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Nat Neurosci. 2019 Apr;22(4):618-626. doi: 10.1038/s41593-019-0355-x. Epub 2019 Mar 11.

Long-range inhibitory intersection of a retrosplenial thalamocortical circuit by apical tuft-targeting CA1 neurons.

Author information

1
Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA. naoki.yamawaki@northwestern.edu.
2
Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA.
3
Department of Psychiatry and Behavioral Sciences, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA.
4
Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA. g-shepherd@northwestern.edu.

Abstract

Hippocampus, granular retrosplenial cortex (RSCg), and anterior thalamic nuclei (ATN) interact to mediate diverse cognitive functions. To identify cellular mechanisms underlying hippocampo-thalamo-retrosplenial interactions, we investigated the potential circuit suggested by projections to RSCg layer 1 (L1) from GABAergic CA1 neurons and ATN. We find that CA1→RSCg projections stem from GABAergic neurons with a distinct morphology, electrophysiology, and molecular profile. Their long-range axons inhibit L5 pyramidal neurons in RSCg via potent synapses onto apical tuft dendrites in L1. These inhibitory inputs intercept L1-targeting thalamocortical excitatory inputs from ATN to coregulate RSCg activity. Subicular axons, in contrast, excite proximal dendrites in deeper layers. Short-term plasticity differs at each connection. Chemogenetically abrogating CA1→RSCg or ATN→RSCg connections oppositely affects the encoding of contextual fear memory. Our findings establish retrosplenial-projecting CA1 neurons as a distinct class of long-range dendrite-targeting GABAergic neuron and delineate an unusual cortical circuit specialized for integrating long-range inhibition and thalamocortical excitation.

PMID:
30858601
PMCID:
PMC6435388
DOI:
10.1038/s41593-019-0355-x
[Indexed for MEDLINE]
Free PMC Article

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