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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Veröffentlicht in:Journal of comparative neurology (1911) 2021-08, Vol.529 (12), p.3222-3246
Hauptverfasser: Gedman, Gregory, Haase, Bettina, Durieux, Gillian, Biegler, Matthew T., Fedrigo, Olivier, Jarvis, Erich D.
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container_issue 12
container_start_page 3222
container_title Journal of comparative neurology (1911)
container_volume 529
creator Gedman, Gregory
Haase, Bettina
Durieux, Gillian
Biegler, Matthew T.
Fedrigo, Olivier
Jarvis, Erich D.
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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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><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 &amp; Sons, Inc</publisher><subject>Animals ; avian ; Brain - growth &amp; 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”). 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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. 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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. 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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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