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Research Articles, Cellular/Molecular

Developmentally Transient CB1Rs on Cerebellar Afferents Suppress Afferent Input, Downstream Synaptic Excitation, and Signaling to Migrating Neurons

Jesse L. Barnes, Claudia Mohr, Caitlin R. Ritchey, Chloe M. Erikson, Hiroko Shiina and David J. Rossi
Journal of Neuroscience 5 August 2020, 40 (32) 6133-6145; DOI: https://doi.org/10.1523/JNEUROSCI.1931-19.2020
Jesse L. Barnes
Washington State University, Integrative Physiology and Neuroscience, Pullman, Washington 99164
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Claudia Mohr
Washington State University, Integrative Physiology and Neuroscience, Pullman, Washington 99164
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Caitlin R. Ritchey
Washington State University, Integrative Physiology and Neuroscience, Pullman, Washington 99164
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Chloe M. Erikson
Washington State University, Integrative Physiology and Neuroscience, Pullman, Washington 99164
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Hiroko Shiina
Washington State University, Integrative Physiology and Neuroscience, Pullman, Washington 99164
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David J. Rossi
Washington State University, Integrative Physiology and Neuroscience, Pullman, Washington 99164
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Abstract

The endocannabinoid system plays important roles in brain development, but mechanistic studies have focused on neuronal differentiation, migration, and synaptogenesis, with less attention to transcellular interactions that coordinate neurodevelopmental processes across developing neural networks. We determined that, in the developing rodent cerebellar cortex (of both sexes), there is a transient window when the dominant brain cannabinoid receptor, CB1R, is expressed on afferent terminals instead of output neuron Purkinje cell synapses that dominate the adult cerebellum. Activation of these afferent CB1Rs suppresses synaptic transmission onto developing granule cells, and consequently also suppresses excitation of downstream neurons in the developing cortical network, including nonsynaptic, migrating neurons. Application of a CB1R antagonist during afferent stimulation trains and depolarizing voltage steps caused a significant, sustained potentiation of synaptic amplitude. Our data demonstrate that transiently expressed afferent CB1Rs regulate afferent synaptic strength during synaptogenesis, which enables coordinated dampening of transcortical developmental signals.

SIGNIFICANCE STATEMENT The endogenous cannabinoid system plays diverse roles in brain development, which, combined with the rapidly changing legal and medical status of cannabis-related compounds, makes understanding how exogenous cannabinoids affect brain development an important biomedical objective. The cerebellum is a key brain region in a variety of neurodevelopmental disorders, and the adult cerebellum has one of the highest expression levels of CB1R, but little is known about CB1R in the developing cerebellum. Here we report a developmentally distinct expression and function of CB1R in the cerebellum, in which endogenous or exogenous activation of CB1Rs modifies afferent synaptic strength and coordinated downstream network signaling. These findings have implications for recreational and medical use of exogenous cannabinoids by pregnant and breastfeeding women.

  • cannabinoid
  • cerebellum
  • development
  • marijuana
  • migration
  • THC
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The Journal of Neuroscience: 40 (32)
Journal of Neuroscience
Vol. 40, Issue 32
5 Aug 2020
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Developmentally Transient CB1Rs on Cerebellar Afferents Suppress Afferent Input, Downstream Synaptic Excitation, and Signaling to Migrating Neurons
Jesse L. Barnes, Claudia Mohr, Caitlin R. Ritchey, Chloe M. Erikson, Hiroko Shiina, David J. Rossi
Journal of Neuroscience 5 August 2020, 40 (32) 6133-6145; DOI: 10.1523/JNEUROSCI.1931-19.2020

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Developmentally Transient CB1Rs on Cerebellar Afferents Suppress Afferent Input, Downstream Synaptic Excitation, and Signaling to Migrating Neurons
Jesse L. Barnes, Claudia Mohr, Caitlin R. Ritchey, Chloe M. Erikson, Hiroko Shiina, David J. Rossi
Journal of Neuroscience 5 August 2020, 40 (32) 6133-6145; DOI: 10.1523/JNEUROSCI.1931-19.2020
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Keywords

  • cannabinoid
  • cerebellum
  • development
  • marijuana
  • migration
  • THC

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