Spike firing and IPSPs in layer V pyramidal neurons during beta oscillations in rat primary motor cortex (M1) in vitro

Michael G. Lacey, Gerard Gooding-Williams, Emma Jg Prokic, Naoki Yamawaki, Stephen D. Hall, Ian M. Stanford, Gavin L. Woodhall

Research output: Contribution to journalArticle

Abstract

Beta frequency oscillations (10-35 Hz) in motor regions of cerebral cortex play an important role in stabilising and suppressing unwanted movements, and become intensified during the pathological akinesia of Parkinson's Disease. We have used a cortical slice preparation of rat brain, combined with concurrent intracellular and field recordings from the primary motor cortex (M1), to explore the cellular basis of the persistent beta frequency (27-30 Hz) oscillations manifest in local field potentials (LFP) in layers II and V of M1 produced by continuous perfusion of kainic acid (100 nM) and carbachol (5 µM). Spontaneous depolarizing GABA-ergic IPSPs in layer V cells, intracellularly dialyzed with KCl and IEM1460 (to block glutamatergic EPSCs), were recorded at -80 mV. IPSPs showed a highly significant (P< 0.01) beta frequency component, which was highly significantly coherent with both the Layer II and V LFP oscillation (which were in antiphase to each other). Both IPSPs and the LFP beta oscillations were abolished by the GABAA antagonist bicuculline. Layer V cells at rest fired spontaneous action potentials at sub-beta frequencies (mean of 7.1+1.2 Hz; n = 27) which were phase-locked to the layer V LFP beta oscillation, preceding the peak of the LFP beta oscillation by some 20 ms. We propose that M1 beta oscillations, in common with other oscillations in other brain regions, can arise from synchronous hyperpolarization of pyramidal cells driven by synaptic inputs from a GABA-ergic interneuronal network (or networks) entrained by recurrent excitation derived from pyramidal cells. This mechanism plays an important role in both the physiology and pathophysiology of control of voluntary movement generation.

LanguageEnglish
Article numbere85109
Number of pages10
JournalPLoS ONE
Volume9
Issue number1
DOIs
Publication statusPublished - 20 Jan 2014

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Inhibitory Postsynaptic Potentials
Pyramidal Cells
Motor Cortex
gamma-Aminobutyric Acid
Neurons
oscillation
Rats
Brain
neurons
GABA-A Receptor Antagonists
Bicuculline
Kainic Acid
rats
Physiology
Carbachol
Cerebral Cortex
Action Potentials
Parkinson Disease
gamma-aminobutyric acid
Perfusion

Bibliographical note

© 2014 Lacey et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Cite this

Lacey, Michael G. ; Gooding-Williams, Gerard ; Prokic, Emma Jg ; Yamawaki, Naoki ; Hall, Stephen D. ; Stanford, Ian M. ; Woodhall, Gavin L. / Spike firing and IPSPs in layer V pyramidal neurons during beta oscillations in rat primary motor cortex (M1) in vitro. In: PLoS ONE. 2014 ; Vol. 9, No. 1.
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Spike firing and IPSPs in layer V pyramidal neurons during beta oscillations in rat primary motor cortex (M1) in vitro. / Lacey, Michael G.; Gooding-Williams, Gerard; Prokic, Emma Jg; Yamawaki, Naoki; Hall, Stephen D.; Stanford, Ian M.; Woodhall, Gavin L.

In: PLoS ONE, Vol. 9, No. 1, e85109, 20.01.2014.

Research output: Contribution to journalArticle

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AU - Hall, Stephen D.

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AU - Woodhall, Gavin L.

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