Phase-amplitude coupled persistent theta and gamma oscillations in rat primary motor cortex in vitro

Nicholas W. Johnson, Mazhar Özkan, Adrian P. Burgess, Emma J. Prokic, Keith A. Wafford, Michael J O'Neill, Stuart D. Greenhill, Ian M. Stanford, Gavin L. Woodhall

Research output: Contribution to journalArticle

Abstract

In vivo, theta (4-7 Hz) and gamma (30-80 Hz) neuronal network oscillations are known to coexist and display phase-amplitude coupling (PAC). However, in vitro, these oscillations have for many years been studied in isolation. Using an improved brain slice preparation technique we have, using co-application of carbachol (10 μM) and kainic acid (150 nM), elicited simultaneous theta (6.6 ± 0.1 Hz) and gamma (36.6 ± 0.4 Hz) oscillations in rodent primary motor cortex (M1). Each oscillation showed greatest power in layer V. Using a variety of time series analyses we detected significant cross-frequency coupling 74% of slice preparations. Differences were observed in the pharmacological profile of each oscillation. Thus, gamma oscillations were reduced by the GABAA receptor antagonists, gabazine (250 nM and 2 μM), and picrotoxin (50 μM) and augmented by AMPA receptor antagonism with SYM2206 (20 μM). In contrast, theta oscillatory power was increased by gabazine, picrotoxin and SYM2206. GABAB receptor blockade with CGP55845 (5 μM) increased both theta and gamma power, and similar effects were seen with diazepam, zolpidem, MK801 and a series of metabotropic glutamate receptor antagonists. Oscillatory activity at both frequencies was reduced by the gap junction blocker carbenoxolone (200 μM) and by atropine (5 μM). These data show theta and gamma oscillations in layer V of rat M1 in vitro are cross-frequency coupled, and are mechanistically distinct. The development of an in vitro model of phase-amplitude coupled oscillations will facilitate further mechanistic investigation of the generation and modulation of coupled activity in mammalian cortex.

LanguageEnglish
Pages141–156
Number of pages16
JournalNeuropharmacology
Volume119
Early online date8 Apr 2017
DOIs
Publication statusPublished - Jun 2017

Fingerprint

Motor Cortex
Picrotoxin
Carbenoxolone
GABA-A Receptor Antagonists
Excitatory Amino Acid Antagonists
Metabotropic Glutamate Receptors
AMPA Receptors
Kainic Acid
Gap Junctions
Carbachol
Diazepam
Atropine
Rodentia
Pharmacology
Brain
In Vitro Techniques
gabazine
4-aminophenyl-1,2-dihydro-1-methyl-2-propylcarbamoyl-6,7-methylenedioxyphthalazine

Bibliographical note

© 2017 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)

Funding: BBSRC CASE-Studentship

Keywords

  • gamma
  • M1
  • neuronal network oscillations
  • phase amplitude coupling
  • theta

Cite this

Johnson, Nicholas W. ; Özkan, Mazhar ; Burgess, Adrian P. ; Prokic, Emma J. ; Wafford, Keith A. ; O'Neill, Michael J ; Greenhill, Stuart D. ; Stanford, Ian M. ; Woodhall, Gavin L. / Phase-amplitude coupled persistent theta and gamma oscillations in rat primary motor cortex in vitro. In: Neuropharmacology. 2017 ; Vol. 119. pp. 141–156.
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Phase-amplitude coupled persistent theta and gamma oscillations in rat primary motor cortex in vitro. / Johnson, Nicholas W.; Özkan, Mazhar; Burgess, Adrian P.; Prokic, Emma J.; Wafford, Keith A.; O'Neill, Michael J; Greenhill, Stuart D.; Stanford, Ian M.; Woodhall, Gavin L.

In: Neuropharmacology, Vol. 119, 06.2017, p. 141–156.

Research output: Contribution to journalArticle

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AU - Johnson, Nicholas W.

AU - Özkan, Mazhar

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AU - Wafford, Keith A.

AU - O'Neill, Michael J

AU - Greenhill, Stuart D.

AU - Stanford, Ian M.

AU - Woodhall, Gavin L.

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