Control of parallel hippocampal output pathways by amygdalar long-range inhibition

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Abstract

Projections from the basal amygdala (BA) to the ventral hippocampus (vH) are proposed to provide information about the rewarding or threatening nature of learned associations to support appropriate goal-directed and anxiety-like behaviour. Such behaviour occurs via the differential activity of multiple, parallel populations of pyramidal neurons in vH that project to distinct downstream targets, but the nature of BA input and how it connects with these populations is unclear. Using channelrhodopsin-2-assisted circuit mapping in mice, we show that BA input to vH consists of both excitatory and inhibitory projections. Excitatory input specifically targets BA- and nucleus accumbens-projecting vH neurons, and avoids prefrontal cortex-projecting vH neurons; while inhibitory input preferentially targets BA-projecting neurons. Through this specific connectivity, BA inhibitory projections gate place-value associations by controlling the activity of nucleus accumbens-projecting vH neurons. Our results define a parallel excitatory and inhibitory projection from BA to vH that can support goal-directed behaviour.

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Rawan AlSubaie

Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Ryan WS Wee

Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-0273-5521
Anne Ritoux

Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Karyna Mishchanchuk

Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Jessica Passlack

Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Daniel Regester

Neuroscience, PhysioDepartment of Neuroscience, Physiology and Pharmacologylogy and Pharmacology, University College London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Andrew F MacAskill

Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom

For correspondence
a.macaskill@ucl.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0196-3779

Funding

Wellcome Trust (109360/Z/15/Z)

Andrew F MacAskill

Wellcome Trust (215165/Z/18/Z)

Karyna Mishchanchuk

Wellcome Trust (222292/Z/20/Z)

Jessica Passlack

King Fahad Medical City

Rawan AlSubaie

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments were approved by the U.K. Home Office as defined by the Animals (ScientificProcedures) Act, and University College London ethical guidelines.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.