Oscillatory dynamics and functional connectivity during gating of primary somatosensory responses

Alex I. Wiesman, Elizabeth C Heinrichs-Graham, Nathan M. Coolidge, James E. Gehringer, Max J Kurz, Tony W Wilson

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Key Points: Sensory gating is important for preventing excessive environmental stimulation from overloading neural resources. Gating in the human somatosensory cortices is a critically understudied topic, particularly in the lower extremities. We utilize the unique capabilities of magnetoencephalographic neuroimaging to quantify the normative neural population responses and dynamic functional connectivity of somatosensory gating in the lower extremities of healthy human participants. We show that somatosensory processing is subserved by a robust gating effect in the oscillatory domain, as well as a dynamic effect on interhemispheric functional connectivity between primary sensory cortices. These results provide novel insight into the dynamic neural mechanisms that underlie the processing of somatosensory information in the human brain, and will be vital in better understanding the neural responses that are aberrant in gait-related neurological disorders (e.g. cerebral palsy). Abstract: Sensory gating (SG) is a phenomenon in which neuronal responses to subsequent similar stimuli are weaker, and is considered to be an important mechanism for preventing excessive environmental stimulation from overloading shared neural resources. Although gating has been demonstrated in multiple sensory systems, the neural dynamics and developmental trajectory underlying SG remain poorly understood. In the present study, we adopt a data-driven approach to map the spectrotemporal amplitude and functional connectivity (FC) dynamics that support gating in the somatosensory system (somato-SG) in healthy children and adolescents using magnetoencephalography (MEG). These data underwent time-frequency decomposition and the significant signal changes were imaged using a beamformer. Voxel time series were then extracted from the peak voxels and these signals were examined in the time and time-frequency domains, and then subjected to dynamic FC analysis. The results obtained indicate a significant decrease in the amplitude of the neural response following the second stimulation relative to the first in the primary somatosensory cortex (SI). A significant decrease in response latency was also found between stimulations, and each stimulation induced a sharp decrease in FC between somatosensory cortical areas. Furthermore, there were no significant correlations between somato-SG metrics and age. We conclude that somato-SG can be observed in SI in both the time and oscillatory domains, with rich dynamics and alterations in inter-hemispheric FC, and that this phenomenon has already matured by early childhood. A better understanding of these dynamics may provide insight to the numerous psychiatric and neurologic conditions that have been associated with aberrant SG across multiple modalities.

Original languageEnglish (US)
Pages (from-to)1365-1375
Number of pages11
JournalJournal of Physiology
Volume595
Issue number4
DOIs
StatePublished - Feb 15 2017

Fingerprint

Sensory Gating
Somatosensory Cortex
Lower Extremity
Magnetoencephalography
Population Dynamics
Cerebral Palsy
Nervous System Diseases
Automatic Data Processing
Gait
Neuroimaging
Nervous System
Reaction Time
Psychiatry
Healthy Volunteers
Brain

Keywords

  • MEG
  • cortical oscillations
  • development
  • phase coherence

ASJC Scopus subject areas

  • Physiology

Cite this

Oscillatory dynamics and functional connectivity during gating of primary somatosensory responses. / Wiesman, Alex I.; Heinrichs-Graham, Elizabeth C; Coolidge, Nathan M.; Gehringer, James E.; Kurz, Max J; Wilson, Tony W.

In: Journal of Physiology, Vol. 595, No. 4, 15.02.2017, p. 1365-1375.

Research output: Contribution to journalArticle

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