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[Preprint]. 2023 Aug 7:2023.08.05.552108. [Version 1] doi: 10.1101/2023.08.05.552108

Feed-forward metabotropic signaling by Cav1 Ca 2+ channels supports pacemaking in pedunculopontine cholinergic neurons

C Tubert, E Zampese, T Pancani, T Tkatch, D J Surmeier
PMCID: PMC10441306  PMID: 37609299

Abstract

Like a handful of other neuronal types in the brain, cholinergic neurons (CNs) in the pedunculopontine nucleus (PPN) are lost in the course of Parkinson’s disease (PD). Why this is the case is unknown. One neuronal trait implicated in PD selective neuronal vulnerability is the engagement of feed-forward stimulation of mitochondrial oxidative phosphorylation (OXPHOS) to meet high bioenergetic demand, leading to sustained oxidant stress and ultimately degeneration. The extent to which this trait is shared by PPN CNs is unresolved. To address this question, a combination of molecular and physiological approaches were used. These studies revealed that PPN CNs are autonomous pacemakers with modest spike-associated cytosolic Ca 2+ transients. These Ca 2+ transients were attributable in part to the opening of high-threshold Cav1.2 Ca 2+ channels, but not Cav1.3 channels. Nevertheless, Cav1.2 channel signaling through endoplasmic reticulum ryanodine receptors stimulated mitochondrial OXPHOS to help maintain cytosolic adenosine triphosphate (ATP) levels necessary for pacemaking. Inhibition of Cav1.2 channels led to recruitment of ATP-sensitive K + channels and slowing of pacemaking. Cav1.2 channel-mediated stimulation of mitochondria increased oxidant stress. Thus, PPN CNs have a distinctive physiological phenotype that shares some, but not all, of the features of other neurons that are selectively vulnerable in PD.

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