Transient BK outward current enhances motoneurone firing rates during Drosophila larval locomotion
- Publikationstyp:
- Zeitschriftenaufsatz
- Metadaten:
-
- Autoren
- Dimitrios Kadas
- Stefanie Ryglewski
- Carsten Duch
- Autoren-URL
- https://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=fis-test-1&SrcAuth=WosAPI&KeyUT=WOS:000365267700005&DestLinkType=FullRecord&DestApp=WOS_CPL
- DOI
- 10.1113/JP271323
- eISSN
- 1469-7793
- Externe Identifier
- Clarivate Analytics Document Solution ID: CW8RU
- PubMed Identifier: 26332699
- ISSN
- 0022-3751
- Ausgabe der Veröffentlichung
- 22
- Zeitschrift
- JOURNAL OF PHYSIOLOGY-LONDON
- Paginierung
- 4871 - 4888
- Datum der Veröffentlichung
- 2015
- Status
- Published
- Titel
- Transient BK outward current enhances motoneurone firing rates during <i>Drosophila</i> larval locomotion
- Sub types
- Article
- Ausgabe der Zeitschrift
- 593
Datenquelle: Web of Science (Lite)
- Andere Metadatenquellen:
-
- Abstract
- <jats:sec><jats:title>Key points</jats:title><jats:p><jats:list list-type="bullet"> <jats:list-item><jats:p>We combine <jats:italic>in situ</jats:italic> electrophysiology with genetic manipulation in <jats:italic>Drosophila</jats:italic> larvae aiming to investigate the role of fast calcium‐activated potassium currents for motoneurone firing patterns during locomotion.</jats:p></jats:list-item> <jats:list-item><jats:p>We first demonstrate that <jats:italic>slowpoke</jats:italic> channels underlie fast calcium‐activated potassium currents in these motoneurones.</jats:p></jats:list-item> <jats:list-item><jats:p>By conducting recordings in semi‐intact animals that produce crawling‐like movements, we show that <jats:italic>slowpoke</jats:italic> channels are required specifically in motoneurones for maximum firing rates during locomotion.</jats:p></jats:list-item> <jats:list-item><jats:p>Such enhancement of maximum firing rates occurs because <jats:italic>slowpoke</jats:italic> channels prevent depolarization block by limiting the amplitude of motoneurone depolarization in response to synaptic drive. In addition, <jats:italic>slowpoke</jats:italic> channels mediate a fast afterhyperpolarization that ensures the efficient recovery of sodium channels from inactivation during high frequency firing.</jats:p></jats:list-item> <jats:list-item><jats:p>The results of the present study provide new insights into the mechanisms by which outward conductances facilitate neuronal excitability and also provide direct confirmation of the functional relevance of precisely regulated <jats:italic>slowpoke</jats:italic> channel properties in motor control.</jats:p></jats:list-item> </jats:list></jats:p></jats:sec><jats:sec><jats:title>Abstract</jats:title><jats:p>A large number of voltage‐gated ion channels, their interactions with accessory subunits, and their post‐transcriptional modifications generate an immense functional diversity of neurones. Therefore, a key challenge is to understand the genetic basis and precise function of specific ionic conductances for neuronal firing properties in the context of behaviour. The present study identifies <jats:italic>slowpoke</jats:italic> (<jats:italic>slo</jats:italic>) as exclusively mediating fast activating, fast inactivating BK current (<jats:italic>I</jats:italic><jats:sub>CF</jats:sub>) in larval <jats:italic>Drosophila</jats:italic> crawling motoneurones. Combining <jats:italic>in vivo</jats:italic> patch clamp recordings during larval crawling with pharmacology and targeted genetic manipulations reveals that <jats:italic>I</jats:italic><jats:sub>CF</jats:sub> acts specifically in motoneurones to sculpt their firing patterns in response to a given input from the central pattern generating (CPG) networks. First, <jats:italic>I</jats:italic><jats:sub>CF</jats:sub> curtails motoneurone postsynaptic depolarizations during rhythmical CPG drive. Second, <jats:italic>I</jats:italic><jats:sub>CF</jats:sub> is activated during the rising phase of the action potential and mediates a fast afterhyperpolarization. Consequently, <jats:italic>I</jats:italic><jats:sub>CF</jats:sub> is required for maximal intraburst firing rates during locomotion, probably by allowing recovery from inactivation of fast sodium channels and decreased potassium channel activation. This contrasts the common view that outward conductances oppose excitability but is in accordance with reports on transient BK and Kv3 channel function in multiple types of vertebrate neurones. Therefore, our finding that <jats:italic>I</jats:italic><jats:sub>CF</jats:sub> enhances firing rates specifically during bursting patterns relevant to behaviour is probably of relevance to all brains.</jats:p></jats:sec>
- Autoren
- Dimitrios Kadas
- Stefanie Ryglewski
- Carsten Duch
- DOI
- 10.1113/jp271323
- eISSN
- 1469-7793
- ISSN
- 0022-3751
- Ausgabe der Veröffentlichung
- 22
- Zeitschrift
- The Journal of Physiology
- Sprache
- en
- Online publication date
- 2015
- Paginierung
- 4871 - 4888
- Datum der Veröffentlichung
- 2015
- Status
- Published
- Herausgeber
- Wiley
- Herausgeber URL
- http://dx.doi.org/10.1113/jp271323
- Datum der Datenerfassung
- 2023
- Titel
- Transient BK outward current enhances motoneurone firing rates during <i>Drosophila</i> larval locomotion
- Ausgabe der Zeitschrift
- 593
Datenquelle: Crossref
- Abstract
- <h4>Key points</h4>We combine in situ electrophysiology with genetic manipulation in Drosophila larvae aiming to investigate the role of fast calcium-activated potassium currents for motoneurone firing patterns during locomotion. We first demonstrate that slowpoke channels underlie fast calcium-activated potassium currents in these motoneurones. By conducting recordings in semi-intact animals that produce crawling-like movements, we show that slowpoke channels are required specifically in motoneurones for maximum firing rates during locomotion. Such enhancement of maximum firing rates occurs because slowpoke channels prevent depolarization block by limiting the amplitude of motoneurone depolarization in response to synaptic drive. In addition, slowpoke channels mediate a fast afterhyperpolarization that ensures the efficient recovery of sodium channels from inactivation during high frequency firing. The results of the present study provide new insights into the mechanisms by which outward conductances facilitate neuronal excitability and also provide direct confirmation of the functional relevance of precisely regulated slowpoke channel properties in motor control.<h4>Abstract</h4>A large number of voltage-gated ion channels, their interactions with accessory subunits, and their post-transcriptional modifications generate an immense functional diversity of neurones. Therefore, a key challenge is to understand the genetic basis and precise function of specific ionic conductances for neuronal firing properties in the context of behaviour. The present study identifies slowpoke (slo) as exclusively mediating fast activating, fast inactivating BK current (ICF ) in larval Drosophila crawling motoneurones. Combining in vivo patch clamp recordings during larval crawling with pharmacology and targeted genetic manipulations reveals that ICF acts specifically in motoneurones to sculpt their firing patterns in response to a given input from the central pattern generating (CPG) networks. First, ICF curtails motoneurone postsynaptic depolarizations during rhythmical CPG drive. Second, ICF is activated during the rising phase of the action potential and mediates a fast afterhyperpolarization. Consequently, ICF is required for maximal intraburst firing rates during locomotion, probably by allowing recovery from inactivation of fast sodium channels and decreased potassium channel activation. This contrasts the common view that outward conductances oppose excitability but is in accordance with reports on transient BK and Kv3 channel function in multiple types of vertebrate neurones. Therefore, our finding that ICF enhances firing rates specifically during bursting patterns relevant to behaviour is probably of relevance to all brains.
- Addresses
- Institute of Neurobiology, Johannes Gutenberg University of Mainz, Mainz, Germany.
- Autoren
- Dimitrios Kadas
- Stefanie Ryglewski
- Carsten Duch
- DOI
- 10.1113/jp271323
- eISSN
- 1469-7793
- Externe Identifier
- PubMed Identifier: 26332699
- Funding acknowledgements
- NINDS NIH HHS: R01 NS072128
- Deutsche Forschungsgemeinschaft: DFG Du-331/6-1
- Open access
- false
- ISSN
- 0022-3751
- Ausgabe der Veröffentlichung
- 22
- Zeitschrift
- The Journal of physiology
- Schlüsselwörter
- Motor Neurons
- Animals
- Drosophila melanogaster
- Drosophila Proteins
- Action Potentials
- Larva
- Locomotion
- Large-Conductance Calcium-Activated Potassium Channels
- Central Pattern Generators
- Sprache
- eng
- Medium
- Print-Electronic
- Online publication date
- 2015
- Paginierung
- 4871 - 4888
- Datum der Veröffentlichung
- 2015
- Status
- Published
- Datum der Datenerfassung
- 2015
- Titel
- Transient BK outward current enhances motoneurone firing rates during Drosophila larval locomotion.
- Sub types
- Research Support, Non-U.S. Gov't
- Journal Article
- Ausgabe der Zeitschrift
- 593
Datenquelle: Europe PubMed Central
- Abstract
- KEY POINTS: We combine in situ electrophysiology with genetic manipulation in Drosophila larvae aiming to investigate the role of fast calcium-activated potassium currents for motoneurone firing patterns during locomotion. We first demonstrate that slowpoke channels underlie fast calcium-activated potassium currents in these motoneurones. By conducting recordings in semi-intact animals that produce crawling-like movements, we show that slowpoke channels are required specifically in motoneurones for maximum firing rates during locomotion. Such enhancement of maximum firing rates occurs because slowpoke channels prevent depolarization block by limiting the amplitude of motoneurone depolarization in response to synaptic drive. In addition, slowpoke channels mediate a fast afterhyperpolarization that ensures the efficient recovery of sodium channels from inactivation during high frequency firing. The results of the present study provide new insights into the mechanisms by which outward conductances facilitate neuronal excitability and also provide direct confirmation of the functional relevance of precisely regulated slowpoke channel properties in motor control. ABSTRACT: A large number of voltage-gated ion channels, their interactions with accessory subunits, and their post-transcriptional modifications generate an immense functional diversity of neurones. Therefore, a key challenge is to understand the genetic basis and precise function of specific ionic conductances for neuronal firing properties in the context of behaviour. The present study identifies slowpoke (slo) as exclusively mediating fast activating, fast inactivating BK current (ICF ) in larval Drosophila crawling motoneurones. Combining in vivo patch clamp recordings during larval crawling with pharmacology and targeted genetic manipulations reveals that ICF acts specifically in motoneurones to sculpt their firing patterns in response to a given input from the central pattern generating (CPG) networks. First, ICF curtails motoneurone postsynaptic depolarizations during rhythmical CPG drive. Second, ICF is activated during the rising phase of the action potential and mediates a fast afterhyperpolarization. Consequently, ICF is required for maximal intraburst firing rates during locomotion, probably by allowing recovery from inactivation of fast sodium channels and decreased potassium channel activation. This contrasts the common view that outward conductances oppose excitability but is in accordance with reports on transient BK and Kv3 channel function in multiple types of vertebrate neurones. Therefore, our finding that ICF enhances firing rates specifically during bursting patterns relevant to behaviour is probably of relevance to all brains.
- Date of acceptance
- 2015
- Autoren
- Dimitrios Kadas
- Stefanie Ryglewski
- Carsten Duch
- Autoren-URL
- https://www.ncbi.nlm.nih.gov/pubmed/26332699
- DOI
- 10.1113/JP271323
- eISSN
- 1469-7793
- Externe Identifier
- PubMed Central ID: PMC4650413
- Funding acknowledgements
- NINDS NIH HHS: R01 NS072128
- Ausgabe der Veröffentlichung
- 22
- Zeitschrift
- J Physiol
- Schlüsselwörter
- Action Potentials
- Animals
- Central Pattern Generators
- Drosophila Proteins
- Drosophila melanogaster
- Large-Conductance Calcium-Activated Potassium Channels
- Larva
- Locomotion
- Motor Neurons
- Sprache
- eng
- Country
- England
- Paginierung
- 4871 - 4888
- Datum der Veröffentlichung
- 2015
- Status
- Published
- Datum, an dem der Datensatz öffentlich gemacht wurde
- 2016
- Titel
- Transient BK outward current enhances motoneurone firing rates during Drosophila larval locomotion.
- Sub types
- Journal Article
- Research Support, Non-U.S. Gov't
- Ausgabe der Zeitschrift
- 593
Datenquelle: PubMed
- Beziehungen:
- Eigentum von