Primary sensorimotor cortex exhibits complex dependencies of spike-field coherence on neuronal firing rates, field power, and behavior

Author:

Arce-McShane F. I.1ORCID,Sessle B. J.2,Ross C. F.1,Hatsopoulos N. G.13

Affiliation:

1. Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illinois

2. Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada

3. Committees on Computational Neuroscience and Neurobiology, University of Chicago, Chicago, Illinois

Abstract

Spike-field coherence (SFC) is widely used to assess cortico-cortical interactions during sensorimotor behavioral tasks by measuring the consistency of the relative phases between the spike train of a neuron and the concurrent local field potentials (LFPs). Interpretations of SFC as a measure of functional connectivity are complicated by theoretical work suggesting that estimates of SFC depend on overall neuronal activity. We evaluated the dependence of SFC on neuronal firing rates, LFP power, and behavior in the primary motor (MIo) and primary somatosensory (SIo) areas of the orofacial sensorimotor cortex of monkeys ( Macaca mulatta) during performance of a tongue-protrusion task. Although we occasionally observed monotonically increasing linear relationships between coherence and firing rate, we most often found highly complex, nonmonotonic relationships in both SIo and MIo and sometimes even found that coherence decreased with increasing firing rate. The lack of linear relationships was also true for both LFP power and tongue-protrusive force. Moreover, the ratio between maximal firing rate and the firing rate at peak coherence deviated significantly from unity, indicating that MIo and SIo neurons achieved maximal SFC at a submaximal level of spiking. Overall, these results point to complex relationships of SFC to firing rates, LFP power, and behavior during sensorimotor cortico-cortical interactions: coherence is a measure of functional connectivity whose magnitude is not a mere monotonic reflection of changes in firing rate, LFP power, or the relevantly controlled behavioral parameter. NEW & NOTEWORTHY The concern that estimates of spike-field coherence depend on the firing rates of single neurons has influenced analytical methods employed by experimental studies investigating the functional interactions between cortical areas. Our study shows that the overwhelming majority of the estimated spike-field coherence exhibited complex relations with firing rates of neurons in the orofacial sensorimotor cortex. The lack of monotonic relations was also evident after testing the influence of local field potential power and force on spike-field coherence.

Funder

CIHR

HHS | NIH | National Institute of Dental and Craniofacial Research (NIDCR)

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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