Bidirectional control of fear memories by cerebellar neurons projecting to the ventrolateral periaqueductal grey

Jimena Laura Frontera, Hind Baba Aissa, Romain William Sala, Caroline Mailhes-Hamon, Ioana Antoaneta Georgescu, Clément Léna and Daniela Popa ()
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Jimena Laura Frontera: Neurophysiology of Brain Circuits Team, Institut de Biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University
Hind Baba Aissa: Neurophysiology of Brain Circuits Team, Institut de Biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University
Romain William Sala: Neurophysiology of Brain Circuits Team, Institut de Biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University
Caroline Mailhes-Hamon: Neurophysiology of Brain Circuits Team, Institut de Biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University
Ioana Antoaneta Georgescu: Neurophysiology of Brain Circuits Team, Institut de Biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University
Clément Léna: Neurophysiology of Brain Circuits Team, Institut de Biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University
Daniela Popa: Neurophysiology of Brain Circuits Team, Institut de Biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University

Nature Communications, 2020, vol. 11, issue 1, 1-17

Abstract: Abstract Fear conditioning is a form of associative learning that is known to involve different brain areas, notably the amygdala, the prefrontal cortex and the periaqueductal grey (PAG). Here, we describe the functional role of pathways that link the cerebellum with the fear network. We found that the cerebellar fastigial nucleus (FN) sends glutamatergic projections to vlPAG that synapse onto glutamatergic and GABAergic vlPAG neurons. Chemogenetic and optogenetic manipulations revealed that the FN-vlPAG pathway controls bi-directionally the strength of the fear memories, indicating an important role in the association of the conditioned and unconditioned stimuli, a function consistent with vlPAG encoding of fear prediction error. Moreover, FN-vlPAG projections also modulate extinction learning. We also found a FN-parafascicular thalamus pathway, which may relay cerebellar influence to the amygdala and modulates anxiety behaviors. Overall, our results reveal multiple contributions of the cerebellum to the emotional system.

Date: 2020
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DOI: 10.1038/s41467-020-18953-0

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