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Cell. 2016 Nov 3;167(4):961-972.e16. doi: 10.1016/j.cell.2016.09.051. Epub 2016 Oct 20.

Distinct Hippocampal Pathways Mediate Dissociable Roles of Context in Memory Retrieval.

Author information

1
Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland.
2
Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland; University of Basel, 4003 Basel, Switzerland.
3
Systems Neurobiology Laboratories, Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
4
Department of Internal Medicine 2, Technische Universität München, Ismaningerstrasse 22, 81675 Munich, Germany; German Cancer Consortium (DKTK) and German Cancer Research Center (DKFZ), Im Neuenheimer Feld 280, 69120 Heidelberg, Germany.
5
CNC Program, Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA.
6
Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland; University of Basel, 4003 Basel, Switzerland. Electronic address: andreas.luthi@fmi.ch.

Abstract

Memories about sensory experiences are tightly linked to the context in which they were formed. Memory contextualization is fundamental for the selection of appropriate behavioral reactions needed for survival, yet the underlying neuronal circuits are poorly understood. By combining trans-synaptic viral tracing and optogenetic manipulation, we found that the ventral hippocampus (vHC) and the amygdala, two key brain structures encoding context and emotional experiences, interact via multiple parallel pathways. A projection from the vHC to the basal amygdala mediates fear behavior elicited by a conditioned context, whereas a parallel projection from a distinct subset of vHC neurons onto midbrain-projecting neurons in the central amygdala is necessary for context-dependent retrieval of cued fear memories. Our findings demonstrate that two fundamentally distinct roles of context in fear memory retrieval are processed by distinct vHC output pathways, thereby allowing for the formation of robust contextual fear memories while preserving context-dependent behavioral flexibility.

KEYWORDS:

basal amygdala; central amygdala; contextual fear; fear conditioning; fear renewal; optogenetics; rabies-ArchT; trans-synaptic tracing; ventral hippocampus

PMID:
27773481
PMCID:
PMC5382990
DOI:
10.1016/j.cell.2016.09.051
[Indexed for MEDLINE]
Free PMC Article

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