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

Abstract

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.

Temporal resolution relates to sensory hyperreactivity independently of stimulus detection sensitivity in individuals with autism spectrum disorder

“…However, temporal resolution of a discrimination task of a single or double somatosensory stimulus did not correlate with the peak frequency (the frequency with the highest spectral power) in the SI (Baumgarten et al 2017). Instead, our previous study demonstrated that task performance in tactile TOJ was associated with neural activation of the right inferior frontal gyrus in both ASD and TD participants (Ide et al 2020). So far, it has been elucidated that time-based perception demands broader brain functions, such as working memory and interval timing (Buhusi and Meck 2005).…”

“…Indeed, some studies using functional magnetic resonance imaging demonstrated that strong neural responses can be observed in higher-order brain regions including the bilateral frontal and parietal cortices during a TOJ task (Binder 2015;Davis et al 2009;Takahashi et al 2013). Moreover, an ASD individual with sensory hyperreactivity who manifested much superior temporal resolution than that of controls in a TOJ task demonstrated greater neural activity in the left vPMC (Ide et al 2020) where a substantial degree of TOJ-related neural correlates had been reported (Miyazaki et al 2016). Some studies reported that brain areas, such as the putamen and anterior/posterior insular cortices, which are known to be involved in relatively lower-level sensory processing, are 1 2 activated when performing SJ, which is hypothesized to relate generally to the first stage of temporal processing (Kimura et al 2019;Miyazaki et al 2016).…”

“…The high temporal resolution also indicated that they could more precisely judge temporal orders of successive 25-Hz vibrotactile stimuli in a temporal order judgment (TOJ) task compared with that of their TD peers (Tommerdahl et al 2008). An individual with ASD showed extremely high temporal resolution in a TOJ task of vibrotactile stimuli; the resolution was approximately 10-fold better than that of TD controls, and stronger neural activities in the left ventral premotor cortex (vPMC) were identified as neural substrates of the prominent temporal resolution (Ide et al 2020). Another study demonstrated that individuals with ASD with high visual temporal resolution in an SJ task tended to have severe social communication deficits and stereotypic behavior as characteristic ASD symptoms, although there was no difference in temporal resolution between ASD and TD groups (Isaksson et al 2018).…”