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.
more »
« less
Transformation of speech sequences in human sensorimotor circuits
After we listen to a series of words, we can silently replay them in our mind. Does this mental replay involve a reactivation of our original perceptual dynamics? We recorded electrocorticographic (ECoG) activity across the lateral cerebral cortex as people heard and then mentally rehearsed spoken sentences. For each region, we tested whether silent rehearsal of sentences involved reactivation of sentence-specific representations established during perception or transformation to a distinct representation. In sensorimotor and premotor cortex, we observed reliable and temporally precise responses to speech; these patterns transformed to distinct sentence-specific representations during mental rehearsal. In contrast, we observed less reliable and less temporally precise responses in prefrontal and temporoparietal cortex; these higher-order representations, which were sensitive to sentence semantics, were shared across perception and rehearsal of the same sentence. The mental rehearsal of natural speech involves the transformation of stimulus-locked speech representations in sensorimotor and premotor cortex, combined with diffuse reactivation of higher-order semantic representations.
more »
« less
- Award ID(s):
- 1949730
- NSF-PAR ID:
- 10148244
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 117
- Issue:
- 6
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- 3203 to 3213
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
Abstract Modulation of vocal pitch is a key speech feature that conveys important linguistic and affective information. Auditory feedback is used to monitor and maintain pitch. We examined induced neural high gamma power (HGP) (65–150 Hz) using magnetoencephalography during pitch feedback control. Participants phonated into a microphone while hearing their auditory feedback through headphones. During each phonation, a single real‐time 400 ms pitch shift was applied to the auditory feedback. Participants compensated by rapidly changing their pitch to oppose the pitch shifts. This behavioral change required coordination of the neural speech motor control network, including integration of auditory and somatosensory feedback to initiate change in motor plans. We found increases in HGP across both hemispheres within 200 ms of pitch shifts, covering left sensory and right premotor, parietal, temporal, and frontal regions, involved in sensory detection and processing of the pitch shift. Later responses to pitch shifts (200–300 ms) were right dominant, in parietal, frontal, and temporal regions. Timing of activity in these regions indicates their role in coordinating motor change and detecting and processing of the sensory consequences of this change. Subtracting out cortical responses during passive listening to recordings of the phonations isolated HGP increases specific to speech production, highlighting right parietal and premotor cortex, and left posterior temporal cortex involvement in the motor response. Correlation of HGP with behavioral compensation demonstrated right frontal region involvement in modulating participant's compensatory response. This study highlights the bihemispheric sensorimotor cortical network involvement in auditory feedback‐based control of vocal pitch.
Hum Brain Mapp 37:1474‐1485, 2016 . © 2016 Wiley Periodicals, Inc. -
Little is known about how neural representations of natural sounds differ across species. For example, speech and music play a unique role in human hearing, yet it is unclear how auditory representations of speech and music differ between humans and other animals. Using functional ultrasound imaging, we measured responses in ferrets to a set of natural and spectrotemporally matched synthetic sounds previously tested in humans. Ferrets showed similar lower-level frequency and modulation tuning to that observed in humans. But while humans showed substantially larger responses to natural vs. synthetic speech and music in non-primary regions, ferret responses to natural and synthetic sounds were closely matched throughout primary and non-primary auditory cortex, even when tested with ferret vocalizations. This finding reveals that auditory representations in humans and ferrets diverge sharply at late stages of cortical processing, potentially driven by higher-order processing demands in speech and music.more » « less
-
more » « less
Abstract Objective. Sensorimotor decisions require the brain to process external information and combine it with relevant knowledge prior to actions. In this study, we explore the neural predictors of motor actions in a novel, realistic driving task designed to study decisions while driving.Approach. Through a spatiospectral assessment of functional connectivity during the premotor period, we identified the organization of visual cortex regions of interest into a distinct scene processing network. Additionally, we identified a motor action selection network characterized by coherence between the anterior cingulate cortex (ACC) and dorsolateral prefrontal cortex (DLPFC).Main results. We show that steering behavior can be predicted from oscillatory power in the visual cortex, DLPFC, and ACC. Power during the premotor periods (specific to the theta and beta bands) correlates with pupil-linked arousal and saccade duration.Significance. We interpret our findings in the context of network-level correlations with saccade-related behavior and show that the DLPFC is a key node in arousal circuitry and in sensorimotor decisions. -
more » « less
Abstract The ability to execute a motor plan involves spatiotemporally precise oscillatory activity in primary motor (M1) regions, in concert with recruitment of “higher order” attentional mechanisms for orienting toward current task goals. While current evidence implicates gamma oscillatory activity in M1 as central to the execution of a movement, far less is known about top‐down attentional modulation of this response. Herein, we utilized magnetoencephalography (MEG) during a Posner attention‐reorienting task to investigate top‐down modulation of M1 gamma responses by frontal attention networks in 63 healthy adult participants. MEG data were evaluated in the time–frequency domain and significant oscillatory responses were imaged using a beamformer. Robust increases in theta activity were found in bilateral inferior frontal gyri (IFG), with significantly stronger responses evident in trials that required attentional reorienting relative to those that did not. Additionally, strong gamma oscillations (60–80 Hz) were detected in M1 during movement execution, with similar responses elicited irrespective of attentional reorienting. Whole‐brain voxel‐wise correlations between validity difference scores (i.e., attention reorienting trials—nonreorienting trials) in frontal theta activity and movement‐locked gamma oscillations revealed a robust relationship in the contralateral sensorimotor cortex, supplementary motor area, and right cerebellum, suggesting modulation of these sensorimotor network gamma responses by attentional reorienting. Importantly, the validity difference effect in this distributed motor network was predictive of overall motor function measured outside the scanner and further, based on a mediation analysis this relationship was fully mediated by the reallocation response in the right IFG. These data are the first to characterize the top‐down modulation of movement‐related gamma responses during attentional reorienting and movement execution.
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.1910939117
