An Examination of the Neural Unreliability Thesis of Autism

Butler, John; Molholm, Sophie; Andrade, Gizely N.; Foxe, John J.

doi:10.1093/cercor/bhw375

Cited by 59 publications

(88 citation statements)

References 64 publications

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“…This pattern of results was found across modalities, in visual, auditory, and somatosensory cortices (Dinstein et al, 2012). Similar differences in neural variability were found using resting state measurements in magnetoencephalography (MEG; Domínguez et al, 2013), suggesting that high internal noise is a widespread cortical characteristic of ASD and may represent a fundamental physiological alteration of neural processing (but see, Butler, Molholm, Andrade, & Foxe, 2017;Coskun et al, 2009). At a behavioural level, the impact of internal noise on visual perception in ASD has mostly been investigated in the motion and orientation domain (Manning, Tibber, Charman, Dakin, & Pellicano, 2015;Manning, Tibber, & Dakin, 2017;Park, Schauder, Zhang, Bennetto, & Tadin, 2017;Zaidel, Goin-Kochel, & Angelaki, 2015).…”

Section: Introductionsupporting

confidence: 61%

Internal noise measures in coarse and fine motion direction discrimination tasks, and the correlation with autism traits

Orchard

Dakin

Boxtel

2019

Preprint

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People with autism spectrum disorder (ASD) display abnormalities in motion processing. Motion perception abnormalities in ASD have been linked to high levels of internal noise (unreliable neuronal fluctuations), and deficits in motion pooling (integrating local motion into a global percept). However, the literature overall is equivocal. Traditionally, internal noise in ASD has been investigated through additive internal noise, comparing ASD and control groups. To date, multiplicative internal noise has not been investigated in ASD, and neither type of internal noise has been investigated in relation to traits of autism in the typically-developing population.Here, we investigate how additive and multiplicative internal noise and motion pooling vary across number of autistic traits in typically developed adults. We employed a visual motion integration task with a typically developed population, measuring autistic traits with the Autism Spectrum Questionnaire (AQ). Additive and multiplicative internal noise and motion pooling were calculated from task accuracy and consistency across a range of external noise levels, using a double-pass paradigm.We found that multiplicative noise (but not additive noise, or motion pooling) correlated with AQ. Specifically, multiplicative noise increased with AQ in a coarse motion discrimination task, while it decreased with AQ in a fine motion discrimination task. We suggest that the differences in multiplicative noise may be indicative of decision-variable fluctuations, which are smaller in individuals with a higher number of autistic traits, i.e., they are more focused. Our findings indicate that looking beyond additive noise and incorporating multiplicative noise estimation paradigms can help establish whether there are differences in internal noise levels between individuals with ASD and those without.

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Section: Introductionsupporting

confidence: 61%

Internal noise measures in coarse and fine motion direction discrimination tasks, and the correlation with autism traits

Orchard

Dakin

Boxtel

2019

Preprint

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“…Because there are many variables that have been suggested to indicate neural variability [e.g., Milne, ; Weinger, Zemon, Soorya, & Gordon, ; Haigh et al, ; Arazi et al, ; Butler, Molholm, Andrade, & Foxe, ], it is good practice to apply more than one measure and examine whether there is concordance between the metrics. Measures of neural variability examined in the current study were C1, P1, and N1 variability; intertrial variability in ERP amplitude across the timecourse (timecourse variability); alpha and beta power variability; and EEG SNR.…”

Section: Methodsmentioning

confidence: 99%

Atypical neural variability in carriers of 16p11.2 copy number variants

2019

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Copy number variations (CNVs) at the 16p11.2 chromosomal region are associated with myriad clinical features including intellectual disability and autism spectrum disorder. The aim of this study is to determine whether 16p11.2 deletion (DEL) and duplication (DUP) carriers demonstrate a distinct and reciprocal pattern of electroencephalography (EEG) activity as represented by neural variability measures. EEG data were previously collected as part of the Simons Variation in Individuals Project. Variability measures, as estimated by single-trial ERP and spectral power analyses in the alpha and beta frequency bands, in addition to signal-to-noise ratios (SNRs), were analyzed in DEL (n = 20), DUP (n = 8), and typical (n = 11) groups. We also analyzed mean visual evoked potentials and spectral power (alpha and beta power) to facilitate comparisons with other studies of associated disorders and CNVs. From measures of single-trial variability, we found higher intraparticipant variability in P1 amplitude and timecourse amplitude in DEL compared to controls. Compared to DUP, DEL showed higher variability in absolute alpha and absolute beta power but lower variability in P1 latency. SNRs did not differ between the groups. From measures of amplitude, latency, and spectral power, DUP showed lower relative alpha power compared to controls. Although it is yet unclear whether 16p11.2 CNV dosage impacts neural activity in an opposing manner, findings suggest that 16p11.2 DEL impacts the level of variability of neural responses. Higher neural variability may play a role in a range of cognitive processes in 16p11.2 CNV carriers.Lay Summary: The study analyzed the consistency of patterns of brain waves and rhythms in those affected with a loss or gain of DNA material in the 16p11.2 region. Compared with typical individuals, 16p11.2 deletion carriers showed greater inconsistency in the way the brain responds to the same visual event. This high inconsistency in brain activity may play a role in some core symptoms in 16p11.2 copy number variation carriers.

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“…Using EEG and steady-state visual evoked potentials, another study found reduced signal to noise in individuals with ASD [Weinger, Zemon, Soorya, & Gordon, 2014]. Only two studies have used EEG to examine neural variability through ERP amplitude and/or latency measures after visual, auditory, or tactile stimulation onset in individuals with ASD [Milne, 2011;Butler, Molholm, Andrade, & Foxe, 2017]. Milne found increased variability of the P100 component in these individuals, whereas Butler et al reported no differences across groups on event-related spectral perturbations in somatosensory and visual ERPs.…”

Section: Introductionmentioning

confidence: 99%

Increased Intra‐Subject Variability of Reaction Times and Single‐Trial Event‐Related Potential Components in Children With Autism Spectrum Disorder

et al. 2019

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Autism spectrum disorder (ASD) is an increasingly common neurodevelopmental disorder that affects 1 in 59 children. The cognitive profiles of individuals with ASD are varied, and the neurophysiological underpinnings of these developmental difficulties are unclear. While many studies have focused on overall group differences in the amplitude or latency of event related potential (ERP) responses, recent research suggests that increased intra‐subject neural variability may also be a reliable indicator of atypical brain function in ASD. This study aimed to identify behavioral and neural variability responses during an emotional inhibitory control task in children with ASD compared to typically developing (TD) children. Children with ASD showed increased variability in response to both inhibitory and emotional stimuli, evidenced by greater reaction time variability and single‐trial ERP variability of N200 and N170 amplitudes and/or latencies compared to TD children. These results suggest that the physiological basis of ASD may be more accurately explained by increased intra‐subject variability, in addition to characteristic increases or decreases in the amplitude or latency of neural responses. Autism Res 2020, 13:221–229. © 2019 International Society for Autism Research, Wiley Periodicals, Inc. Lay Summary The cognitive functions including memory, attention, executive functions, and perception, of individuals with ASD are varied, and the physiological underpinnings of these profiles are unclear. In this study, children with ASD showed increased intra‐subject neural and behavioral variability in response to an emotional inhibitory control task compared to typically developing children. These results suggest that the physiological basis of ASD may also be explained by increased behavioral and neural variability in people with ASD, rather than simply characteristic increases or decreases in averaged brain responses.

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An Examination of the Neural Unreliability Thesis of Autism

Cited by 59 publications

References 64 publications

Internal noise measures in coarse and fine motion direction discrimination tasks, and the correlation with autism traits

Internal noise measures in coarse and fine motion direction discrimination tasks, and the correlation with autism traits

Atypical neural variability in carriers of 16p11.2 copy number variants

Increased Intra‐Subject Variability of Reaction Times and Single‐Trial Event‐Related Potential Components in Children With Autism Spectrum Disorder

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