽

...

Keyword(s):

Autism Spectrum Disorder ◽

Children With Autism ◽

Autism Spectrum ◽

Spectrum Disorder ◽

Alpha Band

Download Full-text

Longitudinal associations across vocabulary modalities in children with autism and typical development

Autism ◽

10.1177/1362361317745856 ◽

2018 ◽

Vol 23 (2) ◽

pp. 424-435 ◽

Cited By ~ 2

Author(s):

Kristen Bottema-Beutel ◽

Tiffany Woynaroski ◽

Rebecca Louick ◽

Elizabeth Stringer Keefe ◽

Linda R Watson ◽

...

Keyword(s):

Autism Spectrum Disorder ◽

Children With Autism ◽

Autism Spectrum ◽

Receptive Vocabulary ◽

Spectrum Disorder ◽

Mediation Effect ◽

Typically Developing ◽

Autism Spectrum Disorder Group ◽

Group A ◽

Longitudinal Associations

We examined differences between children with autism spectrum disorder and typically developing children over an 8-month period in: (a) longitudinal associations between expressive and receptive vocabulary and (b) the extent to which caregiver utterances provided within an “optimal” engagement state mediated the pathway from early expressive to later receptive vocabulary. In total, 59 children (28–53 months at Time 1) comprised the autism spectrum disorder group and 46 children (8–24 months at Time 1) comprised the typically developing group. Groups were matched on initial vocabulary sizes. Results showed that the association between early expressive and later receptive vocabulary was moderated by group. A moderated mediation effect was also found, indicating linguistic input provided within an optimal engagement state only mediated associations for the autism spectrum disorder group.

Download Full-text

Increased Dendritic Orientation Dispersion in the Left Occipital Gyrus is Associated with Atypical Visual Processing in Adults with Autism Spectrum Disorder

Cerebral Cortex ◽

10.1093/cercor/bhaa121 ◽

2020 ◽

Vol 30 (11) ◽

pp. 5617-5625

Author(s):

Kiwamu Matsuoka ◽

Manabu Makinodan ◽

Soichiro Kitamura ◽

Masato Takahashi ◽

Hiroaki Yoshikawa ◽

...

Keyword(s):

Autism Spectrum Disorder ◽

Visual Processing ◽

Autism Spectrum ◽

Spectrum Disorder ◽

Sensory Profile ◽

Middle Temporal Gyrus ◽

Adults With Autism ◽

Functional Changes ◽

The Mean ◽

Left Middle Temporal Gyrus

Abstract In autism spectrum disorder (ASD), the complexity-specific hypothesis explains that atypical visual processing is attributable to selective functional changes in visual pathways. We investigated dendritic microstructures and their associations with functional connectivity (FC). Participants included 28 individuals with ASD and 29 typically developed persons. We explored changes in neurite orientation dispersion and density imaging (NODDI) and brain areas whose FC was significantly correlated with NODDI parameters in the explored regions of interests. Individuals with ASD showed significantly higher orientation dispersion index (ODI) values in the left occipital gyrus (OG) corresponding to the secondary visual cortex (V2). FC values between the left OG and the left middle temporal gyrus (MTG) were significantly negatively correlated with mean ODI values. The mean ODI values in the left OG were significantly positively associated with low registration of the visual quadrants of the Adolescent/Adult Sensory Profile (AASP), resulting in a significant positive correlation with passive behavioral responses of the AASP visual quadrants; additionally, the FC values between the left OG and the left MTG were significantly negatively associated with reciprocal social interaction. Our results suggest that abnormal V2 dendritic arborization is associated with atypical visual processing by altered intermediation in the ventral visual pathway.

Download Full-text

Neural features of sustained emotional information processing in autism spectrum disorder

Autism ◽

10.1177/1362361320903137 ◽

2020 ◽

Vol 24 (4) ◽

pp. 941-953 ◽

Cited By ~ 1

Author(s):

Carla A Mazefsky ◽

Amanda Collier ◽

Josh Golt ◽

Greg J Siegle

Keyword(s):

Autism Spectrum Disorder ◽

Emotion Dysregulation ◽

Emotional Processing ◽

Brain Activity ◽

A Priori ◽

Brain Regions ◽

Autism Spectrum ◽

Spectrum Disorder ◽

Typically Developing ◽

Autism Spectrum Disorder Group

Emotion dysregulation is common in autism spectrum disorder; a better understanding of the underlying neural mechanisms could inform treatment development. The tendency toward repetitive cognition in autism spectrum disorder may also increase susceptibility to perseverate on distressing stimuli, which may then increase emotion dysregulation. Therefore, this study investigated the mechanisms of sustained processing of negative information in brain activity using functional magnetic resonance imaging. We used an event-related task that alternated between emotional processing of personally relevant negative words, neutral words, and a non-emotional task. A priori criteria were developed to define heightened and sustained emotional processing, and feature conjunction analysis was conducted to identify all regions satisfying these criteria. Participants included 25 adolescents with autism spectrum disorder and 23 IQ-, age-, and gender-matched typically developing controls. Regions satisfying all a priori criteria included areas in the salience network and the prefrontal dorsolateral cortex, which are areas implicated in emotion regulation outside of autism spectrum disorder. Collectively, activity in the identified regions accounted for a significant amount of variance in emotion dysregulation in the autism spectrum disorder group. Overall, these results may provide a potential neural mechanism to explain emotion dysregulation in autism spectrum disorder, which is a significant risk factor for poor mental health. Lay abstract Many individuals with autism spectrum disorder struggle with emotions that are intense and interfering, which is referred to as emotion dysregulation. Prior research has established that individuals with autism may be more likely than individuals who are not autistic to have repetitive thoughts. It is possible that persistent thoughts about negative or distressing stimuli may contribute to emotion dysregulation in autism spectrum disorder. This study aimed to identify areas of the brain with evidence of persistent processing of negative information via functional magnetic resonance neuroimaging. We used a task that alternated between emotional processing of personally relevant negative words, neutral words, and a non-emotional task. Criteria were developed to define heightened and persistent emotional processing, and analyses were conducted to identify all brain regions satisfying these criteria. Participants included 25 adolescents with autism spectrum disorder and 23 typically developing adolescents who were similar to the autism spectrum disorder group in IQ, age, and gender ratios. Brain regions identified as having greater and continued processing following negative stimuli in the autism spectrum disorder group as compared with the typically developing group included the salience network and the prefrontal dorsolateral cortex. These areas have been previously implicated in emotion dysregulation outside of autism spectrum disorder. Collectively, brain activity in the identified regions was associated with parent-reported emotion dysregulation in the autism spectrum disorder group. These results help to identify a potential process in the brain associated with emotion dysregulation in autism spectrum disorder. This information may be useful for the development of treatments to decrease emotion dysregulation in autism spectrum disorder.

Download Full-text