TY - JOUR
T1 - Dorsal raphe dopamine neurons signal motivational salience dependent on internal state, expectation, and behavioral context
AU - Cho, Jounhong Ryan
AU - Chen, Xinhong
AU - Kahan, Anat
AU - Robinson, J. Elliott
AU - Wagenaar, Daniel A.
AU - Gradinaru, Viviana
N1 - Publisher Copyright:
Copyright © 2021 the authors.
PY - 2021/3/24
Y1 - 2021/3/24
N2 - The ability to recognize motivationally salient events and adaptively respond to them is critical for survival. Here, we tested whether dopamine (DA) neurons in the dorsal raphe nucleus (DRN) contribute to this process in both male and female mice. Population recordings of DRNDA neurons during associative learning tasks showed that their activity dynamically tracks the motivational salience, developing excitation to both reward-paired and shock-paired cues. The DRNDA response to rewardpredicting cues was diminished after satiety, suggesting modulation by internal states. DRNDA activity was also greater for unexpected outcomes than for expected outcomes. Two-photon imaging of DRNDA neurons demonstrated that the majority of individual neurons developed activation to reward-predicting cues and reward but not to shock-predicting cues, which was surprising and qualitatively distinct from the population results. Performing the same fear learning procedures in freely-moving and head-fixed groups revealed that head-fixation itself abolished the neural response to aversive cues, indicating its modulation by behavioral context. Overall, these results suggest that DRNDA neurons encode motivational salience, dependent on internal and external factors.
AB - The ability to recognize motivationally salient events and adaptively respond to them is critical for survival. Here, we tested whether dopamine (DA) neurons in the dorsal raphe nucleus (DRN) contribute to this process in both male and female mice. Population recordings of DRNDA neurons during associative learning tasks showed that their activity dynamically tracks the motivational salience, developing excitation to both reward-paired and shock-paired cues. The DRNDA response to rewardpredicting cues was diminished after satiety, suggesting modulation by internal states. DRNDA activity was also greater for unexpected outcomes than for expected outcomes. Two-photon imaging of DRNDA neurons demonstrated that the majority of individual neurons developed activation to reward-predicting cues and reward but not to shock-predicting cues, which was surprising and qualitatively distinct from the population results. Performing the same fear learning procedures in freely-moving and head-fixed groups revealed that head-fixation itself abolished the neural response to aversive cues, indicating its modulation by behavioral context. Overall, these results suggest that DRNDA neurons encode motivational salience, dependent on internal and external factors.
KW - Dopamine
KW - Dorsal raphe nucleus
KW - Fiber photometry
KW - Head fixation
KW - Motivational salience
KW - Two-photon imaging
UR - http://www.scopus.com/inward/record.url?scp=85103055072&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.2690-20.2021
DO - 10.1523/JNEUROSCI.2690-20.2021
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C2 - 33563725
AN - SCOPUS:85103055072
SN - 0270-6474
VL - 41
SP - 2645
EP - 2655
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 12
ER -