Analogue closed-loop optogenetic modulation of hippocampal pyramidal cells dissociates gamma frequency and amplitude

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Abstract

Gamma-band oscillations are implicated in modulation of attention, integration of sensory information and flexible communication among anatomically connected brain areas. How networks become entrained is incompletely understood. Specifically, it is unclear how the spectral and temporal characteristics of network oscillations can be altered on rapid timescales needed for efficient communication. We use closed-loop optogenetic modulation of principal cell excitability in mouse hippocampal slices to interrogate the dynamical properties of hippocampal oscillations. Gamma frequency and amplitude can be modulated bi-directionally, and dissociated, by phase-advancing or delaying optogenetic feedback to pyramidal cells. Closed-loop modulation alters the synchrony rather than average frequency of action potentials, in principle avoiding disruption of population rate-coding of information. Modulation of phasic excitatory currents in principal neurons is sufficient to manipulate oscillations, suggesting that feed-forward excitation of pyramidal cells has an important role in determining oscillatory dynamics and the ability of networks to couple with one another.

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Source data files have been provided for Figures 1-7.

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Elizabeth Nicholson

UCL Institute of Neurology, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Dmitry A Kuzmin

UCL Institute of Neurology, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Marco Leite

UCL Institute of Neurology, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Thomas E Akam

Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1810-0494
Dimitri Michael Kullmann

UCL Institute of Neurology, University College London, London, United Kingdom

For correspondence
d.kullmann@ucl.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6696-3545

Funding

Wellcome (095580/Z/11/Z)

Dimitri Michael Kullmann

Wellcome (WT104033AIA)

Dimitri Michael Kullmann

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in accordance with the Animals (Scientific Procedures) Act, 1986, and were reviewed by the UCL Institute of Neurology Animal Welfare and Ethical Review Body.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.