TRPM4 Conductances in Thalamic Reticular Nucleus Neurons Generate Persistent Firing during Slow Oscillations
During sleep, neurons in the thalamic reticular nucleus (TRN) participate in distinct types of oscillatory activity. While the reciprocal synaptic circuits between TRN and sensory relay nuclei are known to underlie the generation of sleep spindles, the mechanisms regulating slow (
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| description | During sleep, neurons in the thalamic reticular nucleus (TRN) participate in distinct types of oscillatory activity. While the reciprocal synaptic circuits between TRN and sensory relay nuclei are known to underlie the generation of sleep spindles, the mechanisms regulating slow ( |
| doi_str_mv | 10.1523/JNEUROSCI.0324-20.2020 |
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conditions, TRN neurons can generate slow oscillations in a cell-intrinsic manner, with postsynaptic Group 1 metabotropic glutamate receptor activation triggering long-lasting plateau potentials thought to be mediated by both T-type Ca
currents and Ca
-activated nonselective cation currents (I
). However, the identity of I
and the possible contribution of thalamic circuits to slow rhythmic activity remain unclear. Using thalamic slices derived from adult mice of either sex, we recorded slow forms of rhythmic activity in TRN neurons, which were driven by fast glutamatergic thalamoreticular inputs but did not require postsynaptic Group 1 metabotropic glutamate receptor activation. For a significant fraction of TRN neurons, synaptic inputs or brief depolarizing current steps led to long-lasting plateau potentials and persistent firing (PF), and in turn, resulted in sustained synaptic inhibition in postsynaptic relay neurons of the ventrobasal thalamus (VB). Pharmacological approachesindicated that plateau potentials were triggered by Ca
influx through T-type Ca
channels and mediated by Ca
- and voltage-dependent transient receptor potential melastatin 4 (TRPM4) channels. Together, our results suggest that thalamic circuits can generate slow oscillatory activity, mediated by an interplay of TRN-VB synaptic circuits that generate rhythmicity and TRN cell-intrinsic mechanisms that control PF and oscillation frequency.
Slow forms of thalamocortical rhythmic activity are thought to be essential for memory consolidation during sleep and the efficient removal of potentially toxic metabolites.
, thalamic slow oscillations are regulated by strong bidirectional synaptic pathways linking neocortex and thalamus. Therefore,
studies in the isolated thalamus offer important insights about the ability of individual neurons and local circuits to generate different forms of rhythmic activity. We found that circuits formed by GABAergic neurons in the thalamic reticular nucleus and glutamatergic relay neurons in the ventrobasal thalamus generated slow oscillatory activity, which was accompanied by persistent firing in thalamic reticular nucleus neurons. Our results identify both cell-intrinsic and synaptic mechanisms that mediate slow forms of rhythmic activity in thalamic circuits.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.0324-20.2020</identifier><identifier>PMID: 32414784</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Action Potentials - physiology ; Activation ; Activity patterns ; Animals ; Calcium channels ; Calcium channels (T-type) ; Calcium channels (voltage-gated) ; Calcium influx ; Calcium ions ; Channels ; Circuits ; Depolarization ; Female ; GABAergic Neurons - physiology ; Glutamatergic transmission ; Glutamic acid receptors ; Glutamic acid receptors (metabotropic) ; Intralaminar Thalamic Nuclei - physiology ; Ion currents ; Male ; Mice ; Mice, Inbred C57BL ; Neural Pathways - physiology ; Neurogenesis ; Neurons ; Organ Culture Techniques ; Oscillations ; Receptor mechanisms ; Receptors ; Rhythms ; Sleep ; Sleep - physiology ; Thalamic reticular nucleus ; Thalamus ; Transient receptor potential proteins ; TRPM Cation Channels - metabolism</subject><ispartof>The Journal of neuroscience, 2020-06, Vol.40 (25), p.4813-4823</ispartof><rights>Copyright © 2020 the authors.</rights><rights>Copyright Society for Neuroscience Jun 17, 2020</rights><rights>Copyright © 2020 the authors 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-30b14cf51fe829bc22cd91da2035d842e8b0b99dfd2ed2fa2de5b304394b8b9f3</citedby><orcidid>0000-0003-0536-5212 ; 0000-0001-9902-3744 ; 0000-0003-2210-3118 ; 0000-0003-3774-1702</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7326353/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7326353/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32414784$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>O'Malley, John J</creatorcontrib><creatorcontrib>Seibt, Frederik</creatorcontrib><creatorcontrib>Chin, Jeannie</creatorcontrib><creatorcontrib>Beierlein, Michael</creatorcontrib><title>TRPM4 Conductances in Thalamic Reticular Nucleus Neurons Generate Persistent Firing during Slow Oscillations</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>During sleep, neurons in the thalamic reticular nucleus (TRN) participate in distinct types of oscillatory activity. While the reciprocal synaptic circuits between TRN and sensory relay nuclei are known to underlie the generation of sleep spindles, the mechanisms regulating slow (<1 Hz) forms of thalamic oscillations are not well understood. Under
conditions, TRN neurons can generate slow oscillations in a cell-intrinsic manner, with postsynaptic Group 1 metabotropic glutamate receptor activation triggering long-lasting plateau potentials thought to be mediated by both T-type Ca
currents and Ca
-activated nonselective cation currents (I
). However, the identity of I
and the possible contribution of thalamic circuits to slow rhythmic activity remain unclear. Using thalamic slices derived from adult mice of either sex, we recorded slow forms of rhythmic activity in TRN neurons, which were driven by fast glutamatergic thalamoreticular inputs but did not require postsynaptic Group 1 metabotropic glutamate receptor activation. For a significant fraction of TRN neurons, synaptic inputs or brief depolarizing current steps led to long-lasting plateau potentials and persistent firing (PF), and in turn, resulted in sustained synaptic inhibition in postsynaptic relay neurons of the ventrobasal thalamus (VB). Pharmacological approachesindicated that plateau potentials were triggered by Ca
influx through T-type Ca
channels and mediated by Ca
- and voltage-dependent transient receptor potential melastatin 4 (TRPM4) channels. Together, our results suggest that thalamic circuits can generate slow oscillatory activity, mediated by an interplay of TRN-VB synaptic circuits that generate rhythmicity and TRN cell-intrinsic mechanisms that control PF and oscillation frequency.
Slow forms of thalamocortical rhythmic activity are thought to be essential for memory consolidation during sleep and the efficient removal of potentially toxic metabolites.
, thalamic slow oscillations are regulated by strong bidirectional synaptic pathways linking neocortex and thalamus. Therefore,
studies in the isolated thalamus offer important insights about the ability of individual neurons and local circuits to generate different forms of rhythmic activity. We found that circuits formed by GABAergic neurons in the thalamic reticular nucleus and glutamatergic relay neurons in the ventrobasal thalamus generated slow oscillatory activity, which was accompanied by persistent firing in thalamic reticular nucleus neurons. Our results identify both cell-intrinsic and synaptic mechanisms that mediate slow forms of rhythmic activity in thalamic circuits.</description><subject>Action Potentials - physiology</subject><subject>Activation</subject><subject>Activity patterns</subject><subject>Animals</subject><subject>Calcium channels</subject><subject>Calcium channels (T-type)</subject><subject>Calcium channels (voltage-gated)</subject><subject>Calcium influx</subject><subject>Calcium ions</subject><subject>Channels</subject><subject>Circuits</subject><subject>Depolarization</subject><subject>Female</subject><subject>GABAergic Neurons - physiology</subject><subject>Glutamatergic transmission</subject><subject>Glutamic acid receptors</subject><subject>Glutamic acid receptors (metabotropic)</subject><subject>Intralaminar Thalamic Nuclei - physiology</subject><subject>Ion currents</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Neural Pathways - physiology</subject><subject>Neurogenesis</subject><subject>Neurons</subject><subject>Organ Culture Techniques</subject><subject>Oscillations</subject><subject>Receptor mechanisms</subject><subject>Receptors</subject><subject>Rhythms</subject><subject>Sleep</subject><subject>Sleep - physiology</subject><subject>Thalamic reticular nucleus</subject><subject>Thalamus</subject><subject>Transient receptor potential proteins</subject><subject>TRPM Cation Channels - metabolism</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUFvEzEQhS0EoqHwFypLnDeMx97s7gUJRW0papMqTc-W1_a2rhxvsddF_HscWqJymsPMe_P0PkJOGMxZjfzLj9Xp7WZ9s7yYA0dRIcwREN6QWdl2FQpgb8kMsIFqIRpxRD6k9AAADbDmPTkqEiaaVsyI326urwRdjsFkPamgbaIu0O298mrnNN3YyensVaSrrL3Nia5sjmNI9NwGG9Vk6bWNyaXJhomeuejCHTX577jx4y-6Ttp5ryZXNB_Ju0H5ZD-9zGNye3a6XX6vLtfnF8tvl5UWAqeKQ8-EHmo22Ba7XiNq0zGjEHhtWoG27aHvOjMYtAYHhcbWPQfBO9G3fTfwY_L12fcx9ztrdIkWlZeP0e1U_C1H5eT_m-Du5d34JBuOC17zYvD5xSCOP7NNk3wYcwwlsyzN1aLpSo_lavF8peOYUrTD4QMDuackD5TknpJEkHtKRXjyOt9B9g8L_wNaoJGM</recordid><startdate>20200617</startdate><enddate>20200617</enddate><creator>O'Malley, John J</creator><creator>Seibt, Frederik</creator><creator>Chin, Jeannie</creator><creator>Beierlein, Michael</creator><general>Society for Neuroscience</general><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>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0536-5212</orcidid><orcidid>https://orcid.org/0000-0001-9902-3744</orcidid><orcidid>https://orcid.org/0000-0003-2210-3118</orcidid><orcidid>https://orcid.org/0000-0003-3774-1702</orcidid></search><sort><creationdate>20200617</creationdate><title>TRPM4 Conductances in Thalamic Reticular Nucleus Neurons Generate Persistent Firing during Slow Oscillations</title><author>O'Malley, John J ; Seibt, Frederik ; Chin, Jeannie ; Beierlein, Michael</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-30b14cf51fe829bc22cd91da2035d842e8b0b99dfd2ed2fa2de5b304394b8b9f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Action Potentials - physiology</topic><topic>Activation</topic><topic>Activity patterns</topic><topic>Animals</topic><topic>Calcium channels</topic><topic>Calcium channels (T-type)</topic><topic>Calcium channels (voltage-gated)</topic><topic>Calcium influx</topic><topic>Calcium ions</topic><topic>Channels</topic><topic>Circuits</topic><topic>Depolarization</topic><topic>Female</topic><topic>GABAergic Neurons - physiology</topic><topic>Glutamatergic transmission</topic><topic>Glutamic acid receptors</topic><topic>Glutamic acid receptors (metabotropic)</topic><topic>Intralaminar Thalamic Nuclei - physiology</topic><topic>Ion currents</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Neural Pathways - physiology</topic><topic>Neurogenesis</topic><topic>Neurons</topic><topic>Organ Culture Techniques</topic><topic>Oscillations</topic><topic>Receptor mechanisms</topic><topic>Receptors</topic><topic>Rhythms</topic><topic>Sleep</topic><topic>Sleep - physiology</topic><topic>Thalamic reticular nucleus</topic><topic>Thalamus</topic><topic>Transient receptor potential proteins</topic><topic>TRPM Cation Channels - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>O'Malley, John J</creatorcontrib><creatorcontrib>Seibt, Frederik</creatorcontrib><creatorcontrib>Chin, Jeannie</creatorcontrib><creatorcontrib>Beierlein, Michael</creatorcontrib><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>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>O'Malley, John J</au><au>Seibt, Frederik</au><au>Chin, Jeannie</au><au>Beierlein, Michael</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>TRPM4 Conductances in Thalamic Reticular Nucleus Neurons Generate Persistent Firing during Slow Oscillations</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2020-06-17</date><risdate>2020</risdate><volume>40</volume><issue>25</issue><spage>4813</spage><epage>4823</epage><pages>4813-4823</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>During sleep, neurons in the thalamic reticular nucleus (TRN) participate in distinct types of oscillatory activity. While the reciprocal synaptic circuits between TRN and sensory relay nuclei are known to underlie the generation of sleep spindles, the mechanisms regulating slow (<1 Hz) forms of thalamic oscillations are not well understood. Under
conditions, TRN neurons can generate slow oscillations in a cell-intrinsic manner, with postsynaptic Group 1 metabotropic glutamate receptor activation triggering long-lasting plateau potentials thought to be mediated by both T-type Ca
currents and Ca
-activated nonselective cation currents (I
). However, the identity of I
and the possible contribution of thalamic circuits to slow rhythmic activity remain unclear. Using thalamic slices derived from adult mice of either sex, we recorded slow forms of rhythmic activity in TRN neurons, which were driven by fast glutamatergic thalamoreticular inputs but did not require postsynaptic Group 1 metabotropic glutamate receptor activation. For a significant fraction of TRN neurons, synaptic inputs or brief depolarizing current steps led to long-lasting plateau potentials and persistent firing (PF), and in turn, resulted in sustained synaptic inhibition in postsynaptic relay neurons of the ventrobasal thalamus (VB). Pharmacological approachesindicated that plateau potentials were triggered by Ca
influx through T-type Ca
channels and mediated by Ca
- and voltage-dependent transient receptor potential melastatin 4 (TRPM4) channels. Together, our results suggest that thalamic circuits can generate slow oscillatory activity, mediated by an interplay of TRN-VB synaptic circuits that generate rhythmicity and TRN cell-intrinsic mechanisms that control PF and oscillation frequency.
Slow forms of thalamocortical rhythmic activity are thought to be essential for memory consolidation during sleep and the efficient removal of potentially toxic metabolites.
, thalamic slow oscillations are regulated by strong bidirectional synaptic pathways linking neocortex and thalamus. Therefore,
studies in the isolated thalamus offer important insights about the ability of individual neurons and local circuits to generate different forms of rhythmic activity. We found that circuits formed by GABAergic neurons in the thalamic reticular nucleus and glutamatergic relay neurons in the ventrobasal thalamus generated slow oscillatory activity, which was accompanied by persistent firing in thalamic reticular nucleus neurons. Our results identify both cell-intrinsic and synaptic mechanisms that mediate slow forms of rhythmic activity in thalamic circuits.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>32414784</pmid><doi>10.1523/JNEUROSCI.0324-20.2020</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-0536-5212</orcidid><orcidid>https://orcid.org/0000-0001-9902-3744</orcidid><orcidid>https://orcid.org/0000-0003-2210-3118</orcidid><orcidid>https://orcid.org/0000-0003-3774-1702</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Action Potentials - physiology Activation Activity patterns Animals Calcium channels Calcium channels (T-type) Calcium channels (voltage-gated) Calcium influx Calcium ions Channels Circuits Depolarization Female GABAergic Neurons - physiology Glutamatergic transmission Glutamic acid receptors Glutamic acid receptors (metabotropic) Intralaminar Thalamic Nuclei - physiology Ion currents Male Mice Mice, Inbred C57BL Neural Pathways - physiology Neurogenesis Neurons Organ Culture Techniques Oscillations Receptor mechanisms Receptors Rhythms Sleep Sleep - physiology Thalamic reticular nucleus Thalamus Transient receptor potential proteins TRPM Cation Channels - metabolism |
| title | TRPM4 Conductances in Thalamic Reticular Nucleus Neurons Generate Persistent Firing during Slow Oscillations |
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