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Curr Biol. 2018 Aug 20;28(16):2515-2526.e4. doi: 10.1016/j.cub.2018.07.009. Epub 2018 Aug 9.

Phase-Locked Stimulation during Cortical Beta Oscillations Produces Bidirectional Synaptic Plasticity in Awake Monkeys.

Author information

1
Center for Bioelectronic Medicine, Feinstein Institute for Medical Research, 350 Community Drive, Manhasset NY 11030, USA; Department of Physiology & Biophysics, University of Washington, 1705 NE Pacific St, Seattle, WA 98195, USA. Electronic address: stavroszanos@gmail.com.
2
Department of Physiology & Biophysics, University of Washington, 1705 NE Pacific St, Seattle, WA 98195, USA. Electronic address: irene.rembado@gmail.com.
3
Division of Neuroscience, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, 6001 Executive Boulevard, Bethesda, MD 20892, USA. Electronic address: dc342b@nih.gov.
4
Department of Physiology & Biophysics, University of Washington, 1705 NE Pacific St, Seattle, WA 98195, USA. Electronic address: fetz@uw.edu.

Abstract

The functional role of cortical beta oscillations, if any, remains unresolved. During oscillations, the periodic fluctuation in excitability of entrained cells modulates transmission of neural impulses and periodically enhances synaptic interactions. The extent to which oscillatory episodes affect activity-dependent synaptic plasticity remains to be determined. In nonhuman primates, we delivered single-pulse electrical cortical stimulation to a "stimulated" site in sensorimotor cortex triggered on a specific phase of ongoing beta (12-25 Hz) field potential oscillations recorded at a separate "triggering" site. Corticocortical connectivity from the stimulated to the triggering site as well as to other (non-triggering) sites was assessed by cortically evoked potentials elicited by test stimuli to the stimulated site, delivered outside of oscillatory episodes. In separate experiments, connectivity was assessed by intracellular recordings of evoked excitatory postsynaptic potentials. The conditioning paradigm produced transient (1-2 s long) changes in connectivity between the stimulated and the triggering site that outlasted the duration of the oscillatory episodes. The direction of the plasticity effect depended on the phase from which stimulation was triggered: potentiation in depolarizing phases, depression in hyperpolarizing phases. Plasticity effects were also seen at non-triggering sites that exhibited oscillations synchronized with those at the triggering site. These findings indicate that cortical beta oscillations provide a spatial and temporal substrate for short-term, activity-dependent synaptic plasticity in primate neocortex and may help explain the role of oscillations in attention, learning, and cortical reorganization.

KEYWORDS:

beta oscillations; closed loop; cortical connectivity; cortical stimulation; nonhuman primates; synaptic plasticity

PMID:
30100342
PMCID:
PMC6108550
DOI:
10.1016/j.cub.2018.07.009
[Indexed for MEDLINE]
Free PMC Article

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