Silencing CA1 pyramidal cells output reveals the role of feedback inhibition in hippocampal oscillations

Chinnakkaruppan Adaikkan (), Justin Joseph, Georgios Foustoukos, Jun Wang, Denis Polygalov, Roman Boehringer, Steven J. Middleton, Arthur J. Y. Huang, Li-Huei Tsai and Thomas J. McHugh ()
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Chinnakkaruppan Adaikkan: Indian Institute of Science
Justin Joseph: Indian Institute of Science
Georgios Foustoukos: RIKEN Center for Brain Science
Jun Wang: Picower Institute for Learning and Memory, Massachusetts Institute of Technology
Denis Polygalov: RIKEN Center for Brain Science
Roman Boehringer: RIKEN Center for Brain Science
Steven J. Middleton: RIKEN Center for Brain Science
Arthur J. Y. Huang: RIKEN Center for Brain Science
Li-Huei Tsai: Picower Institute for Learning and Memory, Massachusetts Institute of Technology
Thomas J. McHugh: RIKEN Center for Brain Science

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract The precise temporal coordination of neural activity is crucial for brain function. In the hippocampus, this precision is reflected in the oscillatory rhythms observed in CA1. While it is known that a balance between excitatory and inhibitory activity is necessary to generate and maintain these oscillations, the differential contribution of feedforward and feedback inhibition remains ambiguous. Here we use conditional genetics to chronically silence CA1 pyramidal cell transmission, ablating the ability of these neurons to recruit feedback inhibition in the local circuit, while recording physiological activity in mice. We find that this intervention leads to local pathophysiological events, with ripple amplitude and intrinsic frequency becoming significantly larger and spatially triggered local population spikes locked to the trough of the theta oscillation appearing during movement. These phenotypes demonstrate that feedback inhibition is crucial in maintaining local sparsity of activation and reveal the key role of lateral inhibition in CA1 in shaping circuit function.

Date: 2024
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DOI: 10.1038/s41467-024-46478-3

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