A subcortical inhibitory signal for behavioral arrest in the thalamus
The authors show that inhibitory neurons of the pontine reticular formation (PRF) exert powerful control over the intralaminar thalamic nuclei, a major gate of forebrain motor centers. Optogenetic activation of inhibitory PRF terminals antagonizes voluntary movements and promotes slow cortical oscil...
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| Veröffentlicht in: | Nature neuroscience 2015-04, Vol.18 (4), p.562-568 |
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| creator | Giber, Kristóf Diana, Marco A M Plattner, Viktor Dugué, Guillaume P Bokor, Hajnalka Rousseau, Charly V Maglóczky, Zsófia Havas, László Hangya, Balázs Wildner, Hendrik Zeilhofer, Hanns Ulrich Dieudonné, Stéphane Acsády, László |
| description | The authors show that inhibitory neurons of the pontine reticular formation (PRF) exert powerful control over the intralaminar thalamic nuclei, a major gate of forebrain motor centers. Optogenetic activation of inhibitory PRF terminals antagonizes voluntary movements and promotes slow cortical oscillations, highlighting the contribution of brainstem ascending projections to large-scale motor circuits.
Organization of behavior requires rapid coordination of brainstem and forebrain activity. The exact mechanisms of effective communication between these regions are presently unclear. The intralaminar thalamic nuclei (IL) probably serves as a central hub in this circuit by connecting the critical brainstem and forebrain areas. We found that GABAergic and glycinergic fibers ascending from the pontine reticular formation (PRF) of the brainstem evoked fast and reliable inhibition in the IL via large, multisynaptic terminals. This inhibition was fine-tuned through heterogeneous GABAergic and glycinergic receptor ratios expressed at individual synapses. Optogenetic activation of PRF axons in the IL of freely moving mice led to behavioral arrest and transient interruption of awake cortical activity. An afferent system with comparable morphological features was also found in the human IL. These data reveal an evolutionarily conserved ascending system that gates forebrain activity through fast and powerful synaptic inhibition of the IL. |
| doi_str_mv | 10.1038/nn.3951 |
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Organization of behavior requires rapid coordination of brainstem and forebrain activity. The exact mechanisms of effective communication between these regions are presently unclear. The intralaminar thalamic nuclei (IL) probably serves as a central hub in this circuit by connecting the critical brainstem and forebrain areas. We found that GABAergic and glycinergic fibers ascending from the pontine reticular formation (PRF) of the brainstem evoked fast and reliable inhibition in the IL via large, multisynaptic terminals. This inhibition was fine-tuned through heterogeneous GABAergic and glycinergic receptor ratios expressed at individual synapses. Optogenetic activation of PRF axons in the IL of freely moving mice led to behavioral arrest and transient interruption of awake cortical activity. An afferent system with comparable morphological features was also found in the human IL. These data reveal an evolutionarily conserved ascending system that gates forebrain activity through fast and powerful synaptic inhibition of the IL.</description><identifier>ISSN: 1097-6256</identifier><identifier>EISSN: 1546-1726</identifier><identifier>DOI: 10.1038/nn.3951</identifier><identifier>PMID: 25706472</identifier><identifier>CODEN: NANEFN</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>13/1 ; 13/44 ; 13/51 ; 14 ; 14/19 ; 14/28 ; 14/34 ; 631/378/2632 ; 631/378/3920 ; 64/60 ; 82 ; 9/26 ; 9/30 ; 9/74 ; Afferent Pathways - physiology ; Animal Genetics and Genomics ; Animals ; Behavior ; Behavior, Animal - physiology ; Behavioral Sciences ; Biological Techniques ; Biomedicine ; GABAergic Neurons - physiology ; Glycine - metabolism ; Intralaminar Thalamic Nuclei - physiology ; Life Sciences ; Male ; Medical examination ; Mice ; Morphology ; Nerve Fibers - physiology ; Neural Inhibition - physiology ; Neural transmission ; Neurobiology ; Neurons and Cognition ; Neurosciences ; Optogenetics ; Patch-Clamp Techniques ; Physiological aspects ; Pontine Tegmentum - physiology ; Receptors, GABA - metabolism ; Receptors, Glycine - metabolism ; Thalamus</subject><ispartof>Nature neuroscience, 2015-04, Vol.18 (4), p.562-568</ispartof><rights>Springer Nature America, Inc. 2015</rights><rights>COPYRIGHT 2015 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Apr 2015</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c598t-e7db772ebece71e469b4d249d2d369af3e8ed44d9508a74fcf62de0e344ad5ff3</citedby><cites>FETCH-LOGICAL-c598t-e7db772ebece71e469b4d249d2d369af3e8ed44d9508a74fcf62de0e344ad5ff3</cites><orcidid>0000-0002-4106-6132 ; 0000-0002-8928-0154</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nn.3951$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nn.3951$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25706472$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01542374$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Giber, Kristóf</creatorcontrib><creatorcontrib>Diana, Marco A</creatorcontrib><creatorcontrib>M Plattner, Viktor</creatorcontrib><creatorcontrib>Dugué, Guillaume P</creatorcontrib><creatorcontrib>Bokor, Hajnalka</creatorcontrib><creatorcontrib>Rousseau, Charly V</creatorcontrib><creatorcontrib>Maglóczky, Zsófia</creatorcontrib><creatorcontrib>Havas, László</creatorcontrib><creatorcontrib>Hangya, Balázs</creatorcontrib><creatorcontrib>Wildner, Hendrik</creatorcontrib><creatorcontrib>Zeilhofer, Hanns Ulrich</creatorcontrib><creatorcontrib>Dieudonné, Stéphane</creatorcontrib><creatorcontrib>Acsády, László</creatorcontrib><title>A subcortical inhibitory signal for behavioral arrest in the thalamus</title><title>Nature neuroscience</title><addtitle>Nat Neurosci</addtitle><addtitle>Nat Neurosci</addtitle><description>The authors show that inhibitory neurons of the pontine reticular formation (PRF) exert powerful control over the intralaminar thalamic nuclei, a major gate of forebrain motor centers. Optogenetic activation of inhibitory PRF terminals antagonizes voluntary movements and promotes slow cortical oscillations, highlighting the contribution of brainstem ascending projections to large-scale motor circuits.
Organization of behavior requires rapid coordination of brainstem and forebrain activity. The exact mechanisms of effective communication between these regions are presently unclear. The intralaminar thalamic nuclei (IL) probably serves as a central hub in this circuit by connecting the critical brainstem and forebrain areas. We found that GABAergic and glycinergic fibers ascending from the pontine reticular formation (PRF) of the brainstem evoked fast and reliable inhibition in the IL via large, multisynaptic terminals. This inhibition was fine-tuned through heterogeneous GABAergic and glycinergic receptor ratios expressed at individual synapses. Optogenetic activation of PRF axons in the IL of freely moving mice led to behavioral arrest and transient interruption of awake cortical activity. An afferent system with comparable morphological features was also found in the human IL. 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inhibitory neurons of the pontine reticular formation (PRF) exert powerful control over the intralaminar thalamic nuclei, a major gate of forebrain motor centers. Optogenetic activation of inhibitory PRF terminals antagonizes voluntary movements and promotes slow cortical oscillations, highlighting the contribution of brainstem ascending projections to large-scale motor circuits.
Organization of behavior requires rapid coordination of brainstem and forebrain activity. The exact mechanisms of effective communication between these regions are presently unclear. The intralaminar thalamic nuclei (IL) probably serves as a central hub in this circuit by connecting the critical brainstem and forebrain areas. We found that GABAergic and glycinergic fibers ascending from the pontine reticular formation (PRF) of the brainstem evoked fast and reliable inhibition in the IL via large, multisynaptic terminals. This inhibition was fine-tuned through heterogeneous GABAergic and glycinergic receptor ratios expressed at individual synapses. Optogenetic activation of PRF axons in the IL of freely moving mice led to behavioral arrest and transient interruption of awake cortical activity. An afferent system with comparable morphological features was also found in the human IL. These data reveal an evolutionarily conserved ascending system that gates forebrain activity through fast and powerful synaptic inhibition of the IL.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>25706472</pmid><doi>10.1038/nn.3951</doi><tpages>7</tpages><orcidid>https://orcid.org/0000-0002-4106-6132</orcidid><orcidid>https://orcid.org/0000-0002-8928-0154</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Nature neuroscience, 2015-04, Vol.18 (4), p.562-568 |
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| subjects | 13/1 13/44 13/51 14 14/19 14/28 14/34 631/378/2632 631/378/3920 64/60 82 9/26 9/30 9/74 Afferent Pathways - physiology Animal Genetics and Genomics Animals Behavior Behavior, Animal - physiology Behavioral Sciences Biological Techniques Biomedicine GABAergic Neurons - physiology Glycine - metabolism Intralaminar Thalamic Nuclei - physiology Life Sciences Male Medical examination Mice Morphology Nerve Fibers - physiology Neural Inhibition - physiology Neural transmission Neurobiology Neurons and Cognition Neurosciences Optogenetics Patch-Clamp Techniques Physiological aspects Pontine Tegmentum - physiology Receptors, GABA - metabolism Receptors, Glycine - metabolism Thalamus |
| title | A subcortical inhibitory signal for behavioral arrest in the thalamus |
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