As above, so below: Whole transcriptome profiling demonstrates strong molecular similarities between avian dorsal and ventral pallial subdivisions
Over the last two decades, beginning with the Avian Brain Nomenclature Forum in 2000, major revisions have been made to our understanding of the organization and nomenclature of the avian brain. However, there are still unresolved questions on avian pallial organization, particularly whether the cel...
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description | Over the last two decades, beginning with the Avian Brain Nomenclature Forum in 2000, major revisions have been made to our understanding of the organization and nomenclature of the avian brain. However, there are still unresolved questions on avian pallial organization, particularly whether the cells above the vestigial ventricle represent distinct populations to those below it or similar populations. To test these two hypotheses, we profiled the transcriptomes of the major avian pallial subdivisions dorsal and ventral to the vestigial ventricle boundary using RNA sequencing and a new zebra finch genome assembly containing about 22,000 annotated, complete genes. We found that the transcriptomes of neural populations above and below the ventricle were remarkably similar. Each subdivision in dorsal pallium (Wulst) had a corresponding molecular counterpart in the ventral pallium (dorsal ventricular ridge). In turn, each corresponding subdivision exhibited shared gene co‐expression modules that contained gene sets enriched in functional specializations, such as anatomical structure development, synaptic transmission, signaling, and neurogenesis. These findings are more in line with the continuum hypothesis of avian brain subdivision organization above and below the vestigial ventricle space, with the pallium as a whole consisting of four major cell populations (intercalated pallium, mesopallium, hyper‐nidopallium, and arcopallium) instead of seven (hyperpallium apicale, interstitial hyperpallium apicale, intercalated hyperpallium, hyperpallium densocellare, mesopallium, nidopallium, and arcopallium). We suggest adopting a more streamlined hierarchical naming system that reflects the robust similarities in gene expression, neural connectivity motifs, and function. These findings have important implications for our understanding of overall vertebrate brain evolution.
In 2013, our group examined the expression profiles of 50 genes to develop the continuum hypothesis of avian brain organization. It states that the subdivisions of the dorsal pallium develop continuously with those of the ventral pallium, resulting in a “partial mirror image” organization around the vestigial ventricle divide. However, these claims were challenged due to the small number of genes profiled. The present study uses RNA sequencing to profile the whole transcriptome (~20,000 genes) of the principal subdivisions of the avian telencephalon and confirms the remarkable molecularly similarit |
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In 2013, our group examined the expression profiles of 50 genes to develop the continuum hypothesis of avian brain organization. It states that the subdivisions of the dorsal pallium develop continuously with those of the ventral pallium, resulting in a “partial mirror image” organization around the vestigial ventricle divide. However, these claims were challenged due to the small number of genes profiled. The present study uses RNA sequencing to profile the whole transcriptome (~20,000 genes) of the principal subdivisions of the avian telencephalon and confirms the remarkable molecularly similarities between the dorsal and ventral pallium. We recommend adopting a hierarchal nomenclature to reflect these robust molecular similarities.</description><identifier>ISSN: 0021-9967</identifier><identifier>EISSN: 1096-9861</identifier><identifier>DOI: 10.1002/cne.25159</identifier><identifier>PMID: 33871048</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Animals ; avian ; Brain - growth & development ; Brain - metabolism ; Brain architecture ; brain evolution ; Finches ; Gene expression ; Gene Expression Profiling - methods ; Gene Expression Regulation, Developmental - physiology ; Genomes ; Hyperstriatum ; Male ; Neural networks ; Neurogenesis ; Pallium ; RNA‐Seq ; RRIDs ; SCR_000432 ; SCR_001905 ; SCR_003092 ; SCR_003302 ; SCR_004277 ; SCR_010943 ; SCR_012988 ; SCR_014583 ; SCR_015687 ; SCR_015954 ; SCR_017036 ; SCR_018190 ; SCR_021061 ; SCR_021062 ; SCR_021063 ; Sequence Analysis, RNA - methods ; Songbirds ; Synaptic transmission ; Synaptogenesis ; Transcriptomes ; transcriptomics ; Ventricle ; Ventricles (cerebral) ; WGNCA</subject><ispartof>Journal of comparative neurology (1911), 2021-08, Vol.529 (12), p.3222-3246</ispartof><rights>2021 The Authors. published by Wiley Periodicals LLC.</rights><rights>2021 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.</rights><rights>2021. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5499-845e9b2c3c7ddf78fe4b5066004ad826072608a879027bd44592a35398bfeba63</citedby><cites>FETCH-LOGICAL-c5499-845e9b2c3c7ddf78fe4b5066004ad826072608a879027bd44592a35398bfeba63</cites><orcidid>0000-0002-6450-7551 ; 0000-0001-8945-7282 ; 0000-0001-6819-2019 ; 0000-0001-8931-5049 ; 0000-0003-4331-9890</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fcne.25159$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fcne.25159$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,777,781,882,1412,27905,27906,45555,45556</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33871048$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gedman, Gregory</creatorcontrib><creatorcontrib>Haase, Bettina</creatorcontrib><creatorcontrib>Durieux, Gillian</creatorcontrib><creatorcontrib>Biegler, Matthew T.</creatorcontrib><creatorcontrib>Fedrigo, Olivier</creatorcontrib><creatorcontrib>Jarvis, Erich D.</creatorcontrib><title>As above, so below: Whole transcriptome profiling demonstrates strong molecular similarities between avian dorsal and ventral pallial subdivisions</title><title>Journal of comparative neurology (1911)</title><addtitle>J Comp Neurol</addtitle><description>Over the last two decades, beginning with the Avian Brain Nomenclature Forum in 2000, major revisions have been made to our understanding of the organization and nomenclature of the avian brain. However, there are still unresolved questions on avian pallial organization, particularly whether the cells above the vestigial ventricle represent distinct populations to those below it or similar populations. To test these two hypotheses, we profiled the transcriptomes of the major avian pallial subdivisions dorsal and ventral to the vestigial ventricle boundary using RNA sequencing and a new zebra finch genome assembly containing about 22,000 annotated, complete genes. We found that the transcriptomes of neural populations above and below the ventricle were remarkably similar. Each subdivision in dorsal pallium (Wulst) had a corresponding molecular counterpart in the ventral pallium (dorsal ventricular ridge). In turn, each corresponding subdivision exhibited shared gene co‐expression modules that contained gene sets enriched in functional specializations, such as anatomical structure development, synaptic transmission, signaling, and neurogenesis. These findings are more in line with the continuum hypothesis of avian brain subdivision organization above and below the vestigial ventricle space, with the pallium as a whole consisting of four major cell populations (intercalated pallium, mesopallium, hyper‐nidopallium, and arcopallium) instead of seven (hyperpallium apicale, interstitial hyperpallium apicale, intercalated hyperpallium, hyperpallium densocellare, mesopallium, nidopallium, and arcopallium). We suggest adopting a more streamlined hierarchical naming system that reflects the robust similarities in gene expression, neural connectivity motifs, and function. These findings have important implications for our understanding of overall vertebrate brain evolution.
In 2013, our group examined the expression profiles of 50 genes to develop the continuum hypothesis of avian brain organization. It states that the subdivisions of the dorsal pallium develop continuously with those of the ventral pallium, resulting in a “partial mirror image” organization around the vestigial ventricle divide. However, these claims were challenged due to the small number of genes profiled. The present study uses RNA sequencing to profile the whole transcriptome (~20,000 genes) of the principal subdivisions of the avian telencephalon and confirms the remarkable molecularly similarities between the dorsal and ventral pallium. We recommend adopting a hierarchal nomenclature to reflect these robust molecular similarities.</description><subject>Animals</subject><subject>avian</subject><subject>Brain - growth & development</subject><subject>Brain - metabolism</subject><subject>Brain architecture</subject><subject>brain evolution</subject><subject>Finches</subject><subject>Gene expression</subject><subject>Gene Expression Profiling - methods</subject><subject>Gene Expression Regulation, Developmental - physiology</subject><subject>Genomes</subject><subject>Hyperstriatum</subject><subject>Male</subject><subject>Neural networks</subject><subject>Neurogenesis</subject><subject>Pallium</subject><subject>RNA‐Seq</subject><subject>RRIDs</subject><subject>SCR_000432</subject><subject>SCR_001905</subject><subject>SCR_003092</subject><subject>SCR_003302</subject><subject>SCR_004277</subject><subject>SCR_010943</subject><subject>SCR_012988</subject><subject>SCR_014583</subject><subject>SCR_015687</subject><subject>SCR_015954</subject><subject>SCR_017036</subject><subject>SCR_018190</subject><subject>SCR_021061</subject><subject>SCR_021062</subject><subject>SCR_021063</subject><subject>Sequence Analysis, RNA - methods</subject><subject>Songbirds</subject><subject>Synaptic transmission</subject><subject>Synaptogenesis</subject><subject>Transcriptomes</subject><subject>transcriptomics</subject><subject>Ventricle</subject><subject>Ventricles (cerebral)</subject><subject>WGNCA</subject><issn>0021-9967</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kVFr1TAcxYMo7jp98AtIwBcFu6Vt2iZ7EMZlzsHQF8XHkLT_bhlpUpO2l30NP7H_a7ehAx_KgZ5fDic5hLzO2VHOWHHcejgqqryST8gmZ7LOpKjzp2SDXp5JWTcH5EVKN4wxKUvxnByUpWhyxsWG_DpNVJuwwAeaAjXgwu6E_rgODugUtU9ttOMUBqBjDL111l_RDobgE7oTJIoa8N-AB9rZ6UiTHSyqnSy6BqYdgKd6sdrTLsSkHdW-owt4DHB01M5Z1DSbzi42WUx-SZ712iV4daeH5Puns2_bz9nl1_OL7ell1lZcykzwCqQp2rJtuq5vRA_cVKyuGeO6E0XNGvyEFo1kRWM6zitZ6LIqpTA9GF2Xh-TjmjvOZoCuXSupMdpBx1sVtFX_Ot5eq6uwKIFvLSTHgHd3ATH8nCFNarCpBee0hzAntZ-E1Y0Ue_TtI_QmzNHj9ZDirCo4tkXq_Uq1MaQUoX8okzO1X1rh0n9iJbJv_m7_QN5Pi8DxCuysg9v_J6ntl7M18jedHLZ_</recordid><startdate>202108</startdate><enddate>202108</enddate><creator>Gedman, Gregory</creator><creator>Haase, Bettina</creator><creator>Durieux, Gillian</creator><creator>Biegler, Matthew T.</creator><creator>Fedrigo, Olivier</creator><creator>Jarvis, Erich D.</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><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/0000-0002-6450-7551</orcidid><orcidid>https://orcid.org/0000-0001-8945-7282</orcidid><orcidid>https://orcid.org/0000-0001-6819-2019</orcidid><orcidid>https://orcid.org/0000-0001-8931-5049</orcidid><orcidid>https://orcid.org/0000-0003-4331-9890</orcidid></search><sort><creationdate>202108</creationdate><title>As above, so below: Whole transcriptome profiling demonstrates strong molecular similarities between avian dorsal and ventral pallial subdivisions</title><author>Gedman, Gregory ; Haase, Bettina ; Durieux, Gillian ; Biegler, Matthew T. ; Fedrigo, Olivier ; Jarvis, Erich D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5499-845e9b2c3c7ddf78fe4b5066004ad826072608a879027bd44592a35398bfeba63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>avian</topic><topic>Brain - growth & development</topic><topic>Brain - metabolism</topic><topic>Brain architecture</topic><topic>brain evolution</topic><topic>Finches</topic><topic>Gene expression</topic><topic>Gene Expression Profiling - methods</topic><topic>Gene Expression Regulation, Developmental - physiology</topic><topic>Genomes</topic><topic>Hyperstriatum</topic><topic>Male</topic><topic>Neural networks</topic><topic>Neurogenesis</topic><topic>Pallium</topic><topic>RNA‐Seq</topic><topic>RRIDs</topic><topic>SCR_000432</topic><topic>SCR_001905</topic><topic>SCR_003092</topic><topic>SCR_003302</topic><topic>SCR_004277</topic><topic>SCR_010943</topic><topic>SCR_012988</topic><topic>SCR_014583</topic><topic>SCR_015687</topic><topic>SCR_015954</topic><topic>SCR_017036</topic><topic>SCR_018190</topic><topic>SCR_021061</topic><topic>SCR_021062</topic><topic>SCR_021063</topic><topic>Sequence Analysis, RNA - methods</topic><topic>Songbirds</topic><topic>Synaptic transmission</topic><topic>Synaptogenesis</topic><topic>Transcriptomes</topic><topic>transcriptomics</topic><topic>Ventricle</topic><topic>Ventricles (cerebral)</topic><topic>WGNCA</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gedman, Gregory</creatorcontrib><creatorcontrib>Haase, Bettina</creatorcontrib><creatorcontrib>Durieux, Gillian</creatorcontrib><creatorcontrib>Biegler, Matthew T.</creatorcontrib><creatorcontrib>Fedrigo, Olivier</creatorcontrib><creatorcontrib>Jarvis, Erich D.</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><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>Gedman, Gregory</au><au>Haase, Bettina</au><au>Durieux, Gillian</au><au>Biegler, Matthew T.</au><au>Fedrigo, Olivier</au><au>Jarvis, Erich D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>As above, so below: Whole transcriptome profiling demonstrates strong molecular similarities between avian dorsal and ventral pallial subdivisions</atitle><jtitle>Journal of comparative neurology (1911)</jtitle><addtitle>J Comp Neurol</addtitle><date>2021-08</date><risdate>2021</risdate><volume>529</volume><issue>12</issue><spage>3222</spage><epage>3246</epage><pages>3222-3246</pages><issn>0021-9967</issn><eissn>1096-9861</eissn><abstract>Over the last two decades, beginning with the Avian Brain Nomenclature Forum in 2000, major revisions have been made to our understanding of the organization and nomenclature of the avian brain. However, there are still unresolved questions on avian pallial organization, particularly whether the cells above the vestigial ventricle represent distinct populations to those below it or similar populations. To test these two hypotheses, we profiled the transcriptomes of the major avian pallial subdivisions dorsal and ventral to the vestigial ventricle boundary using RNA sequencing and a new zebra finch genome assembly containing about 22,000 annotated, complete genes. We found that the transcriptomes of neural populations above and below the ventricle were remarkably similar. Each subdivision in dorsal pallium (Wulst) had a corresponding molecular counterpart in the ventral pallium (dorsal ventricular ridge). In turn, each corresponding subdivision exhibited shared gene co‐expression modules that contained gene sets enriched in functional specializations, such as anatomical structure development, synaptic transmission, signaling, and neurogenesis. These findings are more in line with the continuum hypothesis of avian brain subdivision organization above and below the vestigial ventricle space, with the pallium as a whole consisting of four major cell populations (intercalated pallium, mesopallium, hyper‐nidopallium, and arcopallium) instead of seven (hyperpallium apicale, interstitial hyperpallium apicale, intercalated hyperpallium, hyperpallium densocellare, mesopallium, nidopallium, and arcopallium). We suggest adopting a more streamlined hierarchical naming system that reflects the robust similarities in gene expression, neural connectivity motifs, and function. These findings have important implications for our understanding of overall vertebrate brain evolution.
In 2013, our group examined the expression profiles of 50 genes to develop the continuum hypothesis of avian brain organization. It states that the subdivisions of the dorsal pallium develop continuously with those of the ventral pallium, resulting in a “partial mirror image” organization around the vestigial ventricle divide. However, these claims were challenged due to the small number of genes profiled. The present study uses RNA sequencing to profile the whole transcriptome (~20,000 genes) of the principal subdivisions of the avian telencephalon and confirms the remarkable molecularly similarities between the dorsal and ventral pallium. We recommend adopting a hierarchal nomenclature to reflect these robust molecular similarities.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>33871048</pmid><doi>10.1002/cne.25159</doi><tpages>25</tpages><orcidid>https://orcid.org/0000-0002-6450-7551</orcidid><orcidid>https://orcid.org/0000-0001-8945-7282</orcidid><orcidid>https://orcid.org/0000-0001-6819-2019</orcidid><orcidid>https://orcid.org/0000-0001-8931-5049</orcidid><orcidid>https://orcid.org/0000-0003-4331-9890</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals avian Brain - growth & development Brain - metabolism Brain architecture brain evolution Finches Gene expression Gene Expression Profiling - methods Gene Expression Regulation, Developmental - physiology Genomes Hyperstriatum Male Neural networks Neurogenesis Pallium RNA‐Seq RRIDs SCR_000432 SCR_001905 SCR_003092 SCR_003302 SCR_004277 SCR_010943 SCR_012988 SCR_014583 SCR_015687 SCR_015954 SCR_017036 SCR_018190 SCR_021061 SCR_021062 SCR_021063 Sequence Analysis, RNA - methods Songbirds Synaptic transmission Synaptogenesis Transcriptomes transcriptomics Ventricle Ventricles (cerebral) WGNCA |
title | As above, so below: Whole transcriptome profiling demonstrates strong molecular similarities between avian dorsal and ventral pallial subdivisions |
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