Single-cell activity and network properties of dorsal raphe nucleus serotonin neurons during emotionally salient behaviors

Grace E Paquelet; Kassandra Carrion; Clay O Lacefield; Pengcheng Zhou; René Hen; Bradley R Miller

doi:10.1016/j.neuron.2022.05.015

Single-cell activity and network properties of dorsal raphe nucleus serotonin neurons during emotionally salient behaviors

Neuron. 2022 Aug 17;110(16):2664-2679.e8. doi: 10.1016/j.neuron.2022.05.015. Epub 2022 Jun 13.

Authors

Grace E Paquelet¹, Kassandra Carrion², Clay O Lacefield³, Pengcheng Zhou⁴, René Hen⁵, Bradley R Miller⁶

Affiliations

¹ Department of Neuroscience, Columbia University, New York, NY 10032, USA.
² Division of Systems Neuroscience, New York State Psychiatric Institute, New York, NY 10032, USA.
³ Division of Systems Neuroscience, New York State Psychiatric Institute, New York, NY 10032, USA; Department of Psychiatry, Columbia University Medical Center, New York, NY 10032, USA.
⁴ Department of Neuroscience, Columbia University, New York, NY 10032, USA; Department of Statistics, Columbia University, New York, NY 10027, USA; Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10027.
⁵ Department of Neuroscience, Columbia University, New York, NY 10032, USA; Division of Systems Neuroscience, New York State Psychiatric Institute, New York, NY 10032, USA; Department of Psychiatry, Columbia University Medical Center, New York, NY 10032, USA.
⁶ Division of Systems Neuroscience, New York State Psychiatric Institute, New York, NY 10032, USA; Department of Psychiatry, Columbia University Medical Center, New York, NY 10032, USA. Electronic address: bradley.miller@nyspi.columbia.edu.

Abstract

The serotonin system modulates a wide variety of emotional behaviors and states, including reward processing, anxiety, and social interaction. To reveal the underlying patterns of neural activity, we visualized serotonergic neurons in the dorsal raphe nucleus (DRN^5-HT) of mice using miniaturized microscopy during diverse emotional behaviors. We discovered ensembles of cells with highly correlated activity and found that DRN^5-HT neurons are preferentially recruited by emotionally salient stimuli as opposed to neutral stimuli. Individual DRN^5-HT neurons responded to diverse combinations of salient stimuli, with some preference for valence and sensory modality. Anatomically defined subpopulations projecting to either a reward-related structure (the ventral tegmental area) or an anxiety-related structure (the bed nucleus of the stria terminalis) contained all response types but were enriched in reward- and anxiety-responsive cells, respectively. Our results suggest that the DRN serotonin system responds to emotional salience using ensembles with mixed selectivity and biases in downstream connectivity.

Keywords: BNST; DRN; VTA; bed nucleus of the stria terminalis; calcium imaging; dorsal raphe nucleus; microendoscopy; salience; serotonin; ventral tegmental area.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Dorsal Raphe Nucleus* / physiology
Mice
Reward
Serotonergic Neurons
Serotonin*
Ventral Tegmental Area / physiology

Substances

Serotonin

Abstract

Publication types

MeSH terms

Substances

Grants and funding