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[Preprint]. 2024 Apr 21:2023.09.23.558668. Originally published 2023 Sep 23. [Version 2] doi: 10.1101/2023.09.23.558668

The representational geometry of emotional states in basolateral amygdala

Pia-Kelsey O'Neill, Lorenzo Posani, Jozsef Meszaros, Phebe Warren, Carl E Schoonover, Andrew JP Fink, Stefano Fusi, C Daniel Salzman
PMCID: PMC10542536  PMID: 37790470

Abstract

Sensory stimuli associated with aversive outcomes cause multiple behavioral responses related to an animal's evolving emotional state, but neural mechanisms underlying these processes remain unclear. Here aversive stimuli were presented to mice, eliciting two responses reflecting fear and flight to safety: tremble and ingress into a virtual burrow. Inactivation of basolateral amygdala (BLA) eliminated differential responses to aversive and neutral stimuli without eliminating responses themselves, suggesting BLA signals valence, not motor commands. However, two-photon imaging revealed that neurons typically exhibited mixed selectivity for stimulus identity, valence, tremble and/or ingress. Despite heterogeneous selectivity, BLA representational geometry was lower-dimensional when encoding valence, tremble and safety, enabling generalization of emotions across conditions. Further, tremble and valence coding directions were orthogonal, allowing linear readouts to specialize. Thus BLA representational geometry confers two computational properties that identify specialized neural circuits encoding variables describing emotional states: generalization across conditions, and readouts lacking interference from other readouts.

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