Hippocampal cholecystokinin-expressing interneurons regulate temporal coding and contextual learning

Rangel Guerrero DK, Balueva K, Barayeu U, Baracskay P, Gridchyn I, Nardin M, Roth CN, Wulff P, Csicsvari JL. 2024. Hippocampal cholecystokinin-expressing interneurons regulate temporal coding and contextual learning. Neuron.

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Abstract
Cholecystokinin-expressing interneurons (CCKIs) are hypothesized to shape pyramidal cell-firing patterns and regulate network oscillations and related network state transitions. To directly probe their role in the CA1 region, we silenced their activity using optogenetic and chemogenetic tools in mice. Opto-tagged CCKIs revealed a heterogeneous population, and their optogenetic silencing triggered wide disinhibitory network changes affecting both pyramidal cells and other interneurons. CCKI silencing enhanced pyramidal cell burst firing and altered the temporal coding of place cells: theta phase precession was disrupted, whereas sequence reactivation was enhanced. Chemogenetic CCKI silencing did not alter the acquisition of spatial reference memories on the Morris water maze but enhanced the recall of contextual fear memories and enabled selective recall when similar environments were tested. This work suggests the key involvement of CCKIs in the control of place-cell temporal coding and the formation of contextual memories.
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Date Published
2024-04-17
Journal Title
Neuron
Acknowledgement
We thank the kind donations from Andrea Varro, Brian Sauer, Edward Boyden, and Peter Jonas. We thank Jago Wallenschus, Kerstin Kronenbitter, and Didier Gremelle for outstanding technical support; Laura Bollepalli for initial viral targeting experiments; Cihan Önal for initial electrophysiology experiments; Yoav Ben-Simon for histological advice; and Anton Nikitenko for contributing to the analysis. We acknowledge support from the Miba Machine Shop, Bioimaging-, Life Science- and Pre-Clinical Facilities at ISTA. This work was supported by the Austrian Science Fund (FWF I3713 to J.C. as part of the FOR 2143 research consortium), the Deutsche Forschungsgemeinschaft (DFG) (WU 503/2-2 to P.W.), and the Medical Research Council, United Kingdom (grant G1100546/2 to P.W.).
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Rangel Guerrero DK, Balueva K, Barayeu U, et al. Hippocampal cholecystokinin-expressing interneurons regulate temporal coding and contextual learning. Neuron. 2024. doi:10.1016/j.neuron.2024.03.019
Rangel Guerrero, D. K., Balueva, K., Barayeu, U., Baracskay, P., Gridchyn, I., Nardin, M., … Csicsvari, J. L. (2024). Hippocampal cholecystokinin-expressing interneurons regulate temporal coding and contextual learning. Neuron. Cell Press. https://doi.org/10.1016/j.neuron.2024.03.019
Rangel Guerrero, Dámaris K, Kira Balueva, Uladzislau Barayeu, Peter Baracskay, Igor Gridchyn, Michele Nardin, Chiara N Roth, Peer Wulff, and Jozsef L Csicsvari. “Hippocampal Cholecystokinin-Expressing Interneurons Regulate Temporal Coding and Contextual Learning.” Neuron. Cell Press, 2024. https://doi.org/10.1016/j.neuron.2024.03.019.
D. K. Rangel Guerrero et al., “Hippocampal cholecystokinin-expressing interneurons regulate temporal coding and contextual learning,” Neuron. Cell Press, 2024.
Rangel Guerrero DK, Balueva K, Barayeu U, Baracskay P, Gridchyn I, Nardin M, Roth CN, Wulff P, Csicsvari JL. 2024. Hippocampal cholecystokinin-expressing interneurons regulate temporal coding and contextual learning. Neuron.
Rangel Guerrero, Dámaris K., et al. “Hippocampal Cholecystokinin-Expressing Interneurons Regulate Temporal Coding and Contextual Learning.” Neuron, Cell Press, 2024, doi:10.1016/j.neuron.2024.03.019.
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