Endogenous cannabinoids in the piriform cortex tune olfactory perception

Geoffrey Terral, Evan Harrell, Gabriel Lepousez, Yohan Wards, Dinghuang Huang, Tiphaine Dolique, Giulio Casali, Antoine Nissant, Pierre-Marie Lledo, Guillaume Ferreira, Giovanni Marsicano and Lisa Roux ()
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Geoffrey Terral: Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297
Evan Harrell: Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297
Gabriel Lepousez: Perception and Memory Unit, CNRS, Joint Research Unit 3571, Université Paris Cité, Institut Pasteur
Yohan Wards: Univ. Bordeaux, INSERM, Neurocentre Magendie, U1215
Dinghuang Huang: Univ. Bordeaux, INSERM, Neurocentre Magendie, U1215
Tiphaine Dolique: Inovarion
Giulio Casali: Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297
Antoine Nissant: Perception and Memory Unit, CNRS, Joint Research Unit 3571, Université Paris Cité, Institut Pasteur
Pierre-Marie Lledo: Perception and Memory Unit, CNRS, Joint Research Unit 3571, Université Paris Cité, Institut Pasteur
Guillaume Ferreira: Univ. Bordeaux, INRAE, Bordeaux INP, NutriNeurO, UMR 1286
Giovanni Marsicano: Univ. Bordeaux, INSERM, Neurocentre Magendie, U1215
Lisa Roux: Univ. Bordeaux, CNRS, Interdisciplinary Institute for Neuroscience, IINS, UMR 5297

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Sensory perception depends on interactions between external inputs transduced by peripheral sensory organs and internal network dynamics generated by central neuronal circuits. In the sensory cortex, desynchronized network states associate with high signal-to-noise ratio stimulus-evoked responses and heightened perception. Cannabinoid-type-1-receptors (CB1Rs) - which influence network coordination in the hippocampus - are present in anterior piriform cortex (aPC), a sensory paleocortex supporting olfactory perception. Yet, how CB1Rs shape aPC network activity and affect odor perception is unknown. Using pharmacological manipulations coupled with multi-electrode recordings or fiber photometry in the aPC of freely moving male mice, we show that systemic CB1R blockade as well as local drug infusion increases the amplitude of gamma oscillations in aPC, while simultaneously reducing the occurrence of synchronized population events involving aPC excitatory neurons. In animals exposed to odor sources, blockade of CB1Rs reduces correlation among aPC excitatory units and lowers behavioral olfactory detection thresholds. These results suggest that endogenous endocannabinoid signaling promotes synchronized population events and dampen gamma oscillations in the aPC which results in a reduced sensitivity to external sensory inputs.

Date: 2024
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DOI: 10.1038/s41467-024-45161-x

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