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Morphological and electrophysiological characteristics of neurons within identified subnuclei of the lateral habenula in rat brain slices
Abstract Based on the specificity of its inputs and targets, the lateral habenular complex (LHb) constitutes a pivotal motor-limbic interface implicated in various cerebral functions particularly in regulating monoamine transmission. Despite its functional significance, cellular characteristics unde...
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Published in: | Neuroscience 2011-01, Vol.172 (1), p.74-93 |
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description | Abstract Based on the specificity of its inputs and targets, the lateral habenular complex (LHb) constitutes a pivotal motor-limbic interface implicated in various cerebral functions particularly in regulating monoamine transmission. Despite its functional significance, cellular characteristics underlying LHb functionality have not been examined systematically. The present study aimed to correlate morphological and electrophysiological properties of neurons within the different subnuclei of the LHb using whole-cell recording and neurobiotin labeling in rat slice preparations. Morphological analysis revealed a heterogeneous population of projection neurons randomly distributed throughout the LHb. According to somatodendritic characteristics four main categories were classified including spherical, fusiform, polymorphic and vertical cells. Electrophysiological characterization of neurons within the different categories demonstrated homologous profiles and no significant differences between groups. Typically, LHb neurons possessed high input resistances and long membrane time constants. They also displayed time-dependent inward rectification and distinct afterhyperpolarization. A salient electrophysiological feature of LHb neurons was their ability to generate rebound bursts of action potentials in response to membrane hyperpolarization. Based on the pattern of spontaneous activity, neurons were classified as silent, tonic or bursting. The occurrence of distinctive firing modes was not related to topographic allocation. The patterns of spontaneous firing and evoked discharge were highly sensitive to alterations in membrane potential and merged upon de- and hyperpolarizing current injection and synaptic stimulation. Besides projection neurons, recordings revealed the existence of a subpopulation of cells possessing morphological and physiological properties of neocortical neurogliaform cells. They were considered to be interneurons. Our data suggest that neurons within the different LHb subnuclei behave electrophysiologically more similar than expected, considering their morphological heterogeneity. We conclude that the formation of functional neuronal entities within the LHb may be achieved through defined synaptic inputs to particular neurons, rather than by individual neuronal morphologies and intrinsic membrane properties. |
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Despite its functional significance, cellular characteristics underlying LHb functionality have not been examined systematically. The present study aimed to correlate morphological and electrophysiological properties of neurons within the different subnuclei of the LHb using whole-cell recording and neurobiotin labeling in rat slice preparations. Morphological analysis revealed a heterogeneous population of projection neurons randomly distributed throughout the LHb. According to somatodendritic characteristics four main categories were classified including spherical, fusiform, polymorphic and vertical cells. Electrophysiological characterization of neurons within the different categories demonstrated homologous profiles and no significant differences between groups. Typically, LHb neurons possessed high input resistances and long membrane time constants. They also displayed time-dependent inward rectification and distinct afterhyperpolarization. A salient electrophysiological feature of LHb neurons was their ability to generate rebound bursts of action potentials in response to membrane hyperpolarization. Based on the pattern of spontaneous activity, neurons were classified as silent, tonic or bursting. The occurrence of distinctive firing modes was not related to topographic allocation. The patterns of spontaneous firing and evoked discharge were highly sensitive to alterations in membrane potential and merged upon de- and hyperpolarizing current injection and synaptic stimulation. Besides projection neurons, recordings revealed the existence of a subpopulation of cells possessing morphological and physiological properties of neocortical neurogliaform cells. They were considered to be interneurons. Our data suggest that neurons within the different LHb subnuclei behave electrophysiologically more similar than expected, considering their morphological heterogeneity. We conclude that the formation of functional neuronal entities within the LHb may be achieved through defined synaptic inputs to particular neurons, rather than by individual neuronal morphologies and intrinsic membrane properties.</description><identifier>ISSN: 0306-4522</identifier><identifier>EISSN: 1873-7544</identifier><identifier>DOI: 10.1016/j.neuroscience.2010.10.047</identifier><identifier>PMID: 20974229</identifier><identifier>CODEN: NRSCDN</identifier><language>eng</language><publisher>Amsterdam: Elsevier Ltd</publisher><subject>Action Potentials - physiology ; Animals ; basal ganglia ; Biological and medical sciences ; Biotin - analogs & derivatives ; Biotin - metabolism ; Cell Polarity - physiology ; Dendrites - physiology ; Fundamental and applied biological sciences. Psychology ; Habenula - cytology ; Habenula - physiology ; habenular subnuclei ; Interneurons - cytology ; Interneurons - physiology ; Membrane Potentials - physiology ; Neural Pathways - cytology ; Neural Pathways - physiology ; neurobiotin ; neurogliaform cell ; Neurology ; Neurons - classification ; Neurons - cytology ; Neurons - physiology ; Organ Culture Techniques ; Rats ; Rats, Wistar ; reward ; Synaptic Transmission - physiology ; Vertebrates: nervous system and sense organs ; whole-cell recording</subject><ispartof>Neuroscience, 2011-01, Vol.172 (1), p.74-93</ispartof><rights>IBRO</rights><rights>2011 IBRO</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2011 IBRO. Published by Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c562t-2d204a70cf6796ba4dacf6cac678fd43044ab588fd5438514a0ad7bdd3c2eec33</citedby><cites>FETCH-LOGICAL-c562t-2d204a70cf6796ba4dacf6cac678fd43044ab588fd5438514a0ad7bdd3c2eec33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23764380$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20974229$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Weiss, T</creatorcontrib><creatorcontrib>Veh, R.W</creatorcontrib><title>Morphological and electrophysiological characteristics of neurons within identified subnuclei of the lateral habenula in rat brain slices</title><title>Neuroscience</title><addtitle>Neuroscience</addtitle><description>Abstract Based on the specificity of its inputs and targets, the lateral habenular complex (LHb) constitutes a pivotal motor-limbic interface implicated in various cerebral functions particularly in regulating monoamine transmission. Despite its functional significance, cellular characteristics underlying LHb functionality have not been examined systematically. The present study aimed to correlate morphological and electrophysiological properties of neurons within the different subnuclei of the LHb using whole-cell recording and neurobiotin labeling in rat slice preparations. Morphological analysis revealed a heterogeneous population of projection neurons randomly distributed throughout the LHb. According to somatodendritic characteristics four main categories were classified including spherical, fusiform, polymorphic and vertical cells. Electrophysiological characterization of neurons within the different categories demonstrated homologous profiles and no significant differences between groups. Typically, LHb neurons possessed high input resistances and long membrane time constants. They also displayed time-dependent inward rectification and distinct afterhyperpolarization. A salient electrophysiological feature of LHb neurons was their ability to generate rebound bursts of action potentials in response to membrane hyperpolarization. Based on the pattern of spontaneous activity, neurons were classified as silent, tonic or bursting. The occurrence of distinctive firing modes was not related to topographic allocation. The patterns of spontaneous firing and evoked discharge were highly sensitive to alterations in membrane potential and merged upon de- and hyperpolarizing current injection and synaptic stimulation. Besides projection neurons, recordings revealed the existence of a subpopulation of cells possessing morphological and physiological properties of neocortical neurogliaform cells. They were considered to be interneurons. Our data suggest that neurons within the different LHb subnuclei behave electrophysiologically more similar than expected, considering their morphological heterogeneity. We conclude that the formation of functional neuronal entities within the LHb may be achieved through defined synaptic inputs to particular neurons, rather than by individual neuronal morphologies and intrinsic membrane properties.</description><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>basal ganglia</subject><subject>Biological and medical sciences</subject><subject>Biotin - analogs & derivatives</subject><subject>Biotin - metabolism</subject><subject>Cell Polarity - physiology</subject><subject>Dendrites - physiology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Habenula - cytology</subject><subject>Habenula - physiology</subject><subject>habenular subnuclei</subject><subject>Interneurons - cytology</subject><subject>Interneurons - physiology</subject><subject>Membrane Potentials - physiology</subject><subject>Neural Pathways - cytology</subject><subject>Neural Pathways - physiology</subject><subject>neurobiotin</subject><subject>neurogliaform cell</subject><subject>Neurology</subject><subject>Neurons - classification</subject><subject>Neurons - cytology</subject><subject>Neurons - physiology</subject><subject>Organ Culture Techniques</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>reward</subject><subject>Synaptic Transmission - physiology</subject><subject>Vertebrates: nervous system and sense organs</subject><subject>whole-cell recording</subject><issn>0306-4522</issn><issn>1873-7544</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqNkkuP0zAQgC0EYsvCX0AREuKU4lfilAPSanlKizgAZ2tiT4iLaxc7AfUn8K9xtmVBXMAXjzTfjB_fEPKI0TWjrH26XQecU8zGYTC45vQ6saZS3SIr1ilRq0bK22RFBW1r2XB-Ru7lvKVlNVLcJWecbpTkfLMiP97FtB-jj5-dAV9BsBV6NFOK-_GQ3U3CjJDATJhcnpzJVRyq60uEXH130-hC5SyGyQ0ObZXnPszGo1uwacTKQ6ksXUboMcweqsInmKo-QYmydwbzfXJnAJ_xwWk_J59evfx4-aa-ev_67eXFVW2alk81t5xKUNQMrdq0PUgLJTRgWtUNVgoqJfRNV-Ly1K5hEihY1VsrDEc0QpyTJ8e--xS_zpgnvXPZoPcQMM5Zdy0VnWKt-jfJmew6JZtCPjuSpmjJCQe9T24H6aAZ1YszvdV_OtOLsyVXnJXih6dj5n6H9qb0l6QCPD4BkIuLIUEwLv_mhGrLU2nhXhw5LN_3zWHSp-OsS0WpttH9332e_9XGeBeWKfiCB8zbOKdQBGmmM9dUf1imbBkyRimTlHfiJyYR1PA</recordid><startdate>20110113</startdate><enddate>20110113</enddate><creator>Weiss, T</creator><creator>Veh, R.W</creator><general>Elsevier Ltd</general><general>Elsevier</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>7X8</scope><scope>7TK</scope></search><sort><creationdate>20110113</creationdate><title>Morphological and electrophysiological characteristics of neurons within identified subnuclei of the lateral habenula in rat brain slices</title><author>Weiss, T ; Veh, R.W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c562t-2d204a70cf6796ba4dacf6cac678fd43044ab588fd5438514a0ad7bdd3c2eec33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>basal ganglia</topic><topic>Biological and medical sciences</topic><topic>Biotin - analogs & derivatives</topic><topic>Biotin - metabolism</topic><topic>Cell Polarity - physiology</topic><topic>Dendrites - physiology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Habenula - cytology</topic><topic>Habenula - physiology</topic><topic>habenular subnuclei</topic><topic>Interneurons - cytology</topic><topic>Interneurons - physiology</topic><topic>Membrane Potentials - physiology</topic><topic>Neural Pathways - cytology</topic><topic>Neural Pathways - physiology</topic><topic>neurobiotin</topic><topic>neurogliaform cell</topic><topic>Neurology</topic><topic>Neurons - classification</topic><topic>Neurons - cytology</topic><topic>Neurons - physiology</topic><topic>Organ Culture Techniques</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>reward</topic><topic>Synaptic Transmission - physiology</topic><topic>Vertebrates: nervous system and sense organs</topic><topic>whole-cell recording</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Weiss, T</creatorcontrib><creatorcontrib>Veh, R.W</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>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><jtitle>Neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Weiss, T</au><au>Veh, R.W</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Morphological and electrophysiological characteristics of neurons within identified subnuclei of the lateral habenula in rat brain slices</atitle><jtitle>Neuroscience</jtitle><addtitle>Neuroscience</addtitle><date>2011-01-13</date><risdate>2011</risdate><volume>172</volume><issue>1</issue><spage>74</spage><epage>93</epage><pages>74-93</pages><issn>0306-4522</issn><eissn>1873-7544</eissn><coden>NRSCDN</coden><abstract>Abstract Based on the specificity of its inputs and targets, the lateral habenular complex (LHb) constitutes a pivotal motor-limbic interface implicated in various cerebral functions particularly in regulating monoamine transmission. Despite its functional significance, cellular characteristics underlying LHb functionality have not been examined systematically. The present study aimed to correlate morphological and electrophysiological properties of neurons within the different subnuclei of the LHb using whole-cell recording and neurobiotin labeling in rat slice preparations. Morphological analysis revealed a heterogeneous population of projection neurons randomly distributed throughout the LHb. According to somatodendritic characteristics four main categories were classified including spherical, fusiform, polymorphic and vertical cells. Electrophysiological characterization of neurons within the different categories demonstrated homologous profiles and no significant differences between groups. Typically, LHb neurons possessed high input resistances and long membrane time constants. They also displayed time-dependent inward rectification and distinct afterhyperpolarization. A salient electrophysiological feature of LHb neurons was their ability to generate rebound bursts of action potentials in response to membrane hyperpolarization. Based on the pattern of spontaneous activity, neurons were classified as silent, tonic or bursting. The occurrence of distinctive firing modes was not related to topographic allocation. The patterns of spontaneous firing and evoked discharge were highly sensitive to alterations in membrane potential and merged upon de- and hyperpolarizing current injection and synaptic stimulation. Besides projection neurons, recordings revealed the existence of a subpopulation of cells possessing morphological and physiological properties of neocortical neurogliaform cells. They were considered to be interneurons. Our data suggest that neurons within the different LHb subnuclei behave electrophysiologically more similar than expected, considering their morphological heterogeneity. We conclude that the formation of functional neuronal entities within the LHb may be achieved through defined synaptic inputs to particular neurons, rather than by individual neuronal morphologies and intrinsic membrane properties.</abstract><cop>Amsterdam</cop><pub>Elsevier Ltd</pub><pmid>20974229</pmid><doi>10.1016/j.neuroscience.2010.10.047</doi><tpages>20</tpages></addata></record> |
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subjects | Action Potentials - physiology Animals basal ganglia Biological and medical sciences Biotin - analogs & derivatives Biotin - metabolism Cell Polarity - physiology Dendrites - physiology Fundamental and applied biological sciences. Psychology Habenula - cytology Habenula - physiology habenular subnuclei Interneurons - cytology Interneurons - physiology Membrane Potentials - physiology Neural Pathways - cytology Neural Pathways - physiology neurobiotin neurogliaform cell Neurology Neurons - classification Neurons - cytology Neurons - physiology Organ Culture Techniques Rats Rats, Wistar reward Synaptic Transmission - physiology Vertebrates: nervous system and sense organs whole-cell recording |
title | Morphological and electrophysiological characteristics of neurons within identified subnuclei of the lateral habenula in rat brain slices |
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