Circuits for Grasping: Spinal dI3 Interneurons Mediate Cutaneous Control of Motor Behavior
Accurate motor performance depends on the integration in spinal microcircuits of sensory feedback information. Hand grasp is a skilled motor behavior known to require cutaneous sensory feedback, but spinal microcircuits that process and relay this feedback to the motor system have not been defined....
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Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2013-04, Vol.78 (1), p.191-204 |
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creator | Bui, Tuan V. Akay, Turgay Loubani, Osama Hnasko, Thomas S. Jessell, Thomas M. Brownstone, Robert M. |
description | Accurate motor performance depends on the integration in spinal microcircuits of sensory feedback information. Hand grasp is a skilled motor behavior known to require cutaneous sensory feedback, but spinal microcircuits that process and relay this feedback to the motor system have not been defined. We sought to define classes of spinal interneurons involved in the cutaneous control of hand grasp in mice and to show that dI3 interneurons, a class of dorsal spinal interneurons marked by the expression of Isl1, convey input from low threshold cutaneous afferents to motoneurons. Mice in which the output of dI3 interneurons has been inactivated exhibit deficits in motor tasks that rely on cutaneous afferent input. Most strikingly, the ability to maintain grip strength in response to increasing load is lost following genetic silencing of dI3 interneuron output. Thus, spinal microcircuits that integrate cutaneous feedback crucial for paw grip rely on the intermediary role of dI3 interneurons.
► Spinal dI3 interneurons are glutamatergic and project to motoneurons ► dI3 interneurons receive direct primary afferent inputs from cutaneous afferents ► Silencing the output of dI3 interneurons disrupts a disynaptic cutaneous reflex ► dI3 interneurons mediate cutaneous control of paw grasp
Bui et al. identify a microcircuit in the mouse spinal cord involved in cutaneous regulation of motor control. Using genetic strategies, they demonstrate that removing dI3 interneuron function from this circuit impairs the ability of mice to regulate grip strength. |
doi_str_mv | 10.1016/j.neuron.2013.02.007 |
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► Spinal dI3 interneurons are glutamatergic and project to motoneurons ► dI3 interneurons receive direct primary afferent inputs from cutaneous afferents ► Silencing the output of dI3 interneurons disrupts a disynaptic cutaneous reflex ► dI3 interneurons mediate cutaneous control of paw grasp
Bui et al. identify a microcircuit in the mouse spinal cord involved in cutaneous regulation of motor control. Using genetic strategies, they demonstrate that removing dI3 interneuron function from this circuit impairs the ability of mice to regulate grip strength.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2013.02.007</identifier><identifier>PMID: 23583114</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Animals, Newborn ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Behavior ; Biotin - analogs & derivatives ; Biotin - metabolism ; Choline O-Acetyltransferase - metabolism ; Electric Stimulation ; Feedback, Sensory - physiology ; Green Fluorescent Proteins - genetics ; Hand Strength - physiology ; Interneurons - physiology ; LIM-Homeodomain Proteins - genetics ; LIM-Homeodomain Proteins - metabolism ; Luminescent Proteins - genetics ; Luminescent Proteins - metabolism ; Medical research ; Membrane Potentials - genetics ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Movement - physiology ; Nerve Net - physiology ; Neurons ; Parvalbumins - metabolism ; Patch-Clamp Techniques ; Reflex - physiology ; RNA, Messenger - metabolism ; Rodents ; Skin - innervation ; Spinal Cord - cytology ; Thy-1 Antigens - genetics ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Vesicular Glutamate Transport Protein 2 - genetics ; Vesicular Glutamate Transport Protein 2 - metabolism</subject><ispartof>Neuron (Cambridge, Mass.), 2013-04, Vol.78 (1), p.191-204</ispartof><rights>2013 Elsevier Inc.</rights><rights>Copyright © 2013 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Apr 10, 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c590t-f4a48cc7849c72c0341c393cd929425d8a64fbd1d8e8440fa45b04ac526b3c733</citedby><cites>FETCH-LOGICAL-c590t-f4a48cc7849c72c0341c393cd929425d8a64fbd1d8e8440fa45b04ac526b3c733</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuron.2013.02.007$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,778,782,883,3539,27907,27908,45978</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23583114$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bui, Tuan V.</creatorcontrib><creatorcontrib>Akay, Turgay</creatorcontrib><creatorcontrib>Loubani, Osama</creatorcontrib><creatorcontrib>Hnasko, Thomas S.</creatorcontrib><creatorcontrib>Jessell, Thomas M.</creatorcontrib><creatorcontrib>Brownstone, Robert M.</creatorcontrib><title>Circuits for Grasping: Spinal dI3 Interneurons Mediate Cutaneous Control of Motor Behavior</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Accurate motor performance depends on the integration in spinal microcircuits of sensory feedback information. Hand grasp is a skilled motor behavior known to require cutaneous sensory feedback, but spinal microcircuits that process and relay this feedback to the motor system have not been defined. We sought to define classes of spinal interneurons involved in the cutaneous control of hand grasp in mice and to show that dI3 interneurons, a class of dorsal spinal interneurons marked by the expression of Isl1, convey input from low threshold cutaneous afferents to motoneurons. Mice in which the output of dI3 interneurons has been inactivated exhibit deficits in motor tasks that rely on cutaneous afferent input. Most strikingly, the ability to maintain grip strength in response to increasing load is lost following genetic silencing of dI3 interneuron output. Thus, spinal microcircuits that integrate cutaneous feedback crucial for paw grip rely on the intermediary role of dI3 interneurons.
► Spinal dI3 interneurons are glutamatergic and project to motoneurons ► dI3 interneurons receive direct primary afferent inputs from cutaneous afferents ► Silencing the output of dI3 interneurons disrupts a disynaptic cutaneous reflex ► dI3 interneurons mediate cutaneous control of paw grasp
Bui et al. identify a microcircuit in the mouse spinal cord involved in cutaneous regulation of motor control. 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Akay, Turgay ; Loubani, Osama ; Hnasko, Thomas S. ; Jessell, Thomas M. ; Brownstone, Robert M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c590t-f4a48cc7849c72c0341c393cd929425d8a64fbd1d8e8440fa45b04ac526b3c733</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Behavior</topic><topic>Biotin - analogs & derivatives</topic><topic>Biotin - metabolism</topic><topic>Choline O-Acetyltransferase - metabolism</topic><topic>Electric Stimulation</topic><topic>Feedback, Sensory - physiology</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Hand Strength - physiology</topic><topic>Interneurons - physiology</topic><topic>LIM-Homeodomain Proteins - genetics</topic><topic>LIM-Homeodomain Proteins - metabolism</topic><topic>Luminescent Proteins - genetics</topic><topic>Luminescent Proteins - metabolism</topic><topic>Medical research</topic><topic>Membrane Potentials - genetics</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Transgenic</topic><topic>Movement - physiology</topic><topic>Nerve Net - physiology</topic><topic>Neurons</topic><topic>Parvalbumins - metabolism</topic><topic>Patch-Clamp Techniques</topic><topic>Reflex - physiology</topic><topic>RNA, Messenger - metabolism</topic><topic>Rodents</topic><topic>Skin - innervation</topic><topic>Spinal Cord - cytology</topic><topic>Thy-1 Antigens - genetics</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>Vesicular Glutamate Transport Protein 2 - genetics</topic><topic>Vesicular Glutamate Transport Protein 2 - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bui, Tuan V.</creatorcontrib><creatorcontrib>Akay, Turgay</creatorcontrib><creatorcontrib>Loubani, Osama</creatorcontrib><creatorcontrib>Hnasko, Thomas S.</creatorcontrib><creatorcontrib>Jessell, Thomas M.</creatorcontrib><creatorcontrib>Brownstone, Robert M.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bui, Tuan V.</au><au>Akay, Turgay</au><au>Loubani, Osama</au><au>Hnasko, Thomas S.</au><au>Jessell, Thomas M.</au><au>Brownstone, Robert M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Circuits for Grasping: Spinal dI3 Interneurons Mediate Cutaneous Control of Motor Behavior</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2013-04-10</date><risdate>2013</risdate><volume>78</volume><issue>1</issue><spage>191</spage><epage>204</epage><pages>191-204</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>Accurate motor performance depends on the integration in spinal microcircuits of sensory feedback information. Hand grasp is a skilled motor behavior known to require cutaneous sensory feedback, but spinal microcircuits that process and relay this feedback to the motor system have not been defined. We sought to define classes of spinal interneurons involved in the cutaneous control of hand grasp in mice and to show that dI3 interneurons, a class of dorsal spinal interneurons marked by the expression of Isl1, convey input from low threshold cutaneous afferents to motoneurons. Mice in which the output of dI3 interneurons has been inactivated exhibit deficits in motor tasks that rely on cutaneous afferent input. Most strikingly, the ability to maintain grip strength in response to increasing load is lost following genetic silencing of dI3 interneuron output. Thus, spinal microcircuits that integrate cutaneous feedback crucial for paw grip rely on the intermediary role of dI3 interneurons.
► Spinal dI3 interneurons are glutamatergic and project to motoneurons ► dI3 interneurons receive direct primary afferent inputs from cutaneous afferents ► Silencing the output of dI3 interneurons disrupts a disynaptic cutaneous reflex ► dI3 interneurons mediate cutaneous control of paw grasp
Bui et al. identify a microcircuit in the mouse spinal cord involved in cutaneous regulation of motor control. Using genetic strategies, they demonstrate that removing dI3 interneuron function from this circuit impairs the ability of mice to regulate grip strength.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>23583114</pmid><doi>10.1016/j.neuron.2013.02.007</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Animals, Newborn Bacterial Proteins - genetics Bacterial Proteins - metabolism Behavior Biotin - analogs & derivatives Biotin - metabolism Choline O-Acetyltransferase - metabolism Electric Stimulation Feedback, Sensory - physiology Green Fluorescent Proteins - genetics Hand Strength - physiology Interneurons - physiology LIM-Homeodomain Proteins - genetics LIM-Homeodomain Proteins - metabolism Luminescent Proteins - genetics Luminescent Proteins - metabolism Medical research Membrane Potentials - genetics Mice Mice, Inbred C57BL Mice, Transgenic Movement - physiology Nerve Net - physiology Neurons Parvalbumins - metabolism Patch-Clamp Techniques Reflex - physiology RNA, Messenger - metabolism Rodents Skin - innervation Spinal Cord - cytology Thy-1 Antigens - genetics Transcription Factors - genetics Transcription Factors - metabolism Vesicular Glutamate Transport Protein 2 - genetics Vesicular Glutamate Transport Protein 2 - metabolism |
title | Circuits for Grasping: Spinal dI3 Interneurons Mediate Cutaneous Control of Motor Behavior |
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