Higher Tactile Temporal Resolution as a Basis of Hypersensitivity in Individuals with Autism Spectrum Disorder

Ide, Masakazu; Yaguchi, Ayako; Sano, Misako; Fukatsu, Reiko; Wada, Makoto

doi:10.1007/s10803-018-3677-8

Cited by 42 publications

(48 citation statements)

References 37 publications

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“…The previously tested sample of children with ASDs [Wada et al, 2015] showed a lower tactile temporal resolution than their age-matched peers, which is consistent with the hypothesis of a developmental delay in individuals with ASDs. In contrast, the tactile temporal resolution of adults with ASDs in our and previous studies [Poole et al, 2015;Ide et al, 2019] was comparable to that of typically developing adults, suggesting that any potential developmental delay in temporal order resolution has been overcome. Notably, tactile temporal order perception and its interactions with external-spatial coding have been related to apparent motion perception [Badde, Röder, & Bruns, 2018;Kitazawa et al, 2008;Takahashi, Kansaku, Wada, Shibuya, & Kitazawa, 2013].…”

Section: Discussioncontrasting

confidence: 69%

Visual and Proprioceptive Influences on Tactile Spatial Processing in Adults with Autism Spectrum Disorders

et al. 2019

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Children with autism spectrum disorders (ASDs) often exhibit altered representations of the external world. Consistently, when localizing touch, children with ASDs were less influenced than their peers by changes of the stimulated limb's location in external space [Wada et al., Scientific Reports 2015, 4(1), 5985]. However, given the protracted development of an external‐spatial dominance in tactile processing in typically developing children, this difference might reflect a developmental delay rather than a set suppression of external space in ASDs. Here, adults with ASDs and matched control‐participants completed (a) the tactile temporal order judgment (TOJ) task previously used to test external‐spatial representation of touch in children with ASDs and (b) a tactile‐visual cross‐modal congruency (CC) task which assesses benefits of task‐irrelevant visual stimuli on tactile localization in external space. In both experiments, participants localized tactile stimuli to the fingers of each hand, while holding their hands either crossed or uncrossed. Performance differences between hand postures reflect the influence of external‐spatial codes. In both groups, tactile TOJ‐performance markedly decreased when participants crossed their hands and CC‐effects were especially large if the visual stimulus was presented at the same side of external space as the task‐relevant touch. The absence of group differences was statistically confirmed using Bayesian statistical modeling: adults with ASDs weighted external‐spatial codes comparable to typically developed adults during tactile and visual‐tactile spatio‐temporal tasks. Thus, atypicalities in the spatial coding of touch for children with ASDs appear to reflect a developmental delay rather than a stable characteristic of ASD. Autism Res 2019, 12: 1745–1757. © 2019 International Society for Autism Research, Wiley Periodicals, Inc. Lay Summary A touched limb's location can be described twofold, with respect to the body (right hand) or the external world (right side). Children and adolescents with autism spectrum disorder (ASD) reportedly rely less than their peers on the external world. Here, adults with and without ASDs completed two tactile localization tasks. Both groups relied to the same degree on external world locations. This opens the possibility that the tendency to relate touch to the external world is typical in individuals with ASDs but emerges with a delay.

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Section: Discussioncontrasting

confidence: 69%

Visual and Proprioceptive Influences on Tactile Spatial Processing in Adults with Autism Spectrum Disorders

et al. 2019

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“…A study showed that ASD had better temporal resolution of vibrotactile stimuli delivered with a synchronized 25-Hz vibrotactile stimuli than typically developing (TD) peers (Tommerdahl et al, 2008). We, however, found no significant difference in tactile temporal resolution (40-Hz and 200-Hz vibrotactile stimuli) between ASD and TD, although individual differences of temporal resolution were associated with the severity of sensory hyper-responsivity (Ide et al, 2019). Miyazaki et al (2016) suggested that the left ventral premotor cortex (vPMC), bilateral dorsal premotor cortex (dPMC), and the left posterior parietal cortex (PPC) extending to the marginal area contiguous to the left superior temporal gyrus (STG) of the motor control network (Kurata, 1993;Pisella et al, 2000) were strongly activated during TOJ task in comparison with a simultaneity judgment task.…”

Section: Introductioncontrasting

confidence: 73%

“…T.R. 's tactile temporal resolution of 6.49 ms studied here fell markedly outside the range of that reported in previous data from healthy subjects (Yamamoto and Kitazawa, 2001;Takahashi et al, 2013;Ide et al, 2019) (e.g. mean: 74 ms; range: 30-131 ms; Yamamoto and Kitazawa, 2001).…”

Section: Discussionsupporting

confidence: 46%

“…Temporal resolution was calculated by fitting the response data in each task to a Gaussian cumulative density function (Yamamoto and Kitazawa, 2001;Ide et al, 2019). The response data were sorted by the SOAs to calculate the order-judgment probability that the right index finger was stimulated later (or the left index finger was stimulated first).…”

Section: Statisticsmentioning

confidence: 99%

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Neural Basis of Extremely High Temporal Sensitivity: Insights From a Patient With Autism

et al. 2020

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The human brain is sensitive to incoming sensory information across multiple time scales. Temporal scales of information represented in the brain generally constrain behavior. Despite reports of the neural correlates of millisecond timing, how the human brain processes sensory stimuli in the sub-second range (≤100 ms) and its behavioral implications are areas of active scientific inquiry. An autism spectrum disorder (ASD) patient showed a tactile discrimination threshold of 6.49 ms on a temporal order judgment (TOJ) task which was approximately 10-fold superior than other ASD and healthy controls (59 and 69 ms, respectively). To investigate the brain regions of this extremely high temporal resolution in the patient, we used functional magnetic resonance imaging (fMRI) during TOJ. We observed greater activity notably in the left superior temporal gyrus (STG) and precentral gyrus (PrG) compared to that of controls. Generally, the left superior frontal gyrus (SFG) correlated positively, while the opercular part of right inferior frontal gyrus (IFG) correlated negatively, with the correct TOJ rate across all subjects (the patient + 22 healthy controls). We found that the performance was negatively correlated with the strength of neural responses in the right IFG overall in 30 participants (the patient + 22 healthy and 7 ASD controls). Our data reveal superior ability of this particular case of ASD in the millisecond scale for sensory inputs. We highlight several neural correlates of TOJ underlying the facilitation and/or inhibition of temporal resolution in humans.

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“…Sensory processing involves registration and modulation of sensory information, as well as an internal organization of afferent inputs (Humphry, 2002). Indeed, sensory hyper-responsiveness is a key feature included in the restricted interests and repetitive behaviors central to an ASD diagnosis (APA, 2013), and some studies have further demonstrated that sensory stimuli detection sensitivity was insufficient to describe the severity of sensory hyperresponsiveness in autism (Ide et al, 2019;Schulz and Stevenson, 2019). Altered sensory processing therefore, may occur in the stream of information processing involving higher-order cognitive processing (Thye et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

GABA Concentration in the Left Ventral Premotor Cortex Associates With Sensory Hyper-Responsiveness in Autism Spectrum Disorders Without Intellectual Disability

et al. 2020

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Individuals with autism spectrum disorder (ASD) often exhibit abnormal processing of sensory inputs from multiple modalities and higher-order cognitive/behavioral response to those inputs. Several lines of evidence suggest that altered γ-aminobutyric acid (GABA), the main inhibitory neurotransmitter in the brain, is a central characteristic of the neurophysiology of ASD. The relationship between GABA in particular brain regions and atypical sensory processing in ASD is poorly understood. We therefore employed 1 H magnetic resonance spectroscopy (1 H-MRS) to examine whether GABA levels in brain regions critical to higher-order motor and/or multiple sensory functions were associated with abnormal sensory responses in ASD. We evaluated atypical sensory processing with a clinically-validated assessment tool. Furthermore, we measured GABA levels in four regions: one each in the primary visual cortex, the left sensorimotor cortex, the left supplementary motor area (SMA), and the left ventral premotor cortex (vPMC). The latter two regions are thought to be involved in executing and coordinating cognitive and behavioral functions in response to multisensory inputs. We found severer sensory hyper-responsiveness in ASD relative to control participants. We also found reduced GABA concentrations in the left SMA but no differences in other regions of interest between ASD and control participants. A correlation analysis revealed a negative association between left vPMC GABA and the severity of sensory hyper-responsiveness across all participants, and the independent ASD group. These findings suggest that reduced inhibitory neurotransmission (reduced GABA) in a higher-order motor area, which modulates motor commands and integrates multiple sensory modalities, may underlie sensory hyper-responsiveness in ASD.

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Higher Tactile Temporal Resolution as a Basis of Hypersensitivity in Individuals with Autism Spectrum Disorder

Cited by 42 publications

References 37 publications

Visual and Proprioceptive Influences on Tactile Spatial Processing in Adults with Autism Spectrum Disorders

Visual and Proprioceptive Influences on Tactile Spatial Processing in Adults with Autism Spectrum Disorders

Neural Basis of Extremely High Temporal Sensitivity: Insights From a Patient With Autism

GABA Concentration in the Left Ventral Premotor Cortex Associates With Sensory Hyper-Responsiveness in Autism Spectrum Disorders Without Intellectual Disability

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