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Curr Biol. 2018 Apr 23;28(8):1179-1188.e3. doi: 10.1016/j.cub.2018.02.061. Epub 2018 Apr 5.

Hippocampal Neural Circuits Respond to Optogenetic Pacing of Theta Frequencies by Generating Accelerated Oscillation Frequencies.

Author information

1
Neurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, 9500 Gilman Dr., La Jolla, CA 92093, USA.
2
Neurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, 9500 Gilman Dr., La Jolla, CA 92093, USA; Douglas Hospital Research Centre, Department of Psychiatry, McGill University, 6875 LaSalle Blvd., Montreal, QC H4H 1R3, Canada. Electronic address: mark.brandon@mcgill.ca.
3
Neurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, 9500 Gilman Dr., La Jolla, CA 92093, USA; Kavli Institute for Brain and Mind, University of California, San Diego, 9500 Gilman Dr., La Jolla, CA 92093, USA. Electronic address: sleutgeb@ucsd.edu.

Abstract

Biological oscillations can be controlled by a small population of rhythmic pacemaker cells, or in the brain, they also can emerge from complex cellular and circuit-level interactions. Whether and how these mechanisms are combined to give rise to oscillatory patterns that govern cognitive function are not well understood. For example, the activity of hippocampal networks is temporally coordinated by a 7- to 9-Hz local field potential (LFP) theta rhythm, yet many individual cells decouple from the LFP frequency to oscillate at frequencies ∼1 Hz higher. To better understand the network interactions that produce these complex oscillatory patterns, we asked whether the relative frequency difference between LFP and individual cells is retained when the LFP frequency is perturbed experimentally. We found that rhythmic optogenetic stimulation of medial septal GABAergic neurons controlled the hippocampal LFP frequency outside of the endogenous theta range, even during behavioral states when endogenous mechanisms would otherwise have generated 7- to 9-Hz theta oscillations. While the LFP frequency matched the optogenetically induced stimulation frequency, the oscillation frequency of individual hippocampal cells remained broadly distributed, and in a subset of cells including interneurons, it was accelerated beyond the new base LFP frequency. The inputs from septal GABAergic neurons to the hippocampus, therefore, do not appear to directly control the cellular oscillation frequency but rather engage cellular and circuit mechanisms that accelerate the rhythmicity of individual cells. Thus, theta oscillations are an example of cortical oscillations that combine inputs from a subcortical pacemaker with local computations to generate complex oscillatory patterns that support cognitive functions.

KEYWORDS:

GABAergic projections; hippocampus; medial septal area; oscillations; parvalbumin interneurons; place cells; theta

PMID:
29628373
PMCID:
PMC6488523
DOI:
10.1016/j.cub.2018.02.061
[Indexed for MEDLINE]
Free PMC Article

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