Recurrent Inhibition to the Medial Nucleus of the Trapezoid Body in the Mongolian Gerbil (Meriones Unguiculatus)
Principal neurons in the medial nucleus of the trapezoid body (MNTB) receive strong and temporally precise excitatory input from globular bushy cells in the cochlear nucleus through the calyx of Held. The extremely large synaptic currents produced by the calyx have sometimes led to the view of the M...
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description | Principal neurons in the medial nucleus of the trapezoid body (MNTB) receive strong and temporally precise excitatory input from globular bushy cells in the cochlear nucleus through the calyx of Held. The extremely large synaptic currents produced by the calyx have sometimes led to the view of the MNTB as a simple relay synapse which converts incoming excitation to outgoing inhibition. However, electrophysiological and anatomical studies have shown the additional presence of inhibitory glycinergic currents that are large enough to suppress action potentials in MNTB neurons at least in some cases. The source(s) of glycinergic inhibition to MNTB are not fully understood. One major extrinsic source of glycinergic inhibitory input to MNTB is the ventral nucleus of the trapezoid body. However, it has been suggested that MNTB neurons receive additional inhibitory inputs via intrinsic connections (collaterals of glycinergic projections of MNTB neurons). While several authors have postulated their presence, these collaterals have never been examined in detail. Here we test the hypothesis that collaterals of MNTB principal cells provide glycinergic inhibition to the MNTB. We injected dye into single principal neurons in the MNTB, traced their projections, and immunohistochemically identified their synapses. We found that collaterals terminate within the MNTB and provide an additional source of inhibition to other principal cells, creating an inhibitory microcircuit within the MNTB. Only about a quarter to a third of MNTB neurons receive such collateral inputs. This microcircuit could produce side band inhibition and enhance frequency tuning of MNTB neurons, consistent with physiological observations. |
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The extremely large synaptic currents produced by the calyx have sometimes led to the view of the MNTB as a simple relay synapse which converts incoming excitation to outgoing inhibition. However, electrophysiological and anatomical studies have shown the additional presence of inhibitory glycinergic currents that are large enough to suppress action potentials in MNTB neurons at least in some cases. The source(s) of glycinergic inhibition to MNTB are not fully understood. One major extrinsic source of glycinergic inhibitory input to MNTB is the ventral nucleus of the trapezoid body. However, it has been suggested that MNTB neurons receive additional inhibitory inputs via intrinsic connections (collaterals of glycinergic projections of MNTB neurons). While several authors have postulated their presence, these collaterals have never been examined in detail. Here we test the hypothesis that collaterals of MNTB principal cells provide glycinergic inhibition to the MNTB. We injected dye into single principal neurons in the MNTB, traced their projections, and immunohistochemically identified their synapses. We found that collaterals terminate within the MNTB and provide an additional source of inhibition to other principal cells, creating an inhibitory microcircuit within the MNTB. Only about a quarter to a third of MNTB neurons receive such collateral inputs. This microcircuit could produce side band inhibition and enhance frequency tuning of MNTB neurons, consistent with physiological observations.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0160241</identifier><identifier>PMID: 27489949</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Animals ; Biology and Life Sciences ; Biophysics ; Circuits ; Cochlea ; Cochlear nuclei ; Female ; Genetic aspects ; Gerbillinae ; Immunohistochemistry ; Inhibition ; Laboratory animals ; Localization ; Lysine - analogs & derivatives ; Lysine - chemistry ; Male ; Medicine ; Medicine and Health Sciences ; Microscopy ; Microscopy, Fluorescence ; Neurons ; Neurons - metabolism ; Neurons - pathology ; Nuclei (cytology) ; Patch-Clamp Techniques ; Physiological aspects ; Physiology ; Research and Analysis Methods ; Single-Cell Analysis ; Studies ; Synapses ; Synapses - metabolism ; Synaptosomal-Associated Protein 25 - metabolism ; Trapezoid body ; Trapezoid Body - cytology ; Trapezoid Body - metabolism</subject><ispartof>PloS one, 2016-08, Vol.11 (8), p.e0160241-e0160241</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Dondzillo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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The extremely large synaptic currents produced by the calyx have sometimes led to the view of the MNTB as a simple relay synapse which converts incoming excitation to outgoing inhibition. However, electrophysiological and anatomical studies have shown the additional presence of inhibitory glycinergic currents that are large enough to suppress action potentials in MNTB neurons at least in some cases. The source(s) of glycinergic inhibition to MNTB are not fully understood. One major extrinsic source of glycinergic inhibitory input to MNTB is the ventral nucleus of the trapezoid body. However, it has been suggested that MNTB neurons receive additional inhibitory inputs via intrinsic connections (collaterals of glycinergic projections of MNTB neurons). While several authors have postulated their presence, these collaterals have never been examined in detail. Here we test the hypothesis that collaterals of MNTB principal cells provide glycinergic inhibition to the MNTB. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dondzillo, Anna</au><au>Thompson, John A</au><au>Klug, Achim</au><au>Sugihara, Izumi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Recurrent Inhibition to the Medial Nucleus of the Trapezoid Body in the Mongolian Gerbil (Meriones Unguiculatus)</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-08-04</date><risdate>2016</risdate><volume>11</volume><issue>8</issue><spage>e0160241</spage><epage>e0160241</epage><pages>e0160241-e0160241</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Principal neurons in the medial nucleus of the trapezoid body (MNTB) receive strong and temporally precise excitatory input from globular bushy cells in the cochlear nucleus through the calyx of Held. The extremely large synaptic currents produced by the calyx have sometimes led to the view of the MNTB as a simple relay synapse which converts incoming excitation to outgoing inhibition. However, electrophysiological and anatomical studies have shown the additional presence of inhibitory glycinergic currents that are large enough to suppress action potentials in MNTB neurons at least in some cases. The source(s) of glycinergic inhibition to MNTB are not fully understood. One major extrinsic source of glycinergic inhibitory input to MNTB is the ventral nucleus of the trapezoid body. However, it has been suggested that MNTB neurons receive additional inhibitory inputs via intrinsic connections (collaterals of glycinergic projections of MNTB neurons). While several authors have postulated their presence, these collaterals have never been examined in detail. Here we test the hypothesis that collaterals of MNTB principal cells provide glycinergic inhibition to the MNTB. We injected dye into single principal neurons in the MNTB, traced their projections, and immunohistochemically identified their synapses. We found that collaterals terminate within the MNTB and provide an additional source of inhibition to other principal cells, creating an inhibitory microcircuit within the MNTB. Only about a quarter to a third of MNTB neurons receive such collateral inputs. This microcircuit could produce side band inhibition and enhance frequency tuning of MNTB neurons, consistent with physiological observations.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27489949</pmid><doi>10.1371/journal.pone.0160241</doi><tpages>e0160241</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acids Animals Biology and Life Sciences Biophysics Circuits Cochlea Cochlear nuclei Female Genetic aspects Gerbillinae Immunohistochemistry Inhibition Laboratory animals Localization Lysine - analogs & derivatives Lysine - chemistry Male Medicine Medicine and Health Sciences Microscopy Microscopy, Fluorescence Neurons Neurons - metabolism Neurons - pathology Nuclei (cytology) Patch-Clamp Techniques Physiological aspects Physiology Research and Analysis Methods Single-Cell Analysis Studies Synapses Synapses - metabolism Synaptosomal-Associated Protein 25 - metabolism Trapezoid body Trapezoid Body - cytology Trapezoid Body - metabolism |
title | Recurrent Inhibition to the Medial Nucleus of the Trapezoid Body in the Mongolian Gerbil (Meriones Unguiculatus) |
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