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Propagating waves mediate information transfer in the motor cortex

Abstract

High-frequency oscillations in the beta range (10–45 Hz) are most active in motor cortex during motor preparation and are postulated to reflect the steady postural state or global attentive state of the animal. By simultaneously recording multiple local field potential signals across the primary motor and dorsal premotor cortices of monkeys (Macaca mulatta) trained to perform an instructed-delay reaching task, we found that these oscillations propagated as waves across the surface of the motor cortex along dominant spatial axes characteristic of the local circuitry of the motor cortex. Moreover, we found that information about the visual target to be reached was encoded in terms of both latency and amplitude of evoked waves at a time when the field phase-locked with respect to the target onset. These findings suggest that high-frequency oscillations may subserve intra- and inter-cortical information transfer during movement preparation and execution.

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Figure 1: Time-frequency analysis of local field potentials in the motor cortex during the instructed-delay reaching task.
Figure 2: Wave propagation in the beta frequency range.
Figure 3: Spatial coherence, phase gradient directionality (PGD) and wave speed.
Figure 4: The direction of propagating waves during the instruction epoch.
Figure 5: Dominant propagation directions of the beta waves on the cortical surface with respect to sulcal landmarks.
Figure 6: Waves evoked by the instruction stimulus.
Figure 7: Information content of instruction stimulus-evoked waves in the beta band.
Figure 8: Target versus movement direction information.

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Acknowledgements

We thank Z. Haga, D. Paulsen and J. Reimer for help with surgical implantation of the arrays, training of monkeys and data collection. We also thank M. Fellows, E. Gunderson and R. Penn for help with surgical procedures. This work was supported by a grant from the Whitehall foundation and a grant R01 NS45853-01 from the US National Institute of Neurological Disease and Stroke, both awarded to N.G.H. K.A.R. received support from a Research Centers in Minority Institutions grant 2G12RR1364-06A1 from the National Center for Research Resources at the US National Institutes of Health.

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Correspondence to Nicholas G Hatsopoulos.

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Competing interests

N.G.H. is a co-founder, board member, and stock holder in a public company, Cyberkinetics Neurotechnology Systems. This company provided the multi-electrode arrays and data acquisition system used in the study reported in the manuscript.

Supplementary information

Supplementary Fig. 1

Beta wave characteristics persist during movement (one second of movement). (PDF 350 kb)

Supplementary Fig. 2

Comparison between the singular value decomposition (SVD) and Hilbert transform methods for analyzing wave propagation. (PDF 152 kb)

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Rubino, D., Robbins, K. & Hatsopoulos, N. Propagating waves mediate information transfer in the motor cortex. Nat Neurosci 9, 1549–1557 (2006). https://doi.org/10.1038/nn1802

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