Additional Component in the Cellular Mechanism of Presynaptic Facilitation Contributes to Behavioral Dishabituation in Aplysia
Sensitization of defensive gill and siphon withdrawal reflexes in Aplysia results, in part, from presynaptic facilitation of transmitter release from mechanoreceptor sensory neurons that innervate the siphon skin and synapse with interneurons and motor neurons. Presynaptic facilitation also can be e...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 1986-11, Vol.83 (22), p.8794-8798 |
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| container_title | Proceedings of the National Academy of Sciences - PNAS |
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| creator | Hochner, Binyamin Klein, Marc Schacher, Samuel Kandel, Eric R. |
| description | Sensitization of defensive gill and siphon withdrawal reflexes in Aplysia results, in part, from presynaptic facilitation of transmitter release from mechanoreceptor sensory neurons that innervate the siphon skin and synapse with interneurons and motor neurons. Presynaptic facilitation also can be elicited by application of serotonin. This facilitation is associated with two phenomena, a prolongation of the presynaptic action potential resulting from a decrease in a specific K+ current and an enhancement of the Ca2+ transients elicited by depolarization. Previous work has shown that prolongation of the action potential enhances synaptic transmission at normal levels of release. Here we report that an additional set of processes also contributes to facilitation. When repeated activation of the sensory neurons induces profound homosynaptic depression, prolonging the duration of action potentials (or of depolarizing commands under voltage clamp) has little effect on transmitter release. Nonetheless, serotonin is still capable of enhancing release. Since homosynaptic depression underlies the behavioral process of habituation, the second set of processes, by counteracting the consequences of the depression, seems to mediate the effects of dishabituation in the sensory neuron. Prolongation of the action potential by closure of the K+ channel seems to mediate the effects of sensitization. |
| doi_str_mv | 10.1073/pnas.83.22.8794 |
| format | Article |
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Presynaptic facilitation also can be elicited by application of serotonin. This facilitation is associated with two phenomena, a prolongation of the presynaptic action potential resulting from a decrease in a specific K+ current and an enhancement of the Ca2+ transients elicited by depolarization. Previous work has shown that prolongation of the action potential enhances synaptic transmission at normal levels of release. Here we report that an additional set of processes also contributes to facilitation. When repeated activation of the sensory neurons induces profound homosynaptic depression, prolonging the duration of action potentials (or of depolarizing commands under voltage clamp) has little effect on transmitter release. Nonetheless, serotonin is still capable of enhancing release. Since homosynaptic depression underlies the behavioral process of habituation, the second set of processes, by counteracting the consequences of the depression, seems to mediate the effects of dishabituation in the sensory neuron. Prolongation of the action potential by closure of the K+ channel seems to mediate the effects of sensitization.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.83.22.8794</identifier><identifier>PMID: 2430300</identifier><identifier>CODEN: PNASA6</identifier><language>eng</language><publisher>Washington, DC: National Academy of Sciences of the United States of America</publisher><subject>Action Potentials ; Animals ; Aplysia - physiology ; Aplysia californica ; Biological and medical sciences ; Calcium - metabolism ; Cell physiology ; Cyclic AMP - physiology ; Depressive disorders ; Fundamental and applied biological sciences. Psychology ; Ganglia ; Ganglia - physiology ; Habituation ; Habituation, Psychophysiologic ; Ion Channels - physiology ; Learning ; Molecular and cellular biology ; Neurons, Afferent - physiology ; Neurotransmission ; Neurotransmitter Agents - metabolism ; Potassium - metabolism ; Radio transmitters ; Sensitization ; Sensory neurons ; Serotonin - pharmacology ; Serotonin receptors ; Synapses ; Synapses - physiology ; Transmitters</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 1986-11, Vol.83 (22), p.8794-8798</ispartof><rights>1987 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c521t-dc128179dca0fbe1541aa5007e0e25c1c8b4f1e128c93ff5d4f8941b5d6f9e753</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/83/22.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/29141$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/29141$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=8016789$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/2430300$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hochner, Binyamin</creatorcontrib><creatorcontrib>Klein, Marc</creatorcontrib><creatorcontrib>Schacher, Samuel</creatorcontrib><creatorcontrib>Kandel, Eric R.</creatorcontrib><title>Additional Component in the Cellular Mechanism of Presynaptic Facilitation Contributes to Behavioral Dishabituation in Aplysia</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Sensitization of defensive gill and siphon withdrawal reflexes in Aplysia results, in part, from presynaptic facilitation of transmitter release from mechanoreceptor sensory neurons that innervate the siphon skin and synapse with interneurons and motor neurons. Presynaptic facilitation also can be elicited by application of serotonin. This facilitation is associated with two phenomena, a prolongation of the presynaptic action potential resulting from a decrease in a specific K+ current and an enhancement of the Ca2+ transients elicited by depolarization. Previous work has shown that prolongation of the action potential enhances synaptic transmission at normal levels of release. Here we report that an additional set of processes also contributes to facilitation. When repeated activation of the sensory neurons induces profound homosynaptic depression, prolonging the duration of action potentials (or of depolarizing commands under voltage clamp) has little effect on transmitter release. Nonetheless, serotonin is still capable of enhancing release. Since homosynaptic depression underlies the behavioral process of habituation, the second set of processes, by counteracting the consequences of the depression, seems to mediate the effects of dishabituation in the sensory neuron. Prolongation of the action potential by closure of the K+ channel seems to mediate the effects of sensitization.</description><subject>Action Potentials</subject><subject>Animals</subject><subject>Aplysia - physiology</subject><subject>Aplysia californica</subject><subject>Biological and medical sciences</subject><subject>Calcium - metabolism</subject><subject>Cell physiology</subject><subject>Cyclic AMP - physiology</subject><subject>Depressive disorders</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Ganglia</subject><subject>Ganglia - physiology</subject><subject>Habituation</subject><subject>Habituation, Psychophysiologic</subject><subject>Ion Channels - physiology</subject><subject>Learning</subject><subject>Molecular and cellular biology</subject><subject>Neurons, Afferent - physiology</subject><subject>Neurotransmission</subject><subject>Neurotransmitter Agents - metabolism</subject><subject>Potassium - metabolism</subject><subject>Radio transmitters</subject><subject>Sensitization</subject><subject>Sensory neurons</subject><subject>Serotonin - pharmacology</subject><subject>Serotonin receptors</subject><subject>Synapses</subject><subject>Synapses - physiology</subject><subject>Transmitters</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1986</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkTGP1DAQhSMEOpaDGgkJ5AJBlb1x4qztgmJZOEA6BAXUluPYxKesnbOdE9vw23G00XI0ULl433uemVcUTzGsMdD6YnQyrlm9rqo1o5zcK1YYOC43hMP9YgVQ0ZKRijwsHsV4DQC8YXBWnFWkhhpgVfzadp1N1js5oJ3fj95pl5B1KPUa7fQwTIMM6LNWvXQ27pE36GvQ8eDkmKxCl1LZwSY5J2S_S8G2U9IRJY_e6l7eWh9y8jsbe9naNB3BHL8dh0O08nHxwMgh6ifLe158v3z_bfexvPry4dNue1WqpsKp7BSuGKa8UxJMq3FDsJQNANWgq0ZhxVpisM6Q4rUxTUcM4wS3TbcxXNOmPi_eHHPHqd3rTuUl81xiDHYvw0F4acXfirO9-OFvRc0oYJb9rxZ_8DeTjknsbVT5PNJpP0VBKSaEwv9BTCjmlNIMXhxBFXyMQZvTMBjEXK2YqxWsFlUl5mqz4_ndHU780mXWXy66jEoOJkinbDxhDPCGMp6xFws255_Uu_-8_icgzDQMSf9MmXx2JK9j8uHPQBwTXP8GxDjRLw</recordid><startdate>19861101</startdate><enddate>19861101</enddate><creator>Hochner, Binyamin</creator><creator>Klein, Marc</creator><creator>Schacher, Samuel</creator><creator>Kandel, Eric R.</creator><general>National Academy of Sciences of the United States of America</general><general>National Acad Sciences</general><scope>IQODW</scope><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>7QG</scope><scope>7TK</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19861101</creationdate><title>Additional Component in the Cellular Mechanism of Presynaptic Facilitation Contributes to Behavioral Dishabituation in Aplysia</title><author>Hochner, Binyamin ; Klein, Marc ; Schacher, Samuel ; Kandel, Eric R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c521t-dc128179dca0fbe1541aa5007e0e25c1c8b4f1e128c93ff5d4f8941b5d6f9e753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1986</creationdate><topic>Action Potentials</topic><topic>Animals</topic><topic>Aplysia - physiology</topic><topic>Aplysia californica</topic><topic>Biological and medical sciences</topic><topic>Calcium - metabolism</topic><topic>Cell physiology</topic><topic>Cyclic AMP - physiology</topic><topic>Depressive disorders</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Ganglia</topic><topic>Ganglia - physiology</topic><topic>Habituation</topic><topic>Habituation, Psychophysiologic</topic><topic>Ion Channels - physiology</topic><topic>Learning</topic><topic>Molecular and cellular biology</topic><topic>Neurons, Afferent - physiology</topic><topic>Neurotransmission</topic><topic>Neurotransmitter Agents - metabolism</topic><topic>Potassium - metabolism</topic><topic>Radio transmitters</topic><topic>Sensitization</topic><topic>Sensory neurons</topic><topic>Serotonin - pharmacology</topic><topic>Serotonin receptors</topic><topic>Synapses</topic><topic>Synapses - physiology</topic><topic>Transmitters</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hochner, Binyamin</creatorcontrib><creatorcontrib>Klein, Marc</creatorcontrib><creatorcontrib>Schacher, Samuel</creatorcontrib><creatorcontrib>Kandel, Eric R.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hochner, Binyamin</au><au>Klein, Marc</au><au>Schacher, Samuel</au><au>Kandel, Eric R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Additional Component in the Cellular Mechanism of Presynaptic Facilitation Contributes to Behavioral Dishabituation in Aplysia</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>1986-11-01</date><risdate>1986</risdate><volume>83</volume><issue>22</issue><spage>8794</spage><epage>8798</epage><pages>8794-8798</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><coden>PNASA6</coden><abstract>Sensitization of defensive gill and siphon withdrawal reflexes in Aplysia results, in part, from presynaptic facilitation of transmitter release from mechanoreceptor sensory neurons that innervate the siphon skin and synapse with interneurons and motor neurons. Presynaptic facilitation also can be elicited by application of serotonin. This facilitation is associated with two phenomena, a prolongation of the presynaptic action potential resulting from a decrease in a specific K+ current and an enhancement of the Ca2+ transients elicited by depolarization. Previous work has shown that prolongation of the action potential enhances synaptic transmission at normal levels of release. Here we report that an additional set of processes also contributes to facilitation. When repeated activation of the sensory neurons induces profound homosynaptic depression, prolonging the duration of action potentials (or of depolarizing commands under voltage clamp) has little effect on transmitter release. Nonetheless, serotonin is still capable of enhancing release. Since homosynaptic depression underlies the behavioral process of habituation, the second set of processes, by counteracting the consequences of the depression, seems to mediate the effects of dishabituation in the sensory neuron. Prolongation of the action potential by closure of the K+ channel seems to mediate the effects of sensitization.</abstract><cop>Washington, DC</cop><pub>National Academy of Sciences of the United States of America</pub><pmid>2430300</pmid><doi>10.1073/pnas.83.22.8794</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
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| source | Jstor Complete Legacy; MEDLINE; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
| subjects | Action Potentials Animals Aplysia - physiology Aplysia californica Biological and medical sciences Calcium - metabolism Cell physiology Cyclic AMP - physiology Depressive disorders Fundamental and applied biological sciences. Psychology Ganglia Ganglia - physiology Habituation Habituation, Psychophysiologic Ion Channels - physiology Learning Molecular and cellular biology Neurons, Afferent - physiology Neurotransmission Neurotransmitter Agents - metabolism Potassium - metabolism Radio transmitters Sensitization Sensory neurons Serotonin - pharmacology Serotonin receptors Synapses Synapses - physiology Transmitters |
| title | Additional Component in the Cellular Mechanism of Presynaptic Facilitation Contributes to Behavioral Dishabituation in Aplysia |
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