Electrical coupling mediates tunable low-frequency oscillations and resonance in the cerebellar Golgi cell network.
Tonic motor control involves oscillatory synchronization of activity at low frequency (5-30 Hz) throughout the sensorimotor system, including cerebellar areas. We investigated the mechanisms underpinning cerebellar oscillations. We found that Golgi interneurons, which gate information transfer in the cerebellar cortex input layer, are extensively coupled through electrical synapses. When depolarized in vitro, these neurons displayed low-frequency oscillatory synchronization, imposing rhythmic inhibition onto granule cells. Combining experiments and modeling, we show that electrical transmission of the spike afterhyperpolarization is the essential component for oscillatory population synchronization. Rhythmic firing arises in spite of strong heterogeneities, is frequency tuned by the mean excitatory input to Golgi cells, and displays pronounced resonance when the modeled network is driven by oscillating inputs. In vivo, unitary Golgi cell activity was found to synchronize with low-frequency LFP oscillations occurring during quiet waking. These results suggest a major role for Golgi cells in coordinating cerebellar sensorimotor integration during oscillatory interactions.
Dugué
Guillaume P
GP
Laboratoire de Neurobiologie, ENS, CNRS, Paris.
Brunel
Nicolas
N
Hakim
Vincent
V
Schwartz
Eric
E
Chat
Mireille
M
Lévesque
Maxime
M
Courtemanche
Richard
R
Léna
Clément
C
Dieudonné
Stéphane
S
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D002531:Cerebellum / Q000166:cytology* / Q000502:physiology; D054351:Electrical Synapses / Q000502:physiology*; D018690:Excitatory Amino Acid Agonists / Q000378:metabolism; D007395:Interneurons / Q000166:cytology / Q000502:physiology*; D007608:Kainic Acid / Q000378:metabolism; D008564:Membrane Potentials / Q000502:physiology; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology*; D009474:Neurons / Q000166:cytology / Q000502:physiology; D018408:Patch-Clamp Techniques; D010507:Periodicity
D018690:Excitatory Amino Acid Agonists; D007608:Kainic Acid