Is Purkinje Neuron Hyperpolarisation Important for Cerebellar Synaptic Plasticity? A Retrospective and Prospective Analy
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REVIEW
Is Purkinje Neuron Hyperpolarisation Important for Cerebellar Synaptic Plasticity? A Retrospective and Prospective Analysis Marco Canepari 1,2,3
# Springer Science+Business Media, LLC, part of Springer Nature 2020
Abstract Two recent studies have demonstrated that the dendritic Ca2+ signal associated with a climbing fibre (CF) input to the cerebellar Purkinje neuron (PN) depends on the membrane potential (Vm). Specifically, when the cell is hyperpolarised, this signal is mediated by T-type voltage-gated Ca2+ channels; in contrast, when the cell is firing, the CF-PN signal is mediated by P/Q-type voltage-gated Ca2+ channels. When the CF input is paired with parallel fibre (PF) activity, the signal is locally amplified at the sites of PF-activated synapses according to the Vm at the time of the CF input, suggesting that the standing Vm is a critical parameter for the induction of PF synaptic plasticity. In this review, I analyse how the Vm can potentially play a role in cerebellar learning focussing, in particular, on the hyperpolarised state that appears to occur episodically, since PNs are mostly firing under physiological conditions. By revisiting the recent literature reporting in vivo recordings and synaptic plasticity studies, I speculate on how a putative role of the PN Vm can provide an interpretation for the results of these studies. Keywords Purkinje neuron . Membrane potential . Calcium channels . Synaptic plasticity . Climbing fibre . Parallel fibres
Introduction In the vertebrate nervous system, the cerebellum integrates the incoming motor and sensory information to produce a feedback output from the cerebellar nuclei to the motor system that controls movements [1]. This output is precisely shaped by the inhibitory input to cerebellar nuclei neurons from cerebellar Purkinje neurons (PNs) in the cerebellar cortex, which also processes incoming motor information. Specifically, PNs fire action potentials at variable frequencies and these frequencies are modulated by the motor information received from the mossy fibres and processed by cerebellar granule cells (CGCs) that send excitatory parallel fibre (PF) inputs to PNs. The PN firing frequency can either increase or decrease during motor activity according to the balance of excitation * Marco Canepari [email protected] 1
University of Grenoble Alpes, CNRS, LIPhy, F-38000 Grenoble France
2
Laboratories of Excellence, Ion Channel Science and Therapeutics, Valbonne France
3
Institut National de la Santé et Recherche Médicale, Paris France
versus feed-forward inhibition by molecular layer interneurons (MLIs) also excited by the same PF inputs [2]. But the whole cerebellar system also receives a large sensory excitatory input through the climbing fibres (CFs) from the brainstem inferior olive targeting both PNs and cerebellar nuclei neurons. According to the early theory proposed by Marr [3] and Albus [4], the principal role of the CF input is to provide an “error” signal that weakens the concomitantly active PFs input, in t
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