Abstract
The avian cerebrum has pallial functions similar to those of the mammalian cortex. Although the avian pallium is organized as nuclear structures, and the mammalian cortex as layers, the avian pallium supports cognitive abilities similar to those of many mammals. We recently presented a global view of the pallial organization of birds, based on quantitative analyses of constitutively expressed or behaviorally regulated genes in different pallial cell populations (Jarvis et al. J Comp Neurol 521:3614–3665, 2013; Chen et al. J Comp Neurol 521:3666–3701, 2013). Here we present a shortened synopsis of these articles. The findings of the constitutively expressed genes and known neural connectivity reveal four major cell populations: (1) a primary sensory input population, (2) a secondary intrapallial population, (3) a tertiary intrapallial population, and (4) a quaternary output population. These populations have greater similarities to cell layers of the mammalian cortex than to the amygdala. 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. Each neural cell population contributes portions to columns that control different sensory or motor systems. These findings influence hypotheses on homologies of the avian pallium with other vertebrates.
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References
Belgard TG, Montiel JF, Wang WZ, Garcia-Moreno F, Margulies EH, Ponting CP, Molnar Z (2013) Adult pallium transcriptomes surprise in not reflecting predicted homologies across diverse chicken and mouse pallial sectors. Proc Natl Acad Sci USA 110:13150–13155. doi:10.1073/pnas.1307444110
Bupesh M, Legaz I, Abellan A, Medina L (2011) Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J Comp Neurol 519:1505–1525. doi:10.1002/cne.22581
Butler AB, Reiner A, Karten HJ (2011) Evolution of the amniote pallium and the origins of mammalian neocortex. Ann N Y Acad Sci 1225:14–27. doi:10.1111/j.1749-6632.2011.06006.x
Carney RS, Alfonso TB, Cohen D et al (2006) Cell migration along the lateral cortical stream to the developing basal telencephalic limbic system. J Neurosci 26:11562–11574. doi:10.1523/JNEUROSCI.3092-06.2006
Chen CC, Winkler CM, Pfenning AR, Jarvis ED (2013) Molecular profiling of the developing avian telencephalon: regional timing and brain subdivision continuities. J Comp Neurol. doi:10.1002/cne.23406
Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature (Lond) 395:272–274. doi:10.1038/26216
Feenders G, Liedvogel M, Rivas M et al (2008) Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLoS One 3, e1768. doi:10.1371/journal.pone.0001768
Gao P, Sultan KT, Zhang XJ, Shi SH (2013) Lineage-dependent circuit assembly in the neocortex. Development (Camb) 140:2645–2655. doi:10.1242/dev.087668
Garcia-Lopez M, Abellan A, Legaz I, Rubenstein JL, Puelles L, Medina L (2008) Histogenetic compartments of the mouse centromedial and extended amygdala based on gene expression patterns during development. J Comp Neurol 506:46–74. doi:10.1002/cne.21524
Garcia-Moreno F, Pedraza M, Di Giovannantonio LG, Di Salvio M, Lopez-Mascaraque L, Simeone A, De Carlos JA (2010) A neuronal migratory pathway crossing from diencephalon to telencephalon populates amygdala nuclei. Nat Neurosci 13:680–689. doi:10.1038/nn.2556
Haesler S, Wada K, Nshdejan A, Morrisey EE, Lints T, Jarvis ED, Scharff C (2004) FoxP2 expression in avian vocal learners and non-learners. J Neurosci 24:3164–3175. doi:10.1523/JNEUROSCI.4369-03.2004
Hara E, Kubikova L, Hessler NA, Jarvis ED (2009) Assessing visual requirements for social context-dependent activation of the songbird song system. Proc Biol Sci 276:279–289. doi:10.1098/rspb.2008.1138
Hirata T, Li P, Lanuza GM, Cocas LA, Huntsman MM, Corbin JG (2009) Identification of distinct telencephalic progenitor pools for neuronal diversity in the amygdala. Nat Neurosci 12:141–149. doi:10.1038/nn.2241
Horita H, Wada K, Rivas MV, Hara E, Jarvis ED (2010) The dusp1 immediate early gene is regulated by natural stimuli predominantly in sensory input neurons. J Comp Neurol 518:2873–2901. doi:10.1002/cne.22370
Horita H, Kobayashi M, Liu WC, Oka K, Jarvis ED, Wada K (2012) Specialized motor-driven dusp1 expression in the song systems of multiple lineages of vocal learning birds. PLoS One 7, e42173. doi:10.1371/journal.pone.0042173
Hunt GR, Gray RD (2003) Diversification and cumulative evolution in New Caledonian crow tool manufacture. Proc Biol Sci 270:867–874. doi:10.1098/rspb.2002.2302
Jarvis ED (2004) Learned birdsong and the neurobiology of human language. Ann N Y Acad Sci 1016:749–777. doi:10.1196/annals.1298.038
Jarvis ED, Mello CV (2000) Molecular mapping of brain areas involved in parrot vocal communication. J Comp Neurol 419:1–31
Jarvis ED, Nottebohm F (1997) Motor-driven gene expression. Proc Natl Acad Sci USA 94:4097–4102
Jarvis ED, Ribeiro S, da Silva ML, Ventura D, Vielliard J, Mello CV (2000) Behaviourally driven gene expression reveals song nuclei in hummingbird brain. Nature (Lond) 406:628–632. doi:10.1038/35020570
Jarvis ED, Gunturkun O, Bruce L et al (2005) Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6:151–159. doi:10.1038/nrn1606
Jarvis ED, Yu J, Rivas MV et al (2013) A global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns. J Comp Neurol. doi:10.1002/cne.23404
Karten HJ (1997) Evolutionary developmental biology meets the brain: the origins of mammalian cortex. Proc Natl Acad Sci USA 94:2800–2804
Kubikova L, Wada K, Jarvis ED (2010) Dopamine receptors in a songbird brain. J Comp Neurol 518:741–769. doi:10.1002/cne.22255
Kuenzel WJ, Medina L, Csillag A, Perkel DJ, Reiner A (2011) The avian subpallium: new insights into structural and functional subdivisions occupying the lateral subpallial wall and their embryological origins. Brain Res 1424:67–101. doi:10.1016/j.brainres.2011.09.037
Liedvogel M, Feenders G, Wada K, Troje NF, Jarvis ED, Mouritsen H (2007) Lateralized activation of Cluster N in the brains of migratory songbirds. Eur J Neurosci 25:1166–1173. doi:10.1111/j.1460-9568.2007.05350.x
Lubow RE (1974) High-order concept formation in the pigeon. J Exp Anal Behav 21:475–483
Medina L, Abellan A (2009) Development and evolution of the pallium. Semin Cell Dev Biol 20:698–711. doi:10.1016/j.semcdb.2009.04.008
Medina L, Reiner A (2000) Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:1–12
Mello CV, Clayton DF (1994) Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J Neurosci 14:6652–6666
Mello CV, Clayton DF (1995) Differential induction of the ZENK gene in the avian forebrain and song control circuit after metrazole-induced depolarization. J Neurobiol 26:145–161. doi:10.1002/neu.480260112
Mello CV, Vicario DS, Clayton DF (1992) Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci USA 89:6818–6822
Molnar Z, Cheung AF (2006) Towards the classification of subpopulations of layer V pyramidal projection neurons. Neurosci Res 55:105–115. doi:10.1016/j.neures.2006.02.008
Montiel JF, Molnar Z (2013) The impact of gene expression analysis on evolving views of avian brain organization. J Comp Neurol 521:3604–3613. doi:10.1002/cne.23403
Mouritsen H, Feenders G, Liedvogel M, Wada K, Jarvis ED (2005) Night-vision brain area in migratory songbirds. Proc Natl Acad Sci USA 102:8339–8344. doi:10.1073/pnas.0409575102
Ohtsuki G, Nishiyama M, Yoshida T, Murakami T, Histed M, Lois C, Ohki K (2012) Similarity of visual selectivity among clonally related neurons in visual cortex. Neuron 75:65–72. doi:10.1016/j.neuron.2012.05.023
Pfenning AR, Hara E, Whitney O et al (2014) Convergent transcriptional specializations in the brains of humans and song-learning birds. Science 346:1256846. doi:10.1126/science.1256846
Puelles L, Kuwana E, Puelles E et al (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409–438
Reiner A, Perkel DJ, Bruce LL et al (2004a) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414. doi:10.1002/cne.20118
Reiner A, Perkel DJ, Bruce LL et al (2004b) The avian brain nomenclature forum: terminology for a new century in comparative neuroanatomy. J Comp Neurol 473:E1–E6. doi:10.1002/cne.20119
Soma M, Aizawa H, Ito Y et al (2009) Development of the mouse amygdala as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation. J Comp Neurol 513:113–128. doi:10.1002/cne.21945
Suzuki IK, Kawasaki T, Gojobori T, Hirata T (2012) The temporal sequence of the mammalian neocortical neurogenetic program drives mediolateral pattern in the chick pallium. Dev Cell 22:863–870. doi:10.1016/j.devcel.2012.01.004
Swanson LW (2000) Cerebral hemisphere regulation of motivated behavior. Brain Res 886:113–164
Veenman CL, Wild JM, Reiner A (1995) Organization of the avian “corticostriatal” projection system: a retrograde and anterograde pathway tracing study in pigeons. J Comp Neurol 354:87–126. doi:10.1002/cne.903540108
Velho TA, Pinaud R, Rodrigues PV, Mello CV (2005) Co-induction of activity-dependent genes in songbirds. Eur J Neurosci 22:1667–1678. doi:10.1111/j.1460-9568.2005.04369.x
Vonfersen L, Delius JD (1989) Long-term retention of many visual-patterns by pigeons. Ethology 82:141–155
Wada K, Sakaguchi H, Jarvis ED, Hagiwara M (2004) Differential expression of glutamate receptors in avian neural pathways for learned vocalization. J Comp Neurol 476:44–64. doi:10.1002/cne.20201
Wada K, Howard JT, McConnell P et al (2006) A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc Natl Acad Sci USA 103:15212–15217. doi:10.1073/pnas.0607098103
Wang Y, Brzozowska-Prechtl A, Karten HJ (2010) Laminar and columnar auditory cortex in avian brain. Proc Natl Acad Sci USA 107:12676–12681. doi:10.1073/pnas.1006645107
Watakabe A, Ichinohe N, Ohsawa S, Hashikawa T, Komatsu Y, Rockland KS, Yamamori T (2007) Comparative analysis of layer-specific genes in mammalian neocortex. Cereb Cortex 17:1918–1933. doi:10.1093/cercor/bhl102
Watanabe S, Sakamoto J, Wakita M (1995) Pigeons’ discrimination of paintings by Monet and Picasso. J Exp Anal Behav 63:165–174
Weir AA, Chappell J, Kacelnik A (2002) Shaping of hooks in New Caledonian crows. Science 297:981. doi:10.1126/science.1073433
Yamamoto K, Sun Z, Wang HB, Reiner A (2005) Subpallial amygdala and nucleus taeniae in birds resemble extended amygdala and medial amygdala in mammals in their expression of markers of regional identity. Brain Res Bull 66:341–347. doi:10.1016/j.brainresbull.2005.02.016
Yu YC, Bultje RS, Wang X, Shi SH (2009) Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature (Lond) 458:501–504. doi:10.1038/nature07722
Zapka M, Heyers D, Hein CM et al (2009) Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature (Lond) 461:1274–1277. doi:10.1038/nature08528
Zapka M, Heyers D, Liedvogel M, Jarvis ED, Mouritsen H (2010) Night-time neuronal activation of Cluster N in a day- and night-migrating songbird. Eur J Neurosci 32:619–624. doi:10.1111/j.1460-9568.2010.07311.x
Zhang G, Li C, Li Q et al (2014) Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346:1311–1320. doi:10.1126/science.1251385
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Wada, K., Chen, CC., Jarvis, E.D. (2017). Molecular Profiling Reveals Insight into Avian Brain Organization and Functional Columnar Commonalities with Mammals. In: Shigeno, S., Murakami, Y., Nomura, T. (eds) Brain Evolution by Design. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56469-0_11
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