Autism spectrum disorder (ASD) is a neurodevelopmental syndrome characterized by impairments in social perception and communication. Growing evidence suggests that the relationship between deficits in social perception and ASD may extend into the neurotypical population. In electroencephalography (EEG), high autism-spectrum traits in both ASD and neurotypical samples are associated with changes to the mu rhythm, an alpha-band (8–12 Hz) oscillation measured over sensorimotor cortex which typically shows reductions in spectral power during both one’s own movements and observation of others’ actions. This mu suppression is thought to reflect integration of perceptual and motor representations for understanding of others’ mental states, which may be disrupted in individuals with autism-spectrum traits. However, because spectral power is usually quantified at the group level, it has limited usefulness for characterizing individual variation in the mu rhythm, particularly with respect to autism-spectrum traits. Instead, individual peak frequency may provide a better measure of mu rhythm variability across participants. Previous developmental studies have linked ASD to slowing of individual peak frequency in the alpha band, or peak alpha frequency (PAF), predominantly associated with selective attention. Yet individual variability in the peak mu frequency (PMF) remains largely unexplored, particularly with respect to autism-spectrum traits. Here we quantified peak frequency of occipitoparietal alpha and sensorimotor mu rhythms across neurotypical individuals as a function of autism-spectrum traits. High-density 128-channel EEG data were collected from 60 participants while they completed two tasks previously reported to reliably index the sensorimotor mu rhythm: motor execution (bimanual finger tapping) and action observation (viewing of whole-body human movements). We found that individual measurement in the peak oscillatory frequency of the mu rhythm was highly reliable within participants, was not driven by resting vs. task states, and showed good correlation across action execution and observation tasks. Within our neurotypical sample, higher autism-spectrum traits were associated with slowing of the PMF, as predicted. This effect was not likely explained by volume conduction of the occipitoparietal PAF associated with attention. Together, these data support individual peak oscillatory alpha-band frequency as a correlate of autism-spectrum traits, warranting further research with larger samples and clinical populations.
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The primacy of rhythm: how discrete actions merge into a stable rhythmic pattern
This study examined how humans spontaneously merge a sequence of discrete actions into a rhythmic pattern, even when periodicity is not required. Two experiments used a virtual throwing task, in which subjects performed a long sequence of discrete throwing movements, aiming to hit a virtual target. In experiment 1, subjects performed the task for 11 sessions. Although there was no instruction to perform rhythmically, the variability of the interthrow intervals decreased to a level comparable to that of synchronizing with a metronome; furthermore, dwell times shortened or even disappeared with practice. Floquet multipliers and decreasing variability of the arm trajectories estimated in state space indicated an increasing degree of dynamic stability. Subjects who achieved a higher level of periodicity and stability also displayed higher accuracy in the throwing task. To directly test whether rhythmicity affected performance, experiment 2 disrupted the evolving continuity and periodicity by enforcing a pause between successive throws. This discrete group performed significantly worse and with higher variability in their arm trajectories than the self-paced group. These findings are discussed in the context of previous neuroimaging results showing that rhythmic movements involve significantly fewer cortical and subcortical activations than discrete movements and therefore may pose a computationally more parsimonious solution. Such emerging stable rhythms in neuromotor subsystems may serve as building blocks or dynamic primitives for complex actions. The tendency for humans to spontaneously fall into a rhythm in voluntary movements is consistent with the ubiquity of rhythms at all levels of the physiological system. NEW & NOTEWORTHY When performing a series of throws to hit a target, humans spontaneously merged successive actions into a continuous approximately periodic pattern. The degree of rhythmicity and stability correlated with hitting accuracy. Enforcing irregular pauses between throws to disrupt the rhythm deteriorated performance. Stable rhythmic patterns may simplify control of movement and serve as dynamic primitives for more complex actions. This observation reveals that biological systems tend to exhibit rhythmic behavior consistent with a plethora of physiological processes.
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- Award ID(s):
- 1637854
- NSF-PAR ID:
- 10124689
- Date Published:
- Journal Name:
- Journal of Neurophysiology
- Volume:
- 121
- Issue:
- 2
- ISSN:
- 0022-3077
- Page Range / eLocation ID:
- 574 to 587
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1152/jn.00587.2018
