Dataset Information

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

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.

SUBMITTER: Zanos S

PROVIDER: S-EPMC6108550 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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

Zanos Stavros S Rembado Irene I Chen Daofen D Fetz Eberhard E EE

Current biology : CB 20180809 16

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 ...[more]

PMID: 30100342

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Project description:We show that a 2-step phospho/dephosphorylation cycle for the alpha-amino-3-hydroxy-5-methyl-4-isoxazole proprionic acid receptor (AMPAR), as used in in vivo learning experiments to assess long-term potentiation (LTP) induction and establishment, exhibits bistability for a wide range of parameters, consistent with values derived from biological literature. The AMPAR model we propose, hence, is a candidate for memory storage and switching behavior at a molecular-microscopic level. Furthermore, the stochastic formulation of the deterministic model leads to a mesoscopic interpretation by considering the effect of enzymatic fluctuations on the Michelis-Menten average dynamics. Under suitable hypotheses, this leads to a stochastic dynamical system with multiplicative noise whose probability density evolves according to a Fokker-Planck equation in the Stratonovich sense. In this approach, the probability density associated with each AMPAR phosphorylation state allows one to compute the probability of any concentration value, whereas the Michaelis-Menten equations consider the average concentration dynamics. We show that bistable dynamics are robust for multiplicative stochastic perturbations and that the presence of both noise and bistability simulates LTP and long-term depression (LTD) behavior. Interestingly, the LTP part of this model has been experimentally verified as a result of in vivo, one-trial inhibitory avoidance learning protocol in rats, that produced the same changes in hippocampal AMPARs phosphorylation state as observed with in vitro induction of LTP with high-frequency stimulation (HFS). A consequence of this model is the possibility of characterizing a molecular switch with a defined biochemical set of reactions showing bistability and bidirectionality. Thus, this 3-enzymes-based biophysical model can predict LTP as well as LTD and their transition rates. The theoretical results can be, in principle, validated by in vitro and in vivo experiments, such as fluorescence measurements and electrophysiological recordings at multiple scales, from molecules to neurons. A further consequence is that the bistable regime occurs only within certain parametric windows, which may simulate a "history-dependent threshold". This effect might be related to the Bienenstock-Cooper-Munro theory of synaptic plasticity.

Dataset Information

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

Publications

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

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