Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale
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 cerebel...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2013-04-01
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| Series: | Frontiers in Neural Circuits |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fncir.2013.00064/full |
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| author | Daniela eGandolfi Daniela eGandolfi Paola eLombardo Jonathan eMapelli Jonathan eMapelli Sergio eSolinas Sergio eSolinas Egidio eD'Angelo Egidio eD'Angelo |
| author_facet | Daniela eGandolfi Daniela eGandolfi Paola eLombardo Jonathan eMapelli Jonathan eMapelli Sergio eSolinas Sergio eSolinas Egidio eD'Angelo Egidio eD'Angelo |
| author_sort | Daniela eGandolfi |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-11T21:56:35Z |
| format | Article |
| id | doaj.art-82266128ffef41b4bb37b07e651a752b |
| institution | Directory Open Access Journal |
| issn | 1662-5110 |
| language | English |
| last_indexed | 2024-12-11T21:56:35Z |
| publishDate | 2013-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj.art-82266128ffef41b4bb37b07e651a752b2022-12-22T00:49:16ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102013-04-01710.3389/fncir.2013.0006444565Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scaleDaniela eGandolfi0Daniela eGandolfi1Paola eLombardo2Jonathan eMapelli3Jonathan eMapelli4Sergio eSolinas5Sergio eSolinas6Egidio eD'Angelo7Egidio eD'Angelo8University of PaviaIRCCS Istituto Neurologico Nazionale C.MondinoUniversity of PaviaIRCCS Istituto Neurologico Nazionale C.MondinoUniversity of Modena and Reggio EmiliaIRCCS Istituto Neurologico Nazionale C.MondinoUniversity of PaviaIRCCS Istituto Neurologico Nazionale C.MondinoUniversity of PaviaThe 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.http://journal.frontiersin.org/Journal/10.3389/fncir.2013.00064/fullCerebellumresonancegranule cellsgranular layergolgi cells |
| spellingShingle | Daniela eGandolfi Daniela eGandolfi Paola eLombardo Jonathan eMapelli Jonathan eMapelli Sergio eSolinas Sergio eSolinas Egidio eD'Angelo Egidio eD'Angelo Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale Frontiers in Neural Circuits Cerebellum resonance granule cells granular layer golgi cells |
| title | Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale |
| title_full | Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale |
| title_fullStr | Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale |
| title_full_unstemmed | Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale |
| title_short | Theta-frequency resonance at the cerebellum input stage improves spike-timing on the millisecond time-scale |
| title_sort | theta frequency resonance at the cerebellum input stage improves spike timing on the millisecond time scale |
| topic | Cerebellum resonance granule cells granular layer golgi cells |
| url | http://journal.frontiersin.org/Journal/10.3389/fncir.2013.00064/full |
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