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

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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 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.

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Item Type	Article
URI	https://reading-clone.eprints-hosting.org/id/eprint/115034
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
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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Funders:	Biotechnology and Biological Sciences Research Council	The sponsoring bodies who contributed funding for the creation of this item. Example: NERC Example: The Royal Society of Chemistry A pick list of funders may appear as you type in the funder's name in full or as an acronym. Select a correct match to complete the field or type in a new entry in full. For new entries, the full name is preferred.
Projects:	Understanding neural excitation and inhibition: implications for the interpretation of extracellular field potentials and neurovascular coupling Funded by: Biotechnology and Biological Sciences Research Council (BB/K010123/2 - £411,603) Project Lead: Ying Zheng 1 April 2014 - 30 June 2016 Understanding neural excitation and inhibition: implications for the interpretation of extracellular field potentials and neurovascular coupling Funded by: Biotechnology and Biological Sciences Research Council (BB/K010123/1 - £411,603) Local Lead (PI): Ying Zheng 1 April 2014 - 30 June 2016	Click Add to select your project (received at Reading) from an autocomplete list.

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Date Deposited:	07 Feb 2024 10:25	Date item deposited into CentAUR
Last Modified:	23 Jun 2024 04:03	Date item last modified

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