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

Authors

  • Erich D. Jarvis,

    Corresponding author
    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
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  • Jing Yu,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. Norvatis, Institutes for Biomedical Research, Cambridge, Massachusetts
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  • Miriam V. Rivas,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. Durham Veteran's Affairs Medical Center, Durham, North Carolina
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  • Haruhito Horita,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. Faculty of Science, Department of Biological Sciences, Hokkaido University, Sapporo, Hokkaido, Japan
    3. School of Medicine, Hirosaki University, Hirosaki, Aomori, Japan
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  • Gesa Feenders,

    1. Research Center for Neurosensory Sciences & Institut für Biologie und Umweltwissenschaften, University of Oldenburg, Oldenburg, Germany
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  • Osceola Whitney,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
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  • Syrus C. Jarvis,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
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  • Electra R. Jarvis,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
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  • Lubica Kubikova,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. Laboratory of Physiology and Neurobiology of Behavior, Institute of Animal Biochemistry and Genetics, Ivanka pri Dunaji, Slovakia
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  • Ana E.P. Puck,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. Department of Obstetrics and Gynecology, Vanderbilt University Medical Center, Nashville, Tennessee
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  • Connie Siang-Bakshi,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. PO Box 42126, Los Angeles, California
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  • Suzanne Martin,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. Beth Israel Deaconess Medical Center, Boston, Massachusetts
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  • Michael McElroy,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. California Department of Public Health, Oakland, California
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  • Erina Hara,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. Department of Biology, New Mexico State University, Las Cruces, New Mexico
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  • Jason Howard,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
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  • Andreas Pfenning,

    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. Department of Biology, New Mexico State University, Las Cruces, New Mexico
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  • Henrik Mouritsen,

    1. Research Center for Neurosensory Sciences & Institut für Biologie und Umweltwissenschaften, University of Oldenburg, Oldenburg, Germany
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  • Chun-Chun Chen,

    Corresponding author
    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
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    • The last two authors contributed equally in co-supervising the project and conducting experiments. The second and last authors began this project originally as part of their graduate theses.

  • Kazuhiro Wada

    Corresponding author
    1. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina
    2. Faculty of Science, Department of Biological Sciences, Hokkaido University, Sapporo, Hokkaido, Japan
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    • The last two authors contributed equally in co-supervising the project and conducting experiments. The second and last authors began this project originally as part of their graduate theses.


  • This research was supported over a 10-year period by grants from the Human Frontiers in Science Program Young Investigators Award, National Science Foundation Alan T. Waterman Award, the NIH Director's Pioneer Award, NIMH grant R01-MH62083, NIDCD grant R01-DC007218, American Recovery and Reinvestment Act NIH supplement 3DP1OD000448-04S1, and HHMI to Erich D. Jarvis. The Oldenburg-related work (G.F., H.M.) was supported by a VW Nachwuchsgruppe grant and a Lichtenberg-professorship grant to H.M.

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.

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