Global view of the functional molecular organization of the avian cerebrum: Mirror images and functional columns

ABSTRACT Based on quantitative cluster analyses of 52 constitutively expressed or behaviorally regulated genes in 23 brain regions, we present a global view of telencephalic organization of birds. The patterns of constitutively expressed genes revealed a partial mirror image organization of three ma...

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Veröffentlicht in:Journal of comparative neurology (1911) 2013-11, Vol.521 (16), p.3614-3665
Hauptverfasser: Jarvis, Erich D., Yu, Jing, Rivas, Miriam V., Horita, Haruhito, Feenders, Gesa, Whitney, Osceola, Jarvis, Syrus C., Jarvis, Electra R., Kubikova, Lubica, Puck, Ana E.P., Siang-Bakshi, Connie, Martin, Suzanne, McElroy, Michael, Hara, Erina, Howard, Jason, Pfenning, Andreas, Mouritsen, Henrik, Chen, Chun-Chun, Wada, Kazuhiro
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container_end_page 3665
container_issue 16
container_start_page 3614
container_title Journal of comparative neurology (1911)
container_volume 521
creator Jarvis, Erich D.
Yu, Jing
Rivas, Miriam V.
Horita, Haruhito
Feenders, Gesa
Whitney, Osceola
Jarvis, Syrus C.
Jarvis, Electra R.
Kubikova, Lubica
Puck, Ana E.P.
Siang-Bakshi, Connie
Martin, Suzanne
McElroy, Michael
Hara, Erina
Howard, Jason
Pfenning, Andreas
Mouritsen, Henrik
Chen, Chun-Chun
Wada, Kazuhiro
description ABSTRACT Based on quantitative cluster analyses of 52 constitutively expressed or behaviorally regulated genes in 23 brain regions, we present a global view of telencephalic organization of birds. The patterns of constitutively expressed genes revealed a partial mirror image organization of three major cell populations that wrap above, around, and below the ventricle and adjacent lamina through the mesopallium. The patterns of behaviorally regulated genes revealed functional columns of activation across boundaries of these cell populations, reminiscent of columns through layers of the mammalian cortex. The avian functionally regulated columns were of two types: those above the ventricle and associated mesopallial lamina, formed by our revised dorsal mesopallium, hyperpallium, and intercalated hyperpallium; and those below the ventricle, formed by our revised ventral mesopallium, nidopallium, and intercalated nidopallium. Based on these findings and known connectivity, we propose that the avian pallium has four major cell populations similar to those in mammalian cortex and some parts of the amygdala: 1) a primary sensory input population (intercalated pallium); 2) a secondary intrapallial population (nidopallium/hyperpallium); 3) a tertiary intrapallial population (mesopallium); and 4) a quaternary output population (the arcopallium). Each population contributes portions to columns that control different sensory or motor systems. We suggest that this organization of cell groups forms by expansion of contiguous developmental cell domains that wrap around the lateral ventricle and its extension through the middle of the mesopallium. We believe that the position of the lateral ventricle and its associated mesopallium lamina has resulted in a conceptual barrier to recognizing related cell groups across its border, thereby confounding our understanding of homologies with mammals. J. Comp. Neurol. 521:3614–3665, 2013. © 2013 Wiley Periodicals, Inc. Using bioinformatic profiling of constitutive and behaviorally regulated genes, we propose a novel view of avian brain organization, which group most of the telencephalon into four major cell populations of which three have mirror image counterparts above and below the lateral ventricle that function in columns for sensory‐motor systems analogous to the mammalian brain.
doi_str_mv 10.1002/cne.23404
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The patterns of constitutively expressed genes revealed a partial mirror image organization of three major cell populations that wrap above, around, and below the ventricle and adjacent lamina through the mesopallium. The patterns of behaviorally regulated genes revealed functional columns of activation across boundaries of these cell populations, reminiscent of columns through layers of the mammalian cortex. The avian functionally regulated columns were of two types: those above the ventricle and associated mesopallial lamina, formed by our revised dorsal mesopallium, hyperpallium, and intercalated hyperpallium; and those below the ventricle, formed by our revised ventral mesopallium, nidopallium, and intercalated nidopallium. Based on these findings and known connectivity, we propose that the avian pallium has four major cell populations similar to those in mammalian cortex and some parts of the amygdala: 1) a primary sensory input population (intercalated pallium); 2) a secondary intrapallial population (nidopallium/hyperpallium); 3) a tertiary intrapallial population (mesopallium); and 4) a quaternary output population (the arcopallium). Each population contributes portions to columns that control different sensory or motor systems. We suggest that this organization of cell groups forms by expansion of contiguous developmental cell domains that wrap around the lateral ventricle and its extension through the middle of the mesopallium. We believe that the position of the lateral ventricle and its associated mesopallium lamina has resulted in a conceptual barrier to recognizing related cell groups across its border, thereby confounding our understanding of homologies with mammals. J. Comp. Neurol. 521:3614–3665, 2013. © 2013 Wiley Periodicals, Inc. Using bioinformatic profiling of constitutive and behaviorally regulated genes, we propose a novel view of avian brain organization, which group most of the telencephalon into four major cell populations of which three have mirror image counterparts above and below the lateral ventricle that function in columns for sensory‐motor systems analogous to the mammalian brain.</description><identifier>ISSN: 0021-9967</identifier><identifier>EISSN: 1096-9861</identifier><identifier>DOI: 10.1002/cne.23404</identifier><identifier>PMID: 23818122</identifier><language>eng</language><publisher>United States: Blackwell Publishing Ltd</publisher><subject>Amygdala ; Animals ; basal ganglia ; Birds - anatomy &amp; histology ; brain evolution ; brain organization ; brain pathways ; Cell Count ; Cerebrum - anatomy &amp; histology ; Cerebrum - metabolism ; claustrum ; cortex ; forebrain ; Gene Expression ; Imaging, Three-Dimensional ; immediate early genes ; motor behavior ; Nerve Tissue Proteins - genetics ; Nerve Tissue Proteins - metabolism ; neural activity ; Neuroimaging ; Neurons - metabolism ; neurotransmitter receptors ; pallidum ; pallium ; primary sensory ; Species Specificity ; striatum</subject><ispartof>Journal of comparative neurology (1911), 2013-11, Vol.521 (16), p.3614-3665</ispartof><rights>Copyright © 2013 The Authors. The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.</rights><rights>Copyright © 2013 Wiley Periodicals, Inc.</rights><rights>2013 Wiley Periodicals, Inc. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5804-427e125b07a7fd4757b4f805d30073bb7eff7d6d2dbf8d7b168a15294d45964f3</citedby><cites>FETCH-LOGICAL-c5804-427e125b07a7fd4757b4f805d30073bb7eff7d6d2dbf8d7b168a15294d45964f3</cites></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.23404$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fcne.23404$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23818122$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jarvis, Erich D.</creatorcontrib><creatorcontrib>Yu, Jing</creatorcontrib><creatorcontrib>Rivas, Miriam V.</creatorcontrib><creatorcontrib>Horita, Haruhito</creatorcontrib><creatorcontrib>Feenders, Gesa</creatorcontrib><creatorcontrib>Whitney, Osceola</creatorcontrib><creatorcontrib>Jarvis, Syrus C.</creatorcontrib><creatorcontrib>Jarvis, Electra R.</creatorcontrib><creatorcontrib>Kubikova, Lubica</creatorcontrib><creatorcontrib>Puck, Ana E.P.</creatorcontrib><creatorcontrib>Siang-Bakshi, Connie</creatorcontrib><creatorcontrib>Martin, Suzanne</creatorcontrib><creatorcontrib>McElroy, Michael</creatorcontrib><creatorcontrib>Hara, Erina</creatorcontrib><creatorcontrib>Howard, Jason</creatorcontrib><creatorcontrib>Pfenning, Andreas</creatorcontrib><creatorcontrib>Mouritsen, Henrik</creatorcontrib><creatorcontrib>Chen, Chun-Chun</creatorcontrib><creatorcontrib>Wada, Kazuhiro</creatorcontrib><title>Global view of the functional molecular organization of the avian cerebrum: Mirror images and functional columns</title><title>Journal of comparative neurology (1911)</title><addtitle>J. Comp. Neurol</addtitle><description>ABSTRACT Based on quantitative cluster analyses of 52 constitutively expressed or behaviorally regulated genes in 23 brain regions, we present a global view of telencephalic organization of birds. The patterns of constitutively expressed genes revealed a partial mirror image organization of three major cell populations that wrap above, around, and below the ventricle and adjacent lamina through the mesopallium. The patterns of behaviorally regulated genes revealed functional columns of activation across boundaries of these cell populations, reminiscent of columns through layers of the mammalian cortex. The avian functionally regulated columns were of two types: those above the ventricle and associated mesopallial lamina, formed by our revised dorsal mesopallium, hyperpallium, and intercalated hyperpallium; and those below the ventricle, formed by our revised ventral mesopallium, nidopallium, and intercalated nidopallium. Based on these findings and known connectivity, we propose that the avian pallium has four major cell populations similar to those in mammalian cortex and some parts of the amygdala: 1) a primary sensory input population (intercalated pallium); 2) a secondary intrapallial population (nidopallium/hyperpallium); 3) a tertiary intrapallial population (mesopallium); and 4) a quaternary output population (the arcopallium). Each population contributes portions to columns that control different sensory or motor systems. We suggest that this organization of cell groups forms by expansion of contiguous developmental cell domains that wrap around the lateral ventricle and its extension through the middle of the mesopallium. We believe that the position of the lateral ventricle and its associated mesopallium lamina has resulted in a conceptual barrier to recognizing related cell groups across its border, thereby confounding our understanding of homologies with mammals. J. Comp. Neurol. 521:3614–3665, 2013. © 2013 Wiley Periodicals, Inc. Using bioinformatic profiling of constitutive and behaviorally regulated genes, we propose a novel view of avian brain organization, which group most of the telencephalon into four major cell populations of which three have mirror image counterparts above and below the lateral ventricle that function in columns for sensory‐motor systems analogous to the mammalian brain.</description><subject>Amygdala</subject><subject>Animals</subject><subject>basal ganglia</subject><subject>Birds - anatomy &amp; histology</subject><subject>brain evolution</subject><subject>brain organization</subject><subject>brain pathways</subject><subject>Cell Count</subject><subject>Cerebrum - anatomy &amp; histology</subject><subject>Cerebrum - metabolism</subject><subject>claustrum</subject><subject>cortex</subject><subject>forebrain</subject><subject>Gene Expression</subject><subject>Imaging, Three-Dimensional</subject><subject>immediate early genes</subject><subject>motor behavior</subject><subject>Nerve Tissue Proteins - genetics</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>neural activity</subject><subject>Neuroimaging</subject><subject>Neurons - metabolism</subject><subject>neurotransmitter receptors</subject><subject>pallidum</subject><subject>pallium</subject><subject>primary sensory</subject><subject>Species Specificity</subject><subject>striatum</subject><issn>0021-9967</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNqNkc1u1DAUhS0EokNhwQugSGxgkfb6J7HDAglGJUWUsuFnaTmJPXVx7MGeTClPj6fTGRUkJFaWfL776doHoacYjjAAOe69PiKUAbuHZhiaumxEje-jWc5w2TQ1P0CPUroEgKah4iE6IFRggQmZoWXrQqdcsbb6qgimWF3owky-X9ng8_UYnO4np2IR4kJ5-0ttgh2o1lb5otdRd3EaXxUfbYwhFnZUC50K5Ye7qj64afTpMXpglEv6ye15iL68O_k8Py3PPrXv52_Oyr4SwEpGuMak6oArbgbGK94xI6AaKACnXce1MXyoBzJ0Rgy8w7VQuCING1jV1MzQQ_R6611O3aiHXvtVVE4uY94uXsugrPwz8fZCLsJaMswqwlgWvLgVxPBj0mklR5t67ZzyOkxJ4sxQTgSI_0CpqDiGusno87_QyzDF_D83FCcAmGyol1uqjyGlqM1-bwxyU7nMlcubyjP77O5D9-Su4wwcb4Er6_T1v01yfn6yU5bbCZtW-ud-QsXvsuaUV_LbeSt5-_a0_QofJKe_AcoHxWo</recordid><startdate>201311</startdate><enddate>201311</enddate><creator>Jarvis, Erich D.</creator><creator>Yu, Jing</creator><creator>Rivas, Miriam V.</creator><creator>Horita, Haruhito</creator><creator>Feenders, Gesa</creator><creator>Whitney, Osceola</creator><creator>Jarvis, Syrus C.</creator><creator>Jarvis, Electra R.</creator><creator>Kubikova, Lubica</creator><creator>Puck, Ana E.P.</creator><creator>Siang-Bakshi, Connie</creator><creator>Martin, Suzanne</creator><creator>McElroy, Michael</creator><creator>Hara, Erina</creator><creator>Howard, Jason</creator><creator>Pfenning, Andreas</creator><creator>Mouritsen, Henrik</creator><creator>Chen, Chun-Chun</creator><creator>Wada, Kazuhiro</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>24P</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></search><sort><creationdate>201311</creationdate><title>Global view of the functional molecular organization of the avian cerebrum: Mirror images and functional columns</title><author>Jarvis, Erich D. ; 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Using bioinformatic profiling of constitutive and behaviorally regulated genes, we propose a novel view of avian brain organization, which group most of the telencephalon into four major cell populations of which three have mirror image counterparts above and below the lateral ventricle that function in columns for sensory‐motor systems analogous to the mammalian brain.</abstract><cop>United States</cop><pub>Blackwell Publishing Ltd</pub><pmid>23818122</pmid><doi>10.1002/cne.23404</doi><tpages>52</tpages><oa>free_for_read</oa></addata></record>
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subjects Amygdala
Animals
basal ganglia
Birds - anatomy & histology
brain evolution
brain organization
brain pathways
Cell Count
Cerebrum - anatomy & histology
Cerebrum - metabolism
claustrum
cortex
forebrain
Gene Expression
Imaging, Three-Dimensional
immediate early genes
motor behavior
Nerve Tissue Proteins - genetics
Nerve Tissue Proteins - metabolism
neural activity
Neuroimaging
Neurons - metabolism
neurotransmitter receptors
pallidum
pallium
primary sensory
Species Specificity
striatum
title Global view of the functional molecular organization of the avian cerebrum: Mirror images and functional columns
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