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Anatomical projections to the dorsal tegmental nucleus and abducens nucleus arise from separate cell populations in the nucleus prepositus hypoglossi, but overlapping cell populations in the medial vestibular nucleus
Specialized circuitry in the brain processes spatial information to provide a sense of direction used for navigation. The dorsal tegmental nucleus (DTN) is a core component of this circuitry and utilizes vestibular inputs to generate neural activity encoding the animal's directional heading. Pr...
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Published in: | Journal of comparative neurology (1911) 2021-07, Vol.529 (10), p.2706-2726, Article cne.25119 |
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description | Specialized circuitry in the brain processes spatial information to provide a sense of direction used for navigation. The dorsal tegmental nucleus (DTN) is a core component of this circuitry and utilizes vestibular inputs to generate neural activity encoding the animal's directional heading. Projections arising from the nucleus prepositus hypoglossi (NPH) and the medial vestibular nucleus (MVe) are thought to transmit critical vestibular signals to the DTN and other brain areas, including the abducens nucleus (ABN), a component of eye movement circuitry. Here, we utilized a dual retrograde tracer approach in rats to investigate whether overlapping or distinct populations of neurons project from the NPH or MVe to the DTN and ABN. We report that individual MVe neurons project to both the DTN and ABN. In contrast, we observed individual NPH neurons that project to either the DTN or ABN, but rarely to both structures simultaneously. We also examined labeling patterns in other structures located in the brainstem and posterior cortex and observed (1) complex patterns of interhemispheric connectivity between the left and right DTN, (2) projections from the supragenual nucleus, interpeduncular nucleus, and retrosplenial cortex to the DTN, (3) projections from the lateral superior olive to the ABN, and (4) a unique population of cerebrospinal fluid‐contacting neurons in the dorsal raphe nucleus. Collectively, our experiments provide valuable new information that extends our understanding of the anatomical organization of the brain's spatial processing circuitry.
Retrograde tracers were utilized to examine projections to the dorsal tegmental nucleus (DTN), a critical component of the head direction cell circuitry, and the abducens nucleus, an oculomotor structure. We found that the medial vestibular nucleus contains individual neurons that project to both the DTN and abducens nucleus. In contrast, neurons in the nucleus prepositus hypoglossi project to either the DTN or abducens nucleus, but rarely to both structures simultaneously. Additionally, we describe interhemispheric connections between the left and right DTN, and projections from the supragenual nucleus, interpeduncular nucleus, and retrosplenial cortex to the DTN. |
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Retrograde tracers were utilized to examine projections to the dorsal tegmental nucleus (DTN), a critical component of the head direction cell circuitry, and the abducens nucleus, an oculomotor structure. We found that the medial vestibular nucleus contains individual neurons that project to both the DTN and abducens nucleus. In contrast, neurons in the nucleus prepositus hypoglossi project to either the DTN or abducens nucleus, but rarely to both structures simultaneously. Additionally, we describe interhemispheric connections between the left and right DTN, and projections from the supragenual nucleus, interpeduncular nucleus, and retrosplenial cortex to the DTN.</description><identifier>ISSN: 0021-9967</identifier><identifier>EISSN: 1096-9861</identifier><identifier>DOI: 10.1002/cne.25119</identifier><identifier>PMID: 33511641</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>abducens nucleus ; Animals ; Brain - cytology ; Brain architecture ; Brain stem ; Cerebral hemispheres ; Cerebrospinal fluid ; Dorsal raphe nucleus ; Dorsal tegmental nucleus ; Female ; head direction cell ; Information processing ; navigation ; Navigation behavior ; Neural networks ; Neural Pathways - cytology ; Neuroanatomical Tract-Tracing Techniques ; Neurons ; Neurons - cytology ; Raphe nuclei ; Rats ; Rats, Long-Evans ; spatial orientation ; Vestibular nuclei ; Vestibular system</subject><ispartof>Journal of comparative neurology (1911), 2021-07, Vol.529 (10), p.2706-2726, Article cne.25119</ispartof><rights>2021 Wiley Periodicals LLC</rights><rights>2021 Wiley Periodicals LLC.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c4039-c19dabaf7e11cd4646d5eca8aa9d9849c8ae162d74bc81a7785af2e6b919527c3</cites><orcidid>0000-0002-6121-1253 ; 0000-0001-6487-0791</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33511641$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mehlman, Max L.</creatorcontrib><creatorcontrib>Marcroft, Jennifer L.</creatorcontrib><creatorcontrib>Taube, Jeffrey S.</creatorcontrib><title>Anatomical projections to the dorsal tegmental nucleus and abducens nucleus arise from separate cell populations in the nucleus prepositus hypoglossi, but overlapping cell populations in the medial vestibular nucleus</title><title>Journal of comparative neurology (1911)</title><addtitle>J Comp Neurol</addtitle><description>Specialized circuitry in the brain processes spatial information to provide a sense of direction used for navigation. The dorsal tegmental nucleus (DTN) is a core component of this circuitry and utilizes vestibular inputs to generate neural activity encoding the animal's directional heading. Projections arising from the nucleus prepositus hypoglossi (NPH) and the medial vestibular nucleus (MVe) are thought to transmit critical vestibular signals to the DTN and other brain areas, including the abducens nucleus (ABN), a component of eye movement circuitry. Here, we utilized a dual retrograde tracer approach in rats to investigate whether overlapping or distinct populations of neurons project from the NPH or MVe to the DTN and ABN. We report that individual MVe neurons project to both the DTN and ABN. In contrast, we observed individual NPH neurons that project to either the DTN or ABN, but rarely to both structures simultaneously. We also examined labeling patterns in other structures located in the brainstem and posterior cortex and observed (1) complex patterns of interhemispheric connectivity between the left and right DTN, (2) projections from the supragenual nucleus, interpeduncular nucleus, and retrosplenial cortex to the DTN, (3) projections from the lateral superior olive to the ABN, and (4) a unique population of cerebrospinal fluid‐contacting neurons in the dorsal raphe nucleus. Collectively, our experiments provide valuable new information that extends our understanding of the anatomical organization of the brain's spatial processing circuitry.
Retrograde tracers were utilized to examine projections to the dorsal tegmental nucleus (DTN), a critical component of the head direction cell circuitry, and the abducens nucleus, an oculomotor structure. We found that the medial vestibular nucleus contains individual neurons that project to both the DTN and abducens nucleus. In contrast, neurons in the nucleus prepositus hypoglossi project to either the DTN or abducens nucleus, but rarely to both structures simultaneously. Additionally, we describe interhemispheric connections between the left and right DTN, and projections from the supragenual nucleus, interpeduncular nucleus, and retrosplenial cortex to the DTN.</description><subject>abducens nucleus</subject><subject>Animals</subject><subject>Brain - cytology</subject><subject>Brain architecture</subject><subject>Brain stem</subject><subject>Cerebral hemispheres</subject><subject>Cerebrospinal fluid</subject><subject>Dorsal raphe nucleus</subject><subject>Dorsal tegmental nucleus</subject><subject>Female</subject><subject>head direction cell</subject><subject>Information processing</subject><subject>navigation</subject><subject>Navigation behavior</subject><subject>Neural networks</subject><subject>Neural Pathways - cytology</subject><subject>Neuroanatomical Tract-Tracing Techniques</subject><subject>Neurons</subject><subject>Neurons - cytology</subject><subject>Raphe nuclei</subject><subject>Rats</subject><subject>Rats, Long-Evans</subject><subject>spatial orientation</subject><subject>Vestibular nuclei</subject><subject>Vestibular system</subject><issn>0021-9967</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp1ks9u1DAQhyMEokvhwAsgS1xAIq2dOIl9qVStyh-pggucrYkz2fUqsYPtLNo35XFwm-4KkHqy5fn86TejybLXjF4wSotLbfGiqBiTT7IVo7LOpajZ02yVaiyXsm7Oshch7CilUpbieXZWlomuOVtlv68tRDcaDQOZvNuhjsbZQKIjcYukcz6kSsTNiDamm531gHMgYDsCbTdrTPDp0ZuApPduJAEn8BCRaByS2U3zAIvZ2Hvz8c_kcXLBxHTdHia3GVwI5gNp50jcHv0A02Ts5lHNiJ1JsfYYomlT0R_FL7NnPQwBXz2c59mPjzff15_z22-fvqyvb3PNaSlzzWQHLfQNMqY7XvO6q1CDAJCdFFxqAcjqomt4qwWDphEV9AXWrWSyKhpdnmdXi3ea2xQmzSN6GNTkzQj-oBwY9W_Fmq3auL0SjJVU1Enw7kHg3c859aFGE-7aBYtuDqrgohRMNCVP6Nv_0J2bvU3tqaIqOGcVlU2i3i-U9mmWHvtTGEbV3b6otC_qfl8S--bv9CfyuCAJuFyAX2bAw-Mmtf56syj_AKc-0p8</recordid><startdate>20210701</startdate><enddate>20210701</enddate><creator>Mehlman, Max L.</creator><creator>Marcroft, Jennifer L.</creator><creator>Taube, Jeffrey S.</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</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>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6121-1253</orcidid><orcidid>https://orcid.org/0000-0001-6487-0791</orcidid></search><sort><creationdate>20210701</creationdate><title>Anatomical projections to the dorsal tegmental nucleus and abducens nucleus arise from separate cell populations in the nucleus prepositus hypoglossi, but overlapping cell populations in the medial vestibular nucleus</title><author>Mehlman, Max L. ; Marcroft, Jennifer L. ; Taube, Jeffrey S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4039-c19dabaf7e11cd4646d5eca8aa9d9849c8ae162d74bc81a7785af2e6b919527c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>abducens nucleus</topic><topic>Animals</topic><topic>Brain - cytology</topic><topic>Brain architecture</topic><topic>Brain stem</topic><topic>Cerebral hemispheres</topic><topic>Cerebrospinal fluid</topic><topic>Dorsal raphe nucleus</topic><topic>Dorsal tegmental nucleus</topic><topic>Female</topic><topic>head direction cell</topic><topic>Information processing</topic><topic>navigation</topic><topic>Navigation behavior</topic><topic>Neural networks</topic><topic>Neural Pathways - cytology</topic><topic>Neuroanatomical Tract-Tracing Techniques</topic><topic>Neurons</topic><topic>Neurons - cytology</topic><topic>Raphe nuclei</topic><topic>Rats</topic><topic>Rats, Long-Evans</topic><topic>spatial orientation</topic><topic>Vestibular nuclei</topic><topic>Vestibular system</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mehlman, Max L.</creatorcontrib><creatorcontrib>Marcroft, Jennifer L.</creatorcontrib><creatorcontrib>Taube, Jeffrey S.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</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>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of comparative neurology (1911)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mehlman, Max L.</au><au>Marcroft, Jennifer L.</au><au>Taube, Jeffrey S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Anatomical projections to the dorsal tegmental nucleus and abducens nucleus arise from separate cell populations in the nucleus prepositus hypoglossi, but overlapping cell populations in the medial vestibular nucleus</atitle><jtitle>Journal of comparative neurology (1911)</jtitle><addtitle>J Comp Neurol</addtitle><date>2021-07-01</date><risdate>2021</risdate><volume>529</volume><issue>10</issue><spage>2706</spage><epage>2726</epage><pages>2706-2726</pages><artnum>cne.25119</artnum><issn>0021-9967</issn><eissn>1096-9861</eissn><abstract>Specialized circuitry in the brain processes spatial information to provide a sense of direction used for navigation. The dorsal tegmental nucleus (DTN) is a core component of this circuitry and utilizes vestibular inputs to generate neural activity encoding the animal's directional heading. Projections arising from the nucleus prepositus hypoglossi (NPH) and the medial vestibular nucleus (MVe) are thought to transmit critical vestibular signals to the DTN and other brain areas, including the abducens nucleus (ABN), a component of eye movement circuitry. Here, we utilized a dual retrograde tracer approach in rats to investigate whether overlapping or distinct populations of neurons project from the NPH or MVe to the DTN and ABN. We report that individual MVe neurons project to both the DTN and ABN. In contrast, we observed individual NPH neurons that project to either the DTN or ABN, but rarely to both structures simultaneously. We also examined labeling patterns in other structures located in the brainstem and posterior cortex and observed (1) complex patterns of interhemispheric connectivity between the left and right DTN, (2) projections from the supragenual nucleus, interpeduncular nucleus, and retrosplenial cortex to the DTN, (3) projections from the lateral superior olive to the ABN, and (4) a unique population of cerebrospinal fluid‐contacting neurons in the dorsal raphe nucleus. Collectively, our experiments provide valuable new information that extends our understanding of the anatomical organization of the brain's spatial processing circuitry.
Retrograde tracers were utilized to examine projections to the dorsal tegmental nucleus (DTN), a critical component of the head direction cell circuitry, and the abducens nucleus, an oculomotor structure. We found that the medial vestibular nucleus contains individual neurons that project to both the DTN and abducens nucleus. In contrast, neurons in the nucleus prepositus hypoglossi project to either the DTN or abducens nucleus, but rarely to both structures simultaneously. Additionally, we describe interhemispheric connections between the left and right DTN, and projections from the supragenual nucleus, interpeduncular nucleus, and retrosplenial cortex to the DTN.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>33511641</pmid><doi>10.1002/cne.25119</doi><tpages>21</tpages><orcidid>https://orcid.org/0000-0002-6121-1253</orcidid><orcidid>https://orcid.org/0000-0001-6487-0791</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | abducens nucleus Animals Brain - cytology Brain architecture Brain stem Cerebral hemispheres Cerebrospinal fluid Dorsal raphe nucleus Dorsal tegmental nucleus Female head direction cell Information processing navigation Navigation behavior Neural networks Neural Pathways - cytology Neuroanatomical Tract-Tracing Techniques Neurons Neurons - cytology Raphe nuclei Rats Rats, Long-Evans spatial orientation Vestibular nuclei Vestibular system |
title | Anatomical projections to the dorsal tegmental nucleus and abducens nucleus arise from separate cell populations in the nucleus prepositus hypoglossi, but overlapping cell populations in the medial vestibular nucleus |
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