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Featured ArticleResearch Articles, Behavioral/Cognitive

Contingent Amygdala Inputs Trigger Heterosynaptic LTP at Hippocampus-To-Accumbens Synapses

Jun Yu, Susan R. Sesack, Yanhua Huang, Oliver M. Schlüter, Anthony A. Grace and Yan Dong
Journal of Neuroscience 24 August 2022, 42 (34) 6581-6592; DOI: https://doi.org/10.1523/JNEUROSCI.0838-22.2022
Jun Yu
1Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
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Susan R. Sesack
1Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
2Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15260
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Yanhua Huang
1Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
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Oliver M. Schlüter
1Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
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Anthony A. Grace
1Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
2Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15260
3Department of Psychology, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
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Yan Dong
1Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
2Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15260
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Abstract

The nucleus accumbens shell (NAcSh) is a key brain region where environmental cues acquire incentive salience to reinforce motivated behaviors. Principal medium spiny neurons (MSNs) in the NAcSh receive extensive glutamatergic projections from limbic regions, among which, the ventral hippocampus (vH) transmits information enriched in contextual cues, and the basolateral amygdala (BLA) encodes real-time arousing states. The vH and BLA project convergently to NAcSh MSNs, both activated in a time-locked manner on a cue-conditioned motivational action. In brain slices prepared from male and female mice, we show that co-activation of the two projections induces long-term potentiation (LTP) at vH-to-NAcSh synapses without affecting BLA-to-NAcSh synapses, revealing a heterosynaptic mechanism through which BLA signals persistently increase the temporally contingent vH-to-NAcSh transmission. Furthermore, this LTP is more prominent in dopamine D1 receptor-expressing (D1) MSNs than D2 MSNs and can be prevented by inhibition of either D1 receptors or dopaminergic terminals in NAcSh. This heterosynaptic LTP may provide a dopamine-guided mechanism through which vH-encoded cue inputs that are contingent to BLA activation acquire increased circuit representation to reinforce behavior.

SIGNIFICANCE STATEMENT In motivated behaviors, environmental cues associated with arousing stimuli acquire increased incentive salience, processes mediated in part by the nucleus accumbens (NAc). NAc principal neurons receive glutamatergic projections from the ventral hippocampus (vH) and basolateral amygdala (BLA), which transmit information encoding contextual cues and affective states, respectively. Our results show that co-activation of the two projections induces long-term potentiation (LTP) at vH-to-NAc synapses without affecting BLA-to-NAc synapses, revealing a heterosynaptic mechanism through which BLA signals potentiate the temporally contingent vH-to-NAc transmission. Furthermore, this LTP is prevented by inhibition of either D1 receptors or dopaminergic axons. This heterosynaptic LTP may provide a dopamine-guided mechanism through which vH-encoded cue inputs that are contingent to BLA activation acquire increased circuit representation to reinforce behavior.

  • amygdala
  • dopamine
  • heterosynaptic
  • hippocampus
  • LTP
  • nucleus accumbens

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The Journal of Neuroscience: 42 (34)
Journal of Neuroscience
Vol. 42, Issue 34
24 Aug 2022
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Contingent Amygdala Inputs Trigger Heterosynaptic LTP at Hippocampus-To-Accumbens Synapses
Jun Yu, Susan R. Sesack, Yanhua Huang, Oliver M. Schlüter, Anthony A. Grace, Yan Dong
Journal of Neuroscience 24 August 2022, 42 (34) 6581-6592; DOI: 10.1523/JNEUROSCI.0838-22.2022

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Contingent Amygdala Inputs Trigger Heterosynaptic LTP at Hippocampus-To-Accumbens Synapses
Jun Yu, Susan R. Sesack, Yanhua Huang, Oliver M. Schlüter, Anthony A. Grace, Yan Dong
Journal of Neuroscience 24 August 2022, 42 (34) 6581-6592; DOI: 10.1523/JNEUROSCI.0838-22.2022
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Keywords

  • amygdala
  • dopamine
  • heterosynaptic
  • hippocampus
  • LTP
  • nucleus accumbens

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