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Spontaneous slow wave oscillations in extracellular field potential recordings reflect the alternating dominance of excitation and inhibition

Zheng, Y. ORCID: https://orcid.org/0000-0001-7472-6427, Kang, S., O'Neill, J. and Bojak, I. ORCID: https://orcid.org/0000-0003-1765-3502 (2024) Spontaneous slow wave oscillations in extracellular field potential recordings reflect the alternating dominance of excitation and inhibition. Journal of Physiology. ISSN 1469-7793

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To link to this item DOI: 10.1113/JP284587

Abstract/Summary

At resting state, cortical neurons can fire action potentials spontaneously but synchronously (Up state), followed by a quiescent period (Down state) before the cycle repeats. Extracellular recordings in the infragranular layer of cortex with a micro-electrode display a negative deflection (depth-negative) during Up states and a positive deflection (depth-positive) during Down states. The resulting Slow Wave Oscillation (SWO has been studied extensively during sleep and under anaesthesia. However, recent research on the balanced nature of synaptic excitation and inhibition has highlighted our limited understanding of its genesis. Specifically, are excitation and inhibition balanced during SWOs? We analyse spontaneous local field potentials (LFPs) during SWOs recorded from anaesthetised rats via a multi-channel laminar micro-electrode and show that the Down state consists of two distinct synaptic states: a dynamic down state associated with depth-positive LFPs and a prominent dipole in the extracellular field, and a static down state with negligible (≈0 mV) LFPs and a lack of dipoles extracellularly. We demonstrate that depth-negative and -positive LFPs are generated by a shift in the balance of synaptic excitation and inhibition from excitation dominance (depth-negative) to inhibition dominance (depth-positive) in the infragranular layer neurons. Thus, although excitation and inhibition co-tune overall, differences in their timing lead to an alternation of dominance, manifesting as SWOs. We further show that Up state initiation is significantly faster if the preceding Down state is dynamic rather than static. Our findings provide a coherent picture of the dependence of SWOs on synaptic activity.

Item Type:Article
Refereed:Yes
Divisions:Interdisciplinary Research Centres (IDRCs) > Centre for Integrative Neuroscience and Neurodynamics (CINN)
Life Sciences > School of Biological Sciences > Department of Bio-Engineering
Life Sciences > School of Psychology and Clinical Language Sciences > Department of Psychology
ID Code:115034
Uncontrolled Keywords:Spontaneous; Extracellular field potential; Slow-wave oscillation; Balance of excitation and inhibition; Up state initiation; Up state termination.
Publisher:Wiley-Blackwell

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