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,...
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Veröffentlicht in: | Journal of neurophysiology 2021-06, Vol.125 (6), p.2339-2355 |
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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 |
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, 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> |
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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 |
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