Synaptic interactions mediating synchrony and oscillations in primate sensorimotor cortex

doi:10.1016/S0928-4257(00)01089-5

Journal of Physiology-Paris

Volume 94, Issues 5–6, 1 December 2000, Pages 323-331

https://doi.org/10.1016/S0928-4257(00)01089-5 Get rights and content

Abstract

The appearance of oscillatory modes of ‘gamma’ activity in many cortical areas of different species has generated interest in understanding their underlying mechanisms and possible functions. This paper reviews evidence from studies on primate motor cortex showing that oscillatory activity entrains many neurons during periods of exploratory manipulative behavior. These oscillatory episodes synchronize widely spread neurons in sensorimotor cortex bilaterally, including descending corticospinal neurons, as evidenced by correlated modulations in EMG activity. The resulting neural synchronization involves task-related and -unrelated neurons similarly, suggesting that it is more likely to play some global role in attention than mediating any obvious interactions involved in coordinating movements. Intracellular recordings have elucidated the strength and types of synaptic interactions between motor cortical neurons that are involved in both normal and oscillatory activity. Spike-triggered averages (STAs) of intracellular membrane potentials have revealed serial connections in the form of unitary excitatory and inhibitory post-synaptic potentials (EPSPs and IPSPs). More commonly, STAs showed large synchronous excitatory or inhibitory potentials (ASEPs and ASIPs) beginning before the trigger spike and composed of multiple unitary events. ASEPs involved synchronous activity in a larger and more widespread group of presynaptic neurons than ASIPs. During oscillatory episodes synchronized excitatory and inhibitory synaptic potentials occurred in varying proportions. EPSPs evoked by stimulating neighboring cortical sites during the depolarizing phase of spontaneous oscillations showed evidence of transient potentiation. These observations are consistent with several functional hypotheses, but fit best with a possible role in attention or arousal.

Introduction

In awake behaving monkeys, sensorimotor cortex neurons display two modes of activity. The predominant mode consists of modulated firing rates, related in relatively reliable ways to specific sensory or motor events. More intermittently, under appropriate behavioral conditions cells can also exhibit transient oscillatory activity in the ‘gamma’ frequency range of 20–40 Hz [3], [10], [17], [19], [20], [21], [25]. Cortical gamma activity has been documented extensively in different cortical areas in many species [1], [4], [5], [13], [15], [16], [22], [24], [26], [29], [30], [31], generating considerable interest in its possible function. The most robust measure of oscillatory activity in primate sensorimotor cortex is the local field potential (LFP); many neurons show a tendency to fire in the negative phase of the LFP oscillations. These two modes of activity are further distinguished by their cortical distribution: the locations of cells with particular types of task-related modulation are somatotopically organized, but the oscillations can occur in phase over wide cortical territories, including pre- and postcentral cortex and both hemispheres. During these coherent oscillations many units at these diverse sites become transiently synchronized. We have investigated the relation of these oscillations and their coherence to behavior in macaque monkeys [19], [20], [21]. Intracellular recordings in awake monkeys have elucidated the synaptic interactions underlying both regular firing and oscillatory activity [6], [7], [8], [18].

Section snippets

Materials and methods

We recorded LFP and unit activity in sensorimotor cortex of three monkeys performing exploratory hand movements to retrieve raisins from the slots of a Klüver board or from unseen locations (the hand of the experimenter, held to the side of the head, which was fixed) [20]. The monkeys also performed alternating wrist movements in a step-tracking task. Cortical activity was recorded with movable tungsten microelectrodes and multiple fixed implanted electrodes. To identify oscillatory cycles, the

Behavioral correlates of oscillations

Gamma frequency oscillations were documented in LFP and unit activity in sensorimotor cortex of three monkeys performing trained wrist movements and untrained exploratory arm and hand movements [20]. The mean frequency of LFP oscillations was about 26 Hz, and the number of cycles per episode was variable, with a mean of 4.2. Neither the frequency nor the number of cycles per episode varied significantly with the observed behavior. However, oscillatory episodes occurred more often during free

Conclusions: possible functions of oscillations

Observations to date indicate that robust intermittent cortical oscillations appear in sensorimotor cortex of awake monkeys, but the data still do not resolve their functional role, if any. The observations are consistent with several hypotheses, including the possibility that oscillations are simply an epiphenomenon of excitability, performing no behavioral function. The problem with this null hypothesis is that the widespread entrainment of neural activity into synchronized bursts would be

Acknowledgments

Supported by National Institutes of Health grants NS12542 and RR00166. We thank Mr Larry Shupe and Mr Jonathan Garlid for technical support and Ms Kate Elias for editorial help.

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View full text

Synaptic interactions mediating synchrony and oscillations in primate sensorimotor cortex

Abstract

Introduction

Section snippets

Materials and methods

Behavioral correlates of oscillations

Conclusions: possible functions of oscillations

Acknowledgments

Clin. Neurophysiol.

Neurosci. Lett.

Trends Neurosci.

Brain Res.

Brain Res.

Int. J. Psychophysiol.

Trends Neurosci.

Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses

Science

The role of synchrony and oscillations in the motor output

Exp. Brain Res.

Synaptic origin and stimulus dependency of neuronal oscillatory activity in the primary visual cortex of the cat

J. Physiol. (Lond.)

Temporal Coding in the Brain

Effect of synchronous neural activity on synaptic transmission in primate cortex

Soc. Neurosci. Abst.

Intracellular correlates of oscillatory activity of cortical neurons in awake behaving monkeys

Soc. Neurosci. Abst.

Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man

J. Physiol. (Lond.)