A novel inhibitory nucleo-cortical circuit controls cerebellar Golgi cell activity

  1. Lea Ankri
  2. Zoé Husson
  3. Katarzyna Pietrajtis
  4. Rémi Proville
  5. Clément Léna
  6. Yosef Yarom
  7. Stéphane Dieudonné  Is a corresponding author
  8. Marylka Yoe Uusisaari
  1. Hebrew University of Jerusalem, Israel
  2. Ecole Normale Supérieure, France

Abstract

The cerebellum, a crucial center for motor coordination, is composed of a cortex and several nuclei. The main mode of interaction between these two parts is considered to be formed by the inhibitory control of the nuclei by cortical Purkinje neurons. We now amend this view by showing that inhibitory GABA-glycinergic neurons of the cerebellar nuclei project profusely into the cerebellar cortex, where they make synaptic contacts on a GABAergic subpopulation of cerebellar Golgi cells. These spontaneously firing Golgi cells are inhibited by optogenetic activation of the inhibitory nucleo-cortical fibers both in vitro and in vivo. Our data suggest that the cerebellar nuclei may contribute to the functional recruitment of the cerebellar cortex by decreasing Golgi cell inhibition onto granule cells.

Article and author information

Author details

  1. Lea Ankri

    Department of Neurobiology, Edmond and Lily Safra Center for Brain Sciences, Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  2. Zoé Husson

    Inhibitory Transmission Team, Institut de Biologie de l'École Normale Supérieure, Ecole Normale Supérieure, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Katarzyna Pietrajtis

    Inhibitory Transmission Team, Institut de Biologie de l'École Normale Supérieure, Ecole Normale Supérieure, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Rémi Proville

    Centre national de la recherche scientifique, Institut de Biologie de l'École Normale Supérieure, Ecole Normale Supérieure, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Clément Léna

    Centre national de la recherche scientifique, Institut de Biologie de l'École Normale Supérieure, Ecole Normale Supérieure, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Yosef Yarom

    Department of Neurobiology, Edmond and Lily Safra Center for Brain Sciences, Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  7. Stéphane Dieudonné

    Inhibitory Transmission Team, Institut de Biologie de l'École Normale Supérieure, Ecole Normale Supérieure, Paris, France
    For correspondence
    dieudon@biologie.ens.fr
    Competing interests
    The authors declare that no competing interests exist.
  8. Marylka Yoe Uusisaari

    Department of Neurobiology, Edmond and Lily Safra Center for Brain Sciences, Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All animal manipulations were made in strict accordance with guidelines of the Centre National de la Recherche Scientifique and the Hebrew University's Animal Care and Use Committee (Ethic permission # NS-12-12505-4).

Copyright

© 2015, Ankri et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,994
    views
  • 777
    downloads
  • 87
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Lea Ankri
  2. Zoé Husson
  3. Katarzyna Pietrajtis
  4. Rémi Proville
  5. Clément Léna
  6. Yosef Yarom
  7. Stéphane Dieudonné
  8. Marylka Yoe Uusisaari
(2015)
A novel inhibitory nucleo-cortical circuit controls cerebellar Golgi cell activity
eLife 4:e06262.
https://doi.org/10.7554/eLife.06262

Share this article

https://doi.org/10.7554/eLife.06262

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Brian DePasquale, Carlos D Brody, Jonathan W Pillow
    Research Article

    Accumulating evidence to make decisions is a core cognitive function. Previous studies have tended to estimate accumulation using either neural or behavioral data alone. Here we develop a unified framework for modeling stimulus-driven behavior and multi-neuron activity simultaneously. We applied our method to choices and neural recordings from three rat brain regions - the posterior parietal cortex (PPC), the frontal orienting fields (FOF), and the anterior-dorsal striatum (ADS) - while subjects performed a pulse-based accumulation task. Each region was best described by a distinct accumulation model, which all differed from the model that best described the animal's choices. FOF activity was consistent with an accumulator where early evidence was favored while the ADS reflected near perfect accumulation. Neural responses within an accumulation framework unveiled a distinct association between each brain region and choice. Choices were better predicted from all regions using a comprehensive, accumulation-based framework and different brain regions were found to differentially reflect choice-related accumulation signals: FOF and ADS both reflected choice but ADS showed more instances of decision vacillation. Previous studies relating neural data to behaviorally-inferred accumulation dynamics have implicitly assumed that individual brain regions reflect the whole-animal level accumulator. Our results suggest that different brain regions represent accumulated evidence in dramatically different ways and that accumulation at the whole-animal level may be constructed from a variety of neural-level accumulators.

    1. Neuroscience
    Sandra P Cárdenas-García, Sundas Ijaz, Alberto E Pereda
    Research Article Updated

    Most nervous systems combine both transmitter-mediated and direct cell–cell communication, known as ‘chemical’ and ‘electrical’ synapses, respectively. Chemical synapses can be identified by their multiple structural components. Electrical synapses are, on the other hand, generally defined by the presence of a ‘gap junction’ (a cluster of intercellular channels) between two neuronal processes. However, while gap junctions provide the communicating mechanism, it is unknown whether electrical transmission requires the contribution of additional cellular structures. We investigated this question at identifiable single synaptic contacts on the zebrafish Mauthner cells, at which gap junctions coexist with specializations for neurotransmitter release and where the contact unequivocally defines the anatomical limits of a synapse. Expansion microscopy of these single contacts revealed a detailed map of the incidence and spatial distribution of proteins pertaining to various synaptic structures. Multiple gap junctions of variable size were identified by the presence of their molecular components. Remarkably, most of the synaptic contact’s surface was occupied by interleaving gap junctions and components of adherens junctions, suggesting a close functional association between these two structures. In contrast, glutamate receptors were confined to small peripheral portions of the contact, indicating that most of the synaptic area functions as an electrical synapse. Thus, our results revealed the overarching organization of an electrical synapse that operates with not one, but multiple gap junctions, in close association with structural and signaling molecules known to be components of adherens junctions. The relationship between these intercellular structures will aid in establishing the boundaries of electrical synapses found throughout animal connectomes and provide insight into the structural organization and functional diversity of electrical synapses.