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

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 cereb...

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Published inNature communications Vol. 11; no. 1; p. 5207
Main Authors Frontera, Jimena Laura, Baba Aissa, Hind, Sala, Romain William, Mailhes-Hamon, Caroline, Georgescu, Ioana Antoaneta, Léna, Clément, Popa, Daniela
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 15.10.2020
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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. The cerebellum has a role in motor control, but may also contribute to other functions. Here the authors demonstrate a role for the cerebellar fastigial nucleus projection onto ventrolateral periaqueductal grey neurons during fear acquisition.
AbstractList 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. The cerebellum has a role in motor control, but may also contribute to other functions. Here the authors demonstrate a role for the cerebellar fastigial nucleus projection onto ventrolateral periaqueductal grey neurons during fear acquisition.
The cerebellum has a role in motor control, but may also contribute to other functions. Here the authors demonstrate a role for the cerebellar fastigial nucleus projection onto ventrolateral periaqueductal grey neurons during fear acquisition.
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.
ArticleNumber 5207
Author Frontera, Jimena Laura
Léna, Clément
Sala, Romain William
Georgescu, Ioana Antoaneta
Baba Aissa, Hind
Popa, Daniela
Mailhes-Hamon, Caroline
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  givenname: Jimena Laura
  surname: Frontera
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  organization: Neurophysiology of Brain Circuits Team, Institut de Biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University
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  givenname: Hind
  surname: Baba Aissa
  fullname: Baba Aissa, Hind
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  givenname: Romain William
  surname: Sala
  fullname: Sala, Romain William
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  givenname: Caroline
  surname: Mailhes-Hamon
  fullname: Mailhes-Hamon, Caroline
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  givenname: Ioana Antoaneta
  orcidid: 0000-0003-2175-5739
  surname: Georgescu
  fullname: Georgescu, Ioana Antoaneta
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  givenname: Clément
  surname: Léna
  fullname: Léna, Clément
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  givenname: Daniela
  orcidid: 0000-0002-8389-1122
  surname: Popa
  fullname: Popa, Daniela
  email: daniela.popa@bio.ens.psl.eu
  organization: Neurophysiology of Brain Circuits Team, Institut de Biologie de l’Ecole normale supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, PSL Research University
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Snippet Fear conditioning is a form of associative learning that is known to involve different brain areas, notably the amygdala, the prefrontal cortex and the...
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 cerebellum has a role in motor control, but may also contribute to other functions. Here the authors demonstrate a role for the cerebellar fastigial...
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Title Bidirectional control of fear memories by cerebellar neurons projecting to the ventrolateral periaqueductal grey
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