title: Neuronal morphology generates high-frequency firing resonance.
abstract: The attenuation of neuronal voltage responses to high-frequency current inputs by the membrane capacitance is believed to limit single-cell bandwidth. However, neuronal populations subject to stochastic fluctuations can follow inputs beyond this limit. We investigated this apparent paradox theoretically and experimentally using Purkinje cells in the cerebellum, a motor structure that benefits from rapid information transfer. We analyzed the modulation of firing in response to the somatic injection of sinusoidal currents. Computational modeling suggested that, instead of decreasing with frequency, modulation amplitude can increase up to high frequencies because of cellular morphology. Electrophysiological measurements in adult rat slices confirmed this prediction and displayed a marked resonance at 200 Hz. We elucidated the underlying mechanism, showing that the two-compartment morphology of the Purkinje cell, interacting with a simple spiking mechanism and dendritic fluctuations, is sufficient to create high-frequency signal amplification. This mechanism, which we term morphology-induced resonance, is selective for somatic inputs, which in the Purkinje cell are exclusively inhibitory. The resonance sensitizes Purkinje cells in the frequency range of population oscillations observed in vivo.
authors.affiliation: Laboratoire de Neurosciences Cognitives, Institut National de la Santé et de la Recherche Médicale (INSERM) Unité 960, srdjan.ostojic@ens.fr.
authors.forename: Srdjan
authors.identifier: http://orcid.org/0000-0002-7473-1223
authors.initials: S
authors.lastname: Ostojic
authors.affiliation: Ecole Normale Supérieure, Institute de Biologie (IBENS), Centre National de la Recherche Scientifique (CNRS) Unité Mixte de Recherche (UMR) 8197, and INSERM Unité 1024, Paris, F-75005 France.
authors.forename: Germán
authors.initials: G
authors.lastname: Szapiro
authors.affiliation: Ecole Normale Supérieure, Institute de Biologie (IBENS), Centre National de la Recherche Scientifique (CNRS) Unité Mixte de Recherche (UMR) 8197, and INSERM Unité 1024, Paris, F-75005 France.
authors.forename: Eric
authors.initials: E
authors.lastname: Schwartz
authors.affiliation: Ecole Normale Supérieure, Institute de Biologie (IBENS), Centre National de la Recherche Scientifique (CNRS) Unité Mixte de Recherche (UMR) 8197, and INSERM Unité 1024, Paris, F-75005 France.
authors.forename: Boris
authors.initials: B
authors.lastname: Barbour
authors.affiliation: Departments of Statistics and Neurobiology, University of Chicago, Chicago, Illinois 60637.
authors.forename: Nicolas
authors.initials: N
authors.lastname: Brunel
authors.affiliation: Laboratoire de Physique Statistique, CNRS UMR 8550, Ecole Normale Supérieure, F-75231 Paris, France, and.
authors.forename: Vincent
authors.initials: V
authors.lastname: Hakim
mesh_terms: D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D002531:Cerebellum / Q000166:cytology / Q000502:physiology; D008297:Male; D009474:Neurons / Q000502:physiology*; D011689:Purkinje Cells / Q000502:physiology*; D051381:Rats; D017208:Rats, Wistar
keywords: Purkinje cell; computational modelling; information bandwidth; neural dynamics