Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale

D. Gandolfi, P. Lombardo, J. Mapelli, S. Solinas, E. D'Angelo

Research output: Contribution to journalArticle

Abstract

The neuronal circuits of the brain are thought to use resonance and oscillations to improve communication over specific frequency bands (Llinas, 1988; Buzsaki, 2006). However, the properties and mechanism of these phenomena in brain circuits remain largely unknown. Here we show that, at the cerebellum input stage, the granular layer generates its maximum response at 5-7 Hz both in vivo following tactile sensory stimulation of the whisker pad and in acute slices following mossy fiber-bundle stimulation. The spatial analysis of granular layer activity performed using voltage-sensitive dye (VSD) imaging revealed 5-7 Hz resonance covering large granular layer areas. In single granule cells, resonance appeared as a reorganization of output spike bursts on the millisecond time-scale, such that the first spike occurred earlier and with higher temporal precision and the probability of spike generation increased. Resonance was independent from circuit inhibition, as it persisted with little variation in the presence of the GABAA receptor blocker, gabazine. However, circuit inhibition reduced the resonance area more markedly at 7 Hz. Simulations with detailed computational models suggested that resonance depended on intrinsic granule cells ionic mechanisms: specifically, Kslow (M-like) and KA currents acted as resonators and the persistent Na current and NMDA current acted as amplifiers. This form of resonance may play an important role for enhancing coherent spike emission from the granular layer when theta-frequency bursts are transmitted by the cerebral cortex and peripheral sensory structures during sensory-motor processing, cognition and learning.

Original languageEnglish
JournalFrontiers in Neural Circuits
Issue numberMAR
DOIs
Publication statusPublished - Mar 20 2013

Fingerprint

Cerebellum
Voltage-Sensitive Dye Imaging
Vibrissae
Spatial Analysis
Brain
Touch
N-Methylaspartate
GABA-A Receptors
Cerebral Cortex
Cognition
Communication
Learning
Inhibition (Psychology)
gabazine

Keywords

  • Cerebellum
  • Granular layer
  • Resonance

ASJC Scopus subject areas

  • Neuroscience (miscellaneous)
  • Cellular and Molecular Neuroscience
  • Sensory Systems
  • Cognitive Neuroscience

Cite this

Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale. / Gandolfi, D.; Lombardo, P.; Mapelli, J.; Solinas, S.; D'Angelo, E.

In: Frontiers in Neural Circuits, No. MAR, 20.03.2013.

Research output: Contribution to journalArticle

@article{3918b578e59d458eb3d1c5f4f77c1a79,
title = "Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale",
abstract = "The neuronal circuits of the brain are thought to use resonance and oscillations to improve communication over specific frequency bands (Llinas, 1988; Buzsaki, 2006). However, the properties and mechanism of these phenomena in brain circuits remain largely unknown. Here we show that, at the cerebellum input stage, the granular layer generates its maximum response at 5-7 Hz both in vivo following tactile sensory stimulation of the whisker pad and in acute slices following mossy fiber-bundle stimulation. The spatial analysis of granular layer activity performed using voltage-sensitive dye (VSD) imaging revealed 5-7 Hz resonance covering large granular layer areas. In single granule cells, resonance appeared as a reorganization of output spike bursts on the millisecond time-scale, such that the first spike occurred earlier and with higher temporal precision and the probability of spike generation increased. Resonance was independent from circuit inhibition, as it persisted with little variation in the presence of the GABAA receptor blocker, gabazine. However, circuit inhibition reduced the resonance area more markedly at 7 Hz. Simulations with detailed computational models suggested that resonance depended on intrinsic granule cells ionic mechanisms: specifically, Kslow (M-like) and KA currents acted as resonators and the persistent Na current and NMDA current acted as amplifiers. This form of resonance may play an important role for enhancing coherent spike emission from the granular layer when theta-frequency bursts are transmitted by the cerebral cortex and peripheral sensory structures during sensory-motor processing, cognition and learning.",
keywords = "Cerebellum, Granular layer, Resonance",
author = "D. Gandolfi and P. Lombardo and J. Mapelli and S. Solinas and E. D'Angelo",
year = "2013",
month = "3",
day = "20",
doi = "10.3389/fncir.2013.00064",
language = "English",
journal = "Frontiers in Neural Circuits",
issn = "1662-5110",
publisher = "Frontiers Research Foundation",
number = "MAR",

}

TY - JOUR

T1 - Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale

AU - Gandolfi, D.

AU - Lombardo, P.

AU - Mapelli, J.

AU - Solinas, S.

AU - D'Angelo, E.

PY - 2013/3/20

Y1 - 2013/3/20

N2 - The neuronal circuits of the brain are thought to use resonance and oscillations to improve communication over specific frequency bands (Llinas, 1988; Buzsaki, 2006). However, the properties and mechanism of these phenomena in brain circuits remain largely unknown. Here we show that, at the cerebellum input stage, the granular layer generates its maximum response at 5-7 Hz both in vivo following tactile sensory stimulation of the whisker pad and in acute slices following mossy fiber-bundle stimulation. The spatial analysis of granular layer activity performed using voltage-sensitive dye (VSD) imaging revealed 5-7 Hz resonance covering large granular layer areas. In single granule cells, resonance appeared as a reorganization of output spike bursts on the millisecond time-scale, such that the first spike occurred earlier and with higher temporal precision and the probability of spike generation increased. Resonance was independent from circuit inhibition, as it persisted with little variation in the presence of the GABAA receptor blocker, gabazine. However, circuit inhibition reduced the resonance area more markedly at 7 Hz. Simulations with detailed computational models suggested that resonance depended on intrinsic granule cells ionic mechanisms: specifically, Kslow (M-like) and KA currents acted as resonators and the persistent Na current and NMDA current acted as amplifiers. This form of resonance may play an important role for enhancing coherent spike emission from the granular layer when theta-frequency bursts are transmitted by the cerebral cortex and peripheral sensory structures during sensory-motor processing, cognition and learning.

AB - The neuronal circuits of the brain are thought to use resonance and oscillations to improve communication over specific frequency bands (Llinas, 1988; Buzsaki, 2006). However, the properties and mechanism of these phenomena in brain circuits remain largely unknown. Here we show that, at the cerebellum input stage, the granular layer generates its maximum response at 5-7 Hz both in vivo following tactile sensory stimulation of the whisker pad and in acute slices following mossy fiber-bundle stimulation. The spatial analysis of granular layer activity performed using voltage-sensitive dye (VSD) imaging revealed 5-7 Hz resonance covering large granular layer areas. In single granule cells, resonance appeared as a reorganization of output spike bursts on the millisecond time-scale, such that the first spike occurred earlier and with higher temporal precision and the probability of spike generation increased. Resonance was independent from circuit inhibition, as it persisted with little variation in the presence of the GABAA receptor blocker, gabazine. However, circuit inhibition reduced the resonance area more markedly at 7 Hz. Simulations with detailed computational models suggested that resonance depended on intrinsic granule cells ionic mechanisms: specifically, Kslow (M-like) and KA currents acted as resonators and the persistent Na current and NMDA current acted as amplifiers. This form of resonance may play an important role for enhancing coherent spike emission from the granular layer when theta-frequency bursts are transmitted by the cerebral cortex and peripheral sensory structures during sensory-motor processing, cognition and learning.

KW - Cerebellum

KW - Granular layer

KW - Resonance

UR - http://www.scopus.com/inward/record.url?scp=84875513520&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84875513520&partnerID=8YFLogxK

U2 - 10.3389/fncir.2013.00064

DO - 10.3389/fncir.2013.00064

M3 - Article

AN - SCOPUS:84875513520

JO - Frontiers in Neural Circuits

JF - Frontiers in Neural Circuits

SN - 1662-5110

IS - MAR

ER -