Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: Simulations of their impact <I>in vivo</I>
The Golgi cells are inhibitory interneurons of the cerebellar granular layer, which respond to afferent stimulation <I>in vivo</I> with a burst-pause sequence interrupting their irregular background low-frequency firing (Vos et al., 1999a. <I>Eur. J. Neurosci.</I> 11, 2621&am...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2007-12-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/neuro.03.004.2007/full |
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| author | Sergio Solinas Sergio Solinas Lia Forti Elisabetta Cesana Jonathan Mapelli Erik De Schutter Erik De Schutter Egidio D‘Angelo |
| author_facet | Sergio Solinas Sergio Solinas Lia Forti Elisabetta Cesana Jonathan Mapelli Erik De Schutter Erik De Schutter Egidio D‘Angelo |
| author_sort | Sergio Solinas |
| collection | DOAJ |
| description | The Golgi cells are inhibitory interneurons of the cerebellar granular layer, which respond to afferent stimulation <I>in vivo</I> with a burst-pause sequence interrupting their irregular background low-frequency firing (Vos et al., 1999a. <I>Eur. J. Neurosci.</I> 11, 2621–2634). However, Golgi cells <I>in vitro</I> are regular pacemakers (Forti et al., 2006. <I>J. Physiol.</I> 574, 711–729), raising the question how their ionic mechanisms could impact on responses during physiological activity. Using patch-clamp recordings in cerebellar slices we show that the pacemaker cycle can be suddenly reset by spikes, making the cell highly sensitive to input variations. Moreover, the neuron resonates around the pacemaker frequency, making it specifically sensitive to patterned stimulation in the theta-frequency band. Computational analysis based on a model developed to reproduce Golgi cell pacemaking (Solinas et al., 2008 <I>Front. Neurosci.</I>, 1:2) predicted that phase-reset required spike-triggered activation of SK channels and that resonance was sustained by a slow voltage-dependent potassium current and amplified by a persistent sodium current. Adding balanced synaptic noise to mimic the irregular discharge observed <I>in vivo</I>, we found that pacemaking converts into spontaneous irregular discharge, that phase-reset plays an important role in generating the burst-pause pattern evoked by sensory stimulation, and that repetitive stimulation at theta-frequency enhances the time-precision of spike coding in the burst. These results suggest that Golgi cell intrinsic properties exert a profound impact on time-dependent signal processing in the cerebellar granular layer. |
| first_indexed | 2024-12-24T03:12:15Z |
| format | Article |
| id | doaj.art-c1c34b3304b841c1978828c7d3d87dde |
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| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-12-24T03:12:15Z |
| publishDate | 2007-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-c1c34b3304b841c1978828c7d3d87dde2022-12-21T17:17:47ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022007-12-01110.3389/neuro.03.004.2007166Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: Simulations of their impact <I>in vivo</I>Sergio Solinas0Sergio Solinas1Lia Forti2Elisabetta Cesana3Jonathan Mapelli4Erik De Schutter5Erik De Schutter6Egidio D‘Angelo7Department of Cellular and Molecular Physiological and Pharmacological Sciences, University of Pavia and CNISMTheoretical Neurobiology, University of AntwerpDepartment of Cellular and Molecular Physiological and Pharmacological Sciences, University of Pavia and CNISMDepartment of Cellular and Molecular Physiological and Pharmacological Sciences, University of Pavia and CNISMDepartment of Cellular and Molecular Physiological and Pharmacological Sciences, University of Pavia and CNISMComputational Neuroscience Unit, Okinawa Institute of Science and TechnologyTheoretical Neurobiology, University of AntwerpDepartment of Cellular and Molecular Physiological and Pharmacological Sciences, University of Pavia and CNISMThe Golgi cells are inhibitory interneurons of the cerebellar granular layer, which respond to afferent stimulation <I>in vivo</I> with a burst-pause sequence interrupting their irregular background low-frequency firing (Vos et al., 1999a. <I>Eur. J. Neurosci.</I> 11, 2621–2634). However, Golgi cells <I>in vitro</I> are regular pacemakers (Forti et al., 2006. <I>J. Physiol.</I> 574, 711–729), raising the question how their ionic mechanisms could impact on responses during physiological activity. Using patch-clamp recordings in cerebellar slices we show that the pacemaker cycle can be suddenly reset by spikes, making the cell highly sensitive to input variations. Moreover, the neuron resonates around the pacemaker frequency, making it specifically sensitive to patterned stimulation in the theta-frequency band. Computational analysis based on a model developed to reproduce Golgi cell pacemaking (Solinas et al., 2008 <I>Front. Neurosci.</I>, 1:2) predicted that phase-reset required spike-triggered activation of SK channels and that resonance was sustained by a slow voltage-dependent potassium current and amplified by a persistent sodium current. Adding balanced synaptic noise to mimic the irregular discharge observed <I>in vivo</I>, we found that pacemaking converts into spontaneous irregular discharge, that phase-reset plays an important role in generating the burst-pause pattern evoked by sensory stimulation, and that repetitive stimulation at theta-frequency enhances the time-precision of spike coding in the burst. These results suggest that Golgi cell intrinsic properties exert a profound impact on time-dependent signal processing in the cerebellar granular layer.http://journal.frontiersin.org/Journal/10.3389/neuro.03.004.2007/fullCerebellummodelingresonancegolgi cellgranular layerphase-reset |
| spellingShingle | Sergio Solinas Sergio Solinas Lia Forti Elisabetta Cesana Jonathan Mapelli Erik De Schutter Erik De Schutter Egidio D‘Angelo Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: Simulations of their impact <I>in vivo</I> Frontiers in Cellular Neuroscience Cerebellum modeling resonance golgi cell granular layer phase-reset |
| title | Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: Simulations of their impact <I>in vivo</I> |
| title_full | Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: Simulations of their impact <I>in vivo</I> |
| title_fullStr | Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: Simulations of their impact <I>in vivo</I> |
| title_full_unstemmed | Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: Simulations of their impact <I>in vivo</I> |
| title_short | Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: Simulations of their impact <I>in vivo</I> |
| title_sort | fast reset of pacemaking and theta frequency resonance patterns in cerebellar golgi cells simulations of their impact i in vivo i |
| topic | Cerebellum modeling resonance golgi cell granular layer phase-reset |
| url | http://journal.frontiersin.org/Journal/10.3389/neuro.03.004.2007/full |
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