Glutamatergic control of a pattern-generating central nucleus in a gymnotiform fish

The activity of central pattern-generating networks (CPGs) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates,...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Journal of neurophysiology 2021-06, Vol.125 (6), p.2339-2355
Hauptverfasser: Comas, Virginia, Borde, Michel
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 2355
container_issue 6
container_start_page 2339
container_title Journal of neurophysiology
container_volume 125
creator Comas, Virginia
Borde, Michel
description The activity of central pattern-generating networks (CPGs) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates, most of their synaptic and cellular bases are not yet well understood in vertebrates. , a pulse-type gymnotiform electric fish, provides a well-suited vertebrate model to investigate these mechanisms. emits rhythmic and stereotyped electric organ discharges (EODs), which function in both perception and communication, under the command of an electromotor CPG. This nucleus is composed of electrotonically coupled intrinsic pacemaker cells, which pace the rhythm, and bulbospinal projecting relay cells that contribute to organize the pattern of the muscle-derived effector activation that produce the EOD. Descending influences target CPG neurons to produce adaptive behavioral electromotor responses to different environmental challenges. We used electrophysiological and pharmacological techniques in brainstem slices of to investigate the underpinnings of the fast transmitter control of its electromotor CPG. We demonstrate that pacemaker, but not relay cells, are endowed with ionotropic and metabotropic glutamate receptor subtypes. We also show that glutamatergic control of the CPG likely involves two types of synapses contacting pacemaker cells, one type containing both α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and -methyl-d-aspartate (NMDA) receptors and the other one only-NMDA receptor. Fast neurotransmitter control of vertebrate CPGs seems to exploit the kinetics of the involved postsynaptic receptors to command different behavioral outputs. The prospect of common neural designs to control CPG activity in vertebrates is discussed. Underpinnings of neuromodulation of central pattern-generating networks (CPG) have been well characterized in many species. The effects of fast neurotransmitter systems remain, however, poorly understood. This research uses in vitro electrophysiological and pharmacological techniques to show that the neurotransmitter control of a vertebrate CPG in gymnotiform fish involves the convergence of only-NMDA and AMPA-NMDA glutamatergic synapses onto neurons that pace the rhythm. These inputs may organize different behavioral outputs according to their distinct functional properties.
doi_str_mv 10.1152/jn.00584.2020
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2526138471</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2526138471</sourcerecordid><originalsourceid>FETCH-LOGICAL-c332t-26fae5862f3c185b08b67f55798cea23a37f8f9acce929781487393cd97e2f5c3</originalsourceid><addsrcrecordid>eNo9kE1PAyEURYnR2FpdujUs3UzlYxhgaRqtJk1cqGtCKYzTzEAFZtF_L7XV1Xu57-Tm5QBwi9EcY0Yetn6OEBP1nCCCzsC0ZKTCTIpzMEWo7BRxPgFXKW0RQpwhcgkmlEouakmm4H3Zj1kPOtvYdgaa4HMMPQwOarjTucS-aq23UefOt9DYctc99KPp7Zhg5wvX7gcfcudCHKDr0tc1uHC6T_bmNGfg8_npY_FSrd6Wr4vHVWUoJbkijdOWiYY4arBgayTWDXeMcSmM1YRqyp1wUhtjJSn_4lpwKqnZSG6JY4bOwP2xdxfD92hTVkOXjO177W0YkyKMNJiKmuOCVkfUxJBStE7tYjfouFcYqYNHtfXq16M6eCz83al6XA9280__iaM_muBuXw</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2526138471</pqid></control><display><type>article</type><title>Glutamatergic control of a pattern-generating central nucleus in a gymnotiform fish</title><source>MEDLINE</source><source>American Physiological Society</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Alma/SFX Local Collection</source><creator>Comas, Virginia ; Borde, Michel</creator><creatorcontrib>Comas, Virginia ; Borde, Michel</creatorcontrib><description>The activity of central pattern-generating networks (CPGs) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates, most of their synaptic and cellular bases are not yet well understood in vertebrates. , a pulse-type gymnotiform electric fish, provides a well-suited vertebrate model to investigate these mechanisms. emits rhythmic and stereotyped electric organ discharges (EODs), which function in both perception and communication, under the command of an electromotor CPG. This nucleus is composed of electrotonically coupled intrinsic pacemaker cells, which pace the rhythm, and bulbospinal projecting relay cells that contribute to organize the pattern of the muscle-derived effector activation that produce the EOD. Descending influences target CPG neurons to produce adaptive behavioral electromotor responses to different environmental challenges. We used electrophysiological and pharmacological techniques in brainstem slices of to investigate the underpinnings of the fast transmitter control of its electromotor CPG. We demonstrate that pacemaker, but not relay cells, are endowed with ionotropic and metabotropic glutamate receptor subtypes. We also show that glutamatergic control of the CPG likely involves two types of synapses contacting pacemaker cells, one type containing both α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and -methyl-d-aspartate (NMDA) receptors and the other one only-NMDA receptor. Fast neurotransmitter control of vertebrate CPGs seems to exploit the kinetics of the involved postsynaptic receptors to command different behavioral outputs. The prospect of common neural designs to control CPG activity in vertebrates is discussed. Underpinnings of neuromodulation of central pattern-generating networks (CPG) have been well characterized in many species. The effects of fast neurotransmitter systems remain, however, poorly understood. This research uses in vitro electrophysiological and pharmacological techniques to show that the neurotransmitter control of a vertebrate CPG in gymnotiform fish involves the convergence of only-NMDA and AMPA-NMDA glutamatergic synapses onto neurons that pace the rhythm. These inputs may organize different behavioral outputs according to their distinct functional properties.</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.00584.2020</identifier><identifier>PMID: 33978492</identifier><language>eng</language><publisher>United States</publisher><subject>Animals ; Biological Clocks - drug effects ; Biological Clocks - physiology ; Central Pattern Generators - drug effects ; Central Pattern Generators - metabolism ; Electric Stimulation ; Electrophysiological Phenomena - drug effects ; Electrophysiological Phenomena - physiology ; Excitatory Amino Acid Agonists - pharmacology ; Excitatory Amino Acid Antagonists - pharmacology ; Gymnotiformes - metabolism ; Gymnotiformes - physiology ; Receptors, Ionotropic Glutamate - drug effects ; Receptors, Ionotropic Glutamate - metabolism ; Receptors, Metabotropic Glutamate - drug effects ; Receptors, Metabotropic Glutamate - metabolism</subject><ispartof>Journal of neurophysiology, 2021-06, Vol.125 (6), p.2339-2355</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c332t-26fae5862f3c185b08b67f55798cea23a37f8f9acce929781487393cd97e2f5c3</citedby><cites>FETCH-LOGICAL-c332t-26fae5862f3c185b08b67f55798cea23a37f8f9acce929781487393cd97e2f5c3</cites><orcidid>0000-0002-7227-5607 ; 0000-0002-5729-8616</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,3026,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33978492$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Comas, Virginia</creatorcontrib><creatorcontrib>Borde, Michel</creatorcontrib><title>Glutamatergic control of a pattern-generating central nucleus in a gymnotiform fish</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>The activity of central pattern-generating networks (CPGs) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates, most of their synaptic and cellular bases are not yet well understood in vertebrates. , a pulse-type gymnotiform electric fish, provides a well-suited vertebrate model to investigate these mechanisms. emits rhythmic and stereotyped electric organ discharges (EODs), which function in both perception and communication, under the command of an electromotor CPG. This nucleus is composed of electrotonically coupled intrinsic pacemaker cells, which pace the rhythm, and bulbospinal projecting relay cells that contribute to organize the pattern of the muscle-derived effector activation that produce the EOD. Descending influences target CPG neurons to produce adaptive behavioral electromotor responses to different environmental challenges. We used electrophysiological and pharmacological techniques in brainstem slices of to investigate the underpinnings of the fast transmitter control of its electromotor CPG. We demonstrate that pacemaker, but not relay cells, are endowed with ionotropic and metabotropic glutamate receptor subtypes. We also show that glutamatergic control of the CPG likely involves two types of synapses contacting pacemaker cells, one type containing both α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and -methyl-d-aspartate (NMDA) receptors and the other one only-NMDA receptor. Fast neurotransmitter control of vertebrate CPGs seems to exploit the kinetics of the involved postsynaptic receptors to command different behavioral outputs. The prospect of common neural designs to control CPG activity in vertebrates is discussed. Underpinnings of neuromodulation of central pattern-generating networks (CPG) have been well characterized in many species. The effects of fast neurotransmitter systems remain, however, poorly understood. This research uses in vitro electrophysiological and pharmacological techniques to show that the neurotransmitter control of a vertebrate CPG in gymnotiform fish involves the convergence of only-NMDA and AMPA-NMDA glutamatergic synapses onto neurons that pace the rhythm. These inputs may organize different behavioral outputs according to their distinct functional properties.</description><subject>Animals</subject><subject>Biological Clocks - drug effects</subject><subject>Biological Clocks - physiology</subject><subject>Central Pattern Generators - drug effects</subject><subject>Central Pattern Generators - metabolism</subject><subject>Electric Stimulation</subject><subject>Electrophysiological Phenomena - drug effects</subject><subject>Electrophysiological Phenomena - physiology</subject><subject>Excitatory Amino Acid Agonists - pharmacology</subject><subject>Excitatory Amino Acid Antagonists - pharmacology</subject><subject>Gymnotiformes - metabolism</subject><subject>Gymnotiformes - physiology</subject><subject>Receptors, Ionotropic Glutamate - drug effects</subject><subject>Receptors, Ionotropic Glutamate - metabolism</subject><subject>Receptors, Metabotropic Glutamate - drug effects</subject><subject>Receptors, Metabotropic Glutamate - metabolism</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kE1PAyEURYnR2FpdujUs3UzlYxhgaRqtJk1cqGtCKYzTzEAFZtF_L7XV1Xu57-Tm5QBwi9EcY0Yetn6OEBP1nCCCzsC0ZKTCTIpzMEWo7BRxPgFXKW0RQpwhcgkmlEouakmm4H3Zj1kPOtvYdgaa4HMMPQwOarjTucS-aq23UefOt9DYctc99KPp7Zhg5wvX7gcfcudCHKDr0tc1uHC6T_bmNGfg8_npY_FSrd6Wr4vHVWUoJbkijdOWiYY4arBgayTWDXeMcSmM1YRqyp1wUhtjJSn_4lpwKqnZSG6JY4bOwP2xdxfD92hTVkOXjO177W0YkyKMNJiKmuOCVkfUxJBStE7tYjfouFcYqYNHtfXq16M6eCz83al6XA9280__iaM_muBuXw</recordid><startdate>20210601</startdate><enddate>20210601</enddate><creator>Comas, Virginia</creator><creator>Borde, Michel</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-7227-5607</orcidid><orcidid>https://orcid.org/0000-0002-5729-8616</orcidid></search><sort><creationdate>20210601</creationdate><title>Glutamatergic control of a pattern-generating central nucleus in a gymnotiform fish</title><author>Comas, Virginia ; Borde, Michel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c332t-26fae5862f3c185b08b67f55798cea23a37f8f9acce929781487393cd97e2f5c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Biological Clocks - drug effects</topic><topic>Biological Clocks - physiology</topic><topic>Central Pattern Generators - drug effects</topic><topic>Central Pattern Generators - metabolism</topic><topic>Electric Stimulation</topic><topic>Electrophysiological Phenomena - drug effects</topic><topic>Electrophysiological Phenomena - physiology</topic><topic>Excitatory Amino Acid Agonists - pharmacology</topic><topic>Excitatory Amino Acid Antagonists - pharmacology</topic><topic>Gymnotiformes - metabolism</topic><topic>Gymnotiformes - physiology</topic><topic>Receptors, Ionotropic Glutamate - drug effects</topic><topic>Receptors, Ionotropic Glutamate - metabolism</topic><topic>Receptors, Metabotropic Glutamate - drug effects</topic><topic>Receptors, Metabotropic Glutamate - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Comas, Virginia</creatorcontrib><creatorcontrib>Borde, Michel</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Comas, Virginia</au><au>Borde, Michel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Glutamatergic control of a pattern-generating central nucleus in a gymnotiform fish</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2021-06-01</date><risdate>2021</risdate><volume>125</volume><issue>6</issue><spage>2339</spage><epage>2355</epage><pages>2339-2355</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>The activity of central pattern-generating networks (CPGs) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates, most of their synaptic and cellular bases are not yet well understood in vertebrates. , a pulse-type gymnotiform electric fish, provides a well-suited vertebrate model to investigate these mechanisms. emits rhythmic and stereotyped electric organ discharges (EODs), which function in both perception and communication, under the command of an electromotor CPG. This nucleus is composed of electrotonically coupled intrinsic pacemaker cells, which pace the rhythm, and bulbospinal projecting relay cells that contribute to organize the pattern of the muscle-derived effector activation that produce the EOD. Descending influences target CPG neurons to produce adaptive behavioral electromotor responses to different environmental challenges. We used electrophysiological and pharmacological techniques in brainstem slices of to investigate the underpinnings of the fast transmitter control of its electromotor CPG. We demonstrate that pacemaker, but not relay cells, are endowed with ionotropic and metabotropic glutamate receptor subtypes. We also show that glutamatergic control of the CPG likely involves two types of synapses contacting pacemaker cells, one type containing both α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and -methyl-d-aspartate (NMDA) receptors and the other one only-NMDA receptor. Fast neurotransmitter control of vertebrate CPGs seems to exploit the kinetics of the involved postsynaptic receptors to command different behavioral outputs. The prospect of common neural designs to control CPG activity in vertebrates is discussed. Underpinnings of neuromodulation of central pattern-generating networks (CPG) have been well characterized in many species. The effects of fast neurotransmitter systems remain, however, poorly understood. This research uses in vitro electrophysiological and pharmacological techniques to show that the neurotransmitter control of a vertebrate CPG in gymnotiform fish involves the convergence of only-NMDA and AMPA-NMDA glutamatergic synapses onto neurons that pace the rhythm. These inputs may organize different behavioral outputs according to their distinct functional properties.</abstract><cop>United States</cop><pmid>33978492</pmid><doi>10.1152/jn.00584.2020</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-7227-5607</orcidid><orcidid>https://orcid.org/0000-0002-5729-8616</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0022-3077
ispartof Journal of neurophysiology, 2021-06, Vol.125 (6), p.2339-2355
issn 0022-3077
1522-1598
language eng
recordid cdi_proquest_miscellaneous_2526138471
source MEDLINE; American Physiological Society; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection
subjects Animals
Biological Clocks - drug effects
Biological Clocks - physiology
Central Pattern Generators - drug effects
Central Pattern Generators - metabolism
Electric Stimulation
Electrophysiological Phenomena - drug effects
Electrophysiological Phenomena - physiology
Excitatory Amino Acid Agonists - pharmacology
Excitatory Amino Acid Antagonists - pharmacology
Gymnotiformes - metabolism
Gymnotiformes - physiology
Receptors, Ionotropic Glutamate - drug effects
Receptors, Ionotropic Glutamate - metabolism
Receptors, Metabotropic Glutamate - drug effects
Receptors, Metabotropic Glutamate - metabolism
title Glutamatergic control of a pattern-generating central nucleus in a gymnotiform fish
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-29T03%3A10%3A10IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Glutamatergic%20control%20of%20a%20pattern-generating%20central%20nucleus%20in%20a%20gymnotiform%20fish&rft.jtitle=Journal%20of%20neurophysiology&rft.au=Comas,%20Virginia&rft.date=2021-06-01&rft.volume=125&rft.issue=6&rft.spage=2339&rft.epage=2355&rft.pages=2339-2355&rft.issn=0022-3077&rft.eissn=1522-1598&rft_id=info:doi/10.1152/jn.00584.2020&rft_dat=%3Cproquest_cross%3E2526138471%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2526138471&rft_id=info:pmid/33978492&rfr_iscdi=true