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A fast BK-type K(Ca) current acts as a postsynaptic modulator of temporal selectivity for communication signals
Temporal patterns of spiking often convey behaviorally relevant information. Various synaptic mechanisms and intrinsic membrane properties can influence neuronal selectivity to temporal patterns of input. However, little is known about how synaptic mechanisms and intrinsic properties together determ...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4166317/ https://www.ncbi.nlm.nih.gov/pubmed/25278836 http://dx.doi.org/10.3389/fncel.2014.00286 |
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author | Kohashi, Tsunehiko Carlson, Bruce A. |
author_facet | Kohashi, Tsunehiko Carlson, Bruce A. |
author_sort | Kohashi, Tsunehiko |
collection | PubMed |
description | Temporal patterns of spiking often convey behaviorally relevant information. Various synaptic mechanisms and intrinsic membrane properties can influence neuronal selectivity to temporal patterns of input. However, little is known about how synaptic mechanisms and intrinsic properties together determine the temporal selectivity of neuronal output. We tackled this question by recording from midbrain electrosensory neurons in mormyrid fish, in which the processing of temporal intervals between communication signals can be studied in a reduced in vitro preparation. Mormyrids communicate by varying interpulse intervals (IPIs) between electric pulses. Within the midbrain posterior exterolateral nucleus (ELp), the temporal patterns of afferent spike trains are filtered to establish single-neuron IPI tuning. We performed whole-cell recording from ELp neurons in a whole-brain preparation and examined the relationship between intrinsic excitability and IPI tuning. We found that spike frequency adaptation of ELp neurons was highly variable. Postsynaptic potentials (PSPs) of strongly adapting (phasic) neurons were more sharply tuned to IPIs than weakly adapting (tonic) neurons. Further, the synaptic filtering of IPIs by tonic neurons was more faithfully converted into variation in spiking output, particularly at short IPIs. Pharmacological manipulation under current- and voltage-clamp revealed that tonic firing is mediated by a fast, large-conductance Ca(2+)-activated K(+) (K(Ca)) current (BK) that speeds up action potential repolarization. These results suggest that BK currents can shape the temporal filtering of sensory inputs by modifying both synaptic responses and PSP-to-spike conversion. Slow SK-type K(Ca) currents have previously been implicated in temporal processing. Thus, both fast and slow K(Ca) currents can fine-tune temporal selectivity. |
format | Online Article Text |
id | pubmed-4166317 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-41663172014-10-02 A fast BK-type K(Ca) current acts as a postsynaptic modulator of temporal selectivity for communication signals Kohashi, Tsunehiko Carlson, Bruce A. Front Cell Neurosci Neuroscience Temporal patterns of spiking often convey behaviorally relevant information. Various synaptic mechanisms and intrinsic membrane properties can influence neuronal selectivity to temporal patterns of input. However, little is known about how synaptic mechanisms and intrinsic properties together determine the temporal selectivity of neuronal output. We tackled this question by recording from midbrain electrosensory neurons in mormyrid fish, in which the processing of temporal intervals between communication signals can be studied in a reduced in vitro preparation. Mormyrids communicate by varying interpulse intervals (IPIs) between electric pulses. Within the midbrain posterior exterolateral nucleus (ELp), the temporal patterns of afferent spike trains are filtered to establish single-neuron IPI tuning. We performed whole-cell recording from ELp neurons in a whole-brain preparation and examined the relationship between intrinsic excitability and IPI tuning. We found that spike frequency adaptation of ELp neurons was highly variable. Postsynaptic potentials (PSPs) of strongly adapting (phasic) neurons were more sharply tuned to IPIs than weakly adapting (tonic) neurons. Further, the synaptic filtering of IPIs by tonic neurons was more faithfully converted into variation in spiking output, particularly at short IPIs. Pharmacological manipulation under current- and voltage-clamp revealed that tonic firing is mediated by a fast, large-conductance Ca(2+)-activated K(+) (K(Ca)) current (BK) that speeds up action potential repolarization. These results suggest that BK currents can shape the temporal filtering of sensory inputs by modifying both synaptic responses and PSP-to-spike conversion. Slow SK-type K(Ca) currents have previously been implicated in temporal processing. Thus, both fast and slow K(Ca) currents can fine-tune temporal selectivity. Frontiers Media S.A. 2014-09-17 /pmc/articles/PMC4166317/ /pubmed/25278836 http://dx.doi.org/10.3389/fncel.2014.00286 Text en Copyright © 2014 Kohashi and Carlson. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Neuroscience Kohashi, Tsunehiko Carlson, Bruce A. A fast BK-type K(Ca) current acts as a postsynaptic modulator of temporal selectivity for communication signals |
title | A fast BK-type K(Ca) current acts as a postsynaptic modulator of temporal selectivity for communication signals |
title_full | A fast BK-type K(Ca) current acts as a postsynaptic modulator of temporal selectivity for communication signals |
title_fullStr | A fast BK-type K(Ca) current acts as a postsynaptic modulator of temporal selectivity for communication signals |
title_full_unstemmed | A fast BK-type K(Ca) current acts as a postsynaptic modulator of temporal selectivity for communication signals |
title_short | A fast BK-type K(Ca) current acts as a postsynaptic modulator of temporal selectivity for communication signals |
title_sort | fast bk-type k(ca) current acts as a postsynaptic modulator of temporal selectivity for communication signals |
topic | Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4166317/ https://www.ncbi.nlm.nih.gov/pubmed/25278836 http://dx.doi.org/10.3389/fncel.2014.00286 |
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