Excitatory VTA to DH projections provide a valence signal to memory circuits

Yuan Han; Yi Zhang; Haram Kim; Viktoriya S. Grayson; Vladimir Jovasevic; Wenjie Ren; Maria V. Centeno; Anita L. Guedea; Mariah A.A. Meyer; Yixin Wu; Philipp Gutruf; Dalton J. Surmeier; Can Gao; Marco Martina; Apkar V. Apkarian; John A. Rogers; Jelena Radulovic

doi:10.1038/s41467-020-15035-z

Excitatory VTA to DH projections provide a valence signal to memory circuits

Yuan Han, Yi Zhang, Haram Kim, Viktoriya S. Grayson, Vladimir Jovasevic, Wenjie Ren, Maria V. Centeno, Anita L. Guedea, Mariah A.A. Meyer, Yixin Wu, Philipp Gutruf, Dalton J. Surmeier, Can Gao, Marco Martina, Apkar V. Apkarian, John A. Rogers, Jelena Radulovic

Research output: Contribution to journal › Article › peer-review

19 Scopus citations

Abstract

The positive or negative value (valence) of past experiences is normally integrated into neuronal circuits that encode episodic memories and plays an important role in guiding behavior. Here, we show, using mouse behavioral models, that glutamatergic afferents from the ventral tegmental area to the dorsal hippocampus (VTA→DH) signal negative valence to memory circuits, leading to the formation of fear-inducing context memories and to context-specific reinstatement of fear. To a lesser extent, these projections also contributed to opioid-induced place preference, suggesting a role in signaling positive valence as well, and thus a lack of dedicated polarity. Manipulations of VTA terminal activity were more effective in females and paralleled by sex differences in glutamatergic signaling. By prioritizing retrieval of negative and positive over neutral memories, the VTA→DH circuit can facilitate the selection of adaptive behaviors when current and past experiences are valence congruent.

Original language	English (US)
Article number	1466
Journal	Nature communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-15035-z
State	Published - Dec 1 2020
Externally published	Yes

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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Han, Y., Zhang, Y., Kim, H., Grayson, V. S., Jovasevic, V., Ren, W., Centeno, M. V., Guedea, A. L., Meyer, M. A. A., Wu, Y., Gutruf, P., Surmeier, D. J., Gao, C., Martina, M., Apkarian, A. V., Rogers, J. A., & Radulovic, J. (2020). Excitatory VTA to DH projections provide a valence signal to memory circuits. Nature communications, 11(1), Article 1466. https://doi.org/10.1038/s41467-020-15035-z

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abstract = "The positive or negative value (valence) of past experiences is normally integrated into neuronal circuits that encode episodic memories and plays an important role in guiding behavior. Here, we show, using mouse behavioral models, that glutamatergic afferents from the ventral tegmental area to the dorsal hippocampus (VTA→DH) signal negative valence to memory circuits, leading to the formation of fear-inducing context memories and to context-specific reinstatement of fear. To a lesser extent, these projections also contributed to opioid-induced place preference, suggesting a role in signaling positive valence as well, and thus a lack of dedicated polarity. Manipulations of VTA terminal activity were more effective in females and paralleled by sex differences in glutamatergic signaling. By prioritizing retrieval of negative and positive over neutral memories, the VTA→DH circuit can facilitate the selection of adaptive behaviors when current and past experiences are valence congruent.",

author = "Yuan Han and Yi Zhang and Haram Kim and Grayson, {Viktoriya S.} and Vladimir Jovasevic and Wenjie Ren and Centeno, {Maria V.} and Guedea, {Anita L.} and Meyer, {Mariah A.A.} and Yixin Wu and Philipp Gutruf and Surmeier, {Dalton J.} and Can Gao and Marco Martina and Apkarian, {Apkar V.} and Rogers, {John A.} and Jelena Radulovic",

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doi = "10.1038/s41467-020-15035-z",

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AU - Zhang, Yi

AU - Kim, Haram

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AU - Jovasevic, Vladimir

AU - Ren, Wenjie

AU - Centeno, Maria V.

AU - Guedea, Anita L.

AU - Meyer, Mariah A.A.

AU - Wu, Yixin

AU - Gutruf, Philipp

AU - Surmeier, Dalton J.

AU - Gao, Can

AU - Martina, Marco

AU - Apkarian, Apkar V.

AU - Rogers, John A.

AU - Radulovic, Jelena

PY - 2020/12/1

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N2 - The positive or negative value (valence) of past experiences is normally integrated into neuronal circuits that encode episodic memories and plays an important role in guiding behavior. Here, we show, using mouse behavioral models, that glutamatergic afferents from the ventral tegmental area to the dorsal hippocampus (VTA→DH) signal negative valence to memory circuits, leading to the formation of fear-inducing context memories and to context-specific reinstatement of fear. To a lesser extent, these projections also contributed to opioid-induced place preference, suggesting a role in signaling positive valence as well, and thus a lack of dedicated polarity. Manipulations of VTA terminal activity were more effective in females and paralleled by sex differences in glutamatergic signaling. By prioritizing retrieval of negative and positive over neutral memories, the VTA→DH circuit can facilitate the selection of adaptive behaviors when current and past experiences are valence congruent.

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Excitatory VTA to DH projections provide a valence signal to memory circuits

Abstract

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