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Peer-reviewedCC BY-NC-NDNature Neuroscience

The representational geometry of emotional states in basolateral amygdala

  • Pia-Kelsey O’Neill1,2,3
  • Lorenzo Posani4,1,5,2
  • József Mészáros6,7
  • Phebe Warren2,8,3
  • Carl Edward Schoonover9,1,10,2,3
  • Andrew J. P. Fink11,1,10,2,3
  • Stefano Fusi4,1,12,2,3
  • C. Daniel Salzman13,14,15,16,17,18,1,6,19,7,3
19 affiliations
  1. 1Department of Neuroscience, Columbia University, New York, NY, USA
  2. 2The Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA
  3. 3The Mortimer B. Zuckerman Mind Brain Behavior Institute, New York, NY, USA
  4. 4Center for Theoretical Neuroscience, Columbia University, New York, NY, USA
  5. 5ICM Paris Brain Institute, Hôpital de la Pitié Salpêtrière, Paris, France
  6. 6Department of Psychiatry, Columbia University, New York, NY, USA
  7. 7New York State Psychiatric Institute, New York, NY, USA
  8. 8Columbia University Mailman School of Public Health, New York, NY, USA
  9. 9Allen Institute for Neural Dynamics, Seattle, WA, USA
  10. 10Howard Hughes Medical Institute, Columbia University, New York, NY, USA
  11. 11Department of Neurobiology, Northwestern University, Evanston, IL, USA
  12. 12Kavli Institute for Brain Science, Columbia University, New York, NY, USA
  13. 13Department of Neuroscience, Columbia University, New York, NY, USA. [email protected]
  14. 14Department of Psychiatry, Columbia University, New York, NY, USA. [email protected]
  15. 15Kavli Institute for Brain Science, Columbia University, New York, NY, USA. [email protected]
  16. 16New York State Psychiatric Institute, New York, NY, USA. [email protected]
  17. 17The Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA. [email protected]
  18. 18Center for Theoretical Neuroscience, Columbia University, New York, NY USA
  19. 19Kavli Institute for Brain Science, Columbia University, New York, NY USA
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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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Cite

BibTeXRIS
BibTeX
@article{oneill2026representational,
  title = {{The representational geometry of emotional states in basolateral amygdala}},
  author = {Pia-Kelsey O’Neill and Lorenzo Posani and József Mészáros and Phebe Warren and Carl Edward Schoonover and Andrew J. P. Fink and Stefano Fusi and C. Daniel Salzman},
  journal = {Nature Neuroscience},
  year = {2026},
  month = jun,
  doi = {10.1038/s41593-026-02315-y},
  url = {https://doi.org/10.1038/s41593-026-02315-y},
  note = {CC BY-NC-ND},
}
RIS
TY  - JOUR
TI  - The representational geometry of emotional states in basolateral amygdala
AU  - Pia-Kelsey O’Neill
AU  - Lorenzo Posani
AU  - József Mészáros
AU  - Phebe Warren
AU  - Carl Edward Schoonover
AU  - Andrew J. P. Fink
AU  - Stefano Fusi
AU  - C. Daniel Salzman
PY  - 2026
DA  - 2026/06/03
JO  - Nature Neuroscience
DO  - 10.1038/s41593-026-02315-y
UR  - https://doi.org/10.1038/s41593-026-02315-y
AB  - 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.
SN  - 1097-6256
SN  - 1546-1726
ER  -