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

Journal of Comparative Neurology

Volumn 521, Issue 16, 2013, Pages 3614-3665

  Jarvis, Erich D ^a   Yu, Jing ^a,b   Rivas, Miriam V ^a,c   Horita, Haruhito ^a,d,e   Feenders, Gesa ^f   Whitney, Osceola ^a   Jarvis, Syrus C ^a   Jarvis, Electra R ^a   Kubikova, Lubica ^a,g   Puck, Ana E P ^a,h   Siang Bakshi, Connie ^a,i   Martin, Suzanne ^a,j   McElroy, Michael ^a,k   Hara, Erina ^a,l   Howard, Jason ^a   Pfenning, Andreas ^a   Mouritsen, Henrik ^f   Chen, Chun Chun ^a   Wada, Kazuhiro ^a,d  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b Institutes for Biomedical Research   (United States)

^c DURHAM VA MEDICAL CENTER   (United States)

^d HOKKAIDO UNIVERSITY   (Japan)

^e HIROSAKI UNIVERSITY   (Japan)

^f UNIVERSITY OF OLDENBURG   (Germany)

^g Institute of Animal Biochemistry and Genetics   (Slovakia)

^h VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

ⁱ Beth Israel Deaconess Medical Center ^*  (United States)

^j BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^k California Department of Public Health   (United States)

^l NEW MEXICO STATE UNIVERSITY   (United States)

more..

Author keywords

Amygdala; Basal ganglia; Brain evolution; Brain organization; Brain pathways; Claustrum; Cortex; Forebrain; Immediate early genes; Motor behavior; Neural activity; Neurotransmitter receptors; Pallidum; Pallium; Primary sensory; Striatum

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 2; DOPAMINE 1A RECEPTOR; DOPAMINE 1B RECEPTOR; DOPAMINE 1C RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; DOPAMINE RECEPTOR; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 4; KAINIC ACID RECEPTOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR 8; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2D; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 3A; SEMAPHORIN; SEMAPHORIN 6A; TRANSCRIPTION FACTOR FOXP2; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIRD; BRAIN CORTEX; BRAIN FUNCTION; BRAIN REGION; BRAIN VENTRICLE; CELL POPULATION; CELLULAR DISTRIBUTION; CLUSTER ANALYSIS; COMPARATIVE ANATOMY; CONTROLLED STUDY; DOVE; GALLIFORMES; GENE EXPRESSION; HUMMINGBIRD; HYPERPALLIUM; INTERCALATED PALLIUM; LATERAL BRAIN VENTRICLE; MAMMAL; MESOPALLIUM; MOTOR SYSTEM; NIDOPALLIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PARROT; PIGEON; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RUFOUS BREASTED HERMIT; SENSORY SYSTEM; SONGBIRD; TELENCEPHALON;

AMYGDALA; BASAL GANGLIA; BRAIN EVOLUTION; BRAIN ORGANIZATION; BRAIN PATHWAYS; CLAUSTRUM; CORTEX; FOREBRAIN; IMMEDIATE EARLY GENES; MOTOR BEHAVIOR; NEURAL ACTIVITY; NEUROTRANSMITTER RECEPTORS; PALLIDUM; PALLIUM; PRIMARY SENSORY; STRIATUM;

ANIMALS; BIRDS; CELL COUNT; CEREBRUM; GENE EXPRESSION; IMAGING, THREE-DIMENSIONAL; NERVE TISSUE PROTEINS; NEUROIMAGING; NEURONS; SPECIES SPECIFICITY;

EID: 84888324608     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23404     Document Type: Article

References (102)

1. Abellan A, Medina L. 2009. Subdivisions and derivatives of the chicken subpallium based on expression of LIM and other regulatory genes and markers of neuron subpopulations during development. J Comp Neurol 515: 465-501.
2. Abellan A, Menuet A, Dehay C, Medina L, Retaux S. 2009. Differential expression of LIM-homeodomain factors in Cajal-Retzius cells of primates, rodents, and birds. Cereb Cortex 20:1788-1798.
3. Ariëns Kappers CU, Huber CG, Crosby EC. 1936. Comparative Anatomy of the Nervous System of Vertebrates, Including Man. New York: Reprinted 1960, Hafner.
4. Aboitiz F. 2011. Genetic and developmental homology in amniote brains. Toward conciliating radical views of brain evolution. Brain Res Bull 84:125-136.
5. Atoji Y, Karim MR. 2012. Expression of the neocortical marker, RORb, in the entopallium and field L2 of adult chicken. Neurosci Lett 521:119-124.
6. Atoji Y, Wild JM. 2005. Afferent and efferent connections of the dorsolateral corticoid area and a comparison with connections of the temporo-parieto-occipital area in the pigeon (Columba livia). J Comp Neurol 485:165-182.
7. Atoji Y, Wild JM. 2006. Anatomy of the avian hippocampal formation. Rev Neurosci 17:3-15.
8. Biedl T, Brejova B, Demaine ED, Hamel AM, Vinar T. 2001. Optimal arrangement of leaves in the tree representing hierarchical clustering of gene expression data. University of Waterloo, Canada.
9. 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.
10. Butler AB, Molnar Z. 2002. Development and evolution of the collopallium in amniotes: a new hypothesis of field homology. Brain Res Bull 57:475-479.
11. 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.
12. Carney RS, Alfonso TB, Cohen D, Dai H, Nery S, Stoica B, Slotkin J, Bregman BS, Fishell G, Corbin JG. 2006. Cell migration along the lateral cortical stream to the developing basal telencephalic limbic system. J Neurosci 26: 11562-11574.
13. Chen CC, Wada K, Jarvis ED. 2012. Radioactive in situ hybridization for detecting diverse gene expression patterns in tissue. J Vis Exp (62). doi:pii: 3764.10.3791/3764.
14. 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 (this issue).
15. Chew SJ, Mello C, Nottebohm F, Jarvis E, Vicario DS. 1995. Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain. Proc Natl Acad Sci U S A 92:3406-3410.
16. Deussing JM, Wurst W. 2007. Amygdala and neocortex: common origins and shared mechanisms. Nat Neurosci 10: 1081-1082.
17. Doupe AJ, Perkel DJ, Reiner A, Stern EA. 2005. Birdbrains could teach basal ganglia research a new song. Trends Neurosci 28:353-363.
18. Dubbeldam JL, Den Boer-Visser AM. 1994. Organization feeding 'of circuits' in birds: pathways for the control of beak and head movements. Eur J Morphol 32:127-133.
19. Dubbeldam JL, van Ommen MH, den Boer-Visser AM. 1999. Immunohistochemical characterization of forebrain areas in the collared dove (Streptopelia Decaocto). Eur J Morphol 37:134-138.
20. Dugas-Ford J, Rowell JJ, Ragsdale CW. 2012. Cell-type homologies and the origins of the neocortex. Proc Natl Acad Sci U S A 109:16974-16979.
21. Edinger L. 1885. The anatomy of the central nervous system of man and of vertebrates in general: 1896 Fifth German ed., English published 1899; Translators W.S. Hall, P.L. Holland, E.P. Carlton. Philadelphia: F.A. Davis.
22. Edinger L. 1908. The relations of comparative anatomy to comparative psychology. Comp Neurol Psychol 18:437-457.
23. Elmore KL, Richman MB. 2001. Euclidean distance as a similarity metric for pricincple component analysis. Month Weather Rev 129:540-549.
24. Feenders G, Liedvogel M, Rivas M, Zapka M, Horita H, Hara E, Wada K, Mouritsen H, Jarvis ED. 2008. Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLoS ONE 3:e1768.
25. Frost BJ, Mouritsen H. 2006. The neural mechanisms of long distance animal navigation. Curr Opin Neurobiol 16:481-488.
26. 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.
27. 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.
28. Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T. 2008. A phylogenomic study of birds reveals their evolutionary history. Science 320:1763-1768.
29. Haesler S, Wada K, Nshdejan A, Morrisey EE, Lints T, Jarvis ED, ScharffC. 2004. FoxP2 expression in avian vocal learners and non-learners. J Neurosci 24:3164-3175.
30. 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.
31. Hara E, Rivas MV, Ward JM, Okanoya K, Jarvis ED. 2012. Convergent differential regulation of parvalbumin in the brains of vocal learners. PLoS ONE 7:e29457.
32. Heyers D, Manns M, Luksch H, Gunturkun O, Mouritsen H. 2007. A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS ONE 2:e937.
33. 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.
34. Holliday IE. 2012.Kolmogorov-Smirnov Test (v1.0.3) Free Statistics Software (v1.1.23-r7).Office for Research Development and Education.
35. 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.
36. 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.
37. Jarvis ED, Mello CV. 2000. Molecular mapping of brain areas involved in parrot vocal communication. J Comp Neurol 419:1-31.
38. Jarvis ED, Nottebohm F. 1997. Motor-driven gene expression. Proc Natl Acad Sci U S A 94:4097-4102.
39. Jarvis ED, Schwabl H, Ribeiro S, Mello CV. 1997. Brain gene regulation by territorial singing behavior in freely ranging songbirds. Neuroreport 8:2073-2077.
40. Jarvis ED, ScharffC, Grossman MR, Ramos JA, Nottebohm F. 1998. For whom the bird sings: context-dependent gene expression. Neuron 21:775-788.
41. 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 406:628-632.
42. Jarvis ED, Gunturkun O, Bruce L, Csillag A, Karten H, Kuenzel W, Medina L, Paxinos G, Perkel DJ, Shimizu T, Striedter G, Wild JM, Ball GF, Dugas-Ford J, Durand SE, Hough GE, Husband S, Kubikova L, Lee DW, Mello CV, Powers A, Siang C, Smulders TV, Wada K, White SA, Yamamoto K, Yu J, Reiner A, Butler AB. 2005. Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6:151-159.
43. Karten HJ. 1991. Homology and evolutionary origins of the 'neocortex'. Brain Behav Evol 38:264-272.
44. Karten HJ, Hodos W. 1967. A stereotaxic atlas of the brain of the pigeon (Columba livia). Baltimore: Johns Hopkins University Press.
45. Karten HJ, Agnieszka B-P, Prechtl J, Wang H, Mitra PP. 2008.3 Digital atlas of the zebra finch brain (Taeniopygia guttata): a dimensional and high resolution photo atlas. Washington, DC: Society for Neuroscience.
46. Kimpo RR, Doupe AJ. 1997. FOS is induced by singing in distinct neuronal populations in a motor network. Neuron 18:315-325.
47. Kubikova L, Wada K, Jarvis ED. 2010. Dopamine receptors in a songbird brain. J Comp Neurol 518:741-769.
48. Kuenzel WJ, Masson M. 1988. A stereotaxic atlas of the brain of the chick (Gallus domesticus). Baltimore: Johns Hopkins University Press.
49. 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.
50. Li X, Wang XJ, Tannenhauser J, Podell S, Mukherjee P, Hertel M, Biane J, Masuda S, Nottebohm F, Gaasterland T. 2007. Genomic resources for songbird research and their use in characterizing gene expression during brain development. Proc Natl Acad Sci U S A 104:6834-6839.
51. 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.
52. Lovell PV, Clayton DF, Replogle KL, Mello CV. 2008. Birdsong "transcriptomics": neurochemical specializations of the oscine song system. PLoS ONE 3:e3440.
53. Medina L, Abellan A. 2009. Development and evolution of the pallium. Semin Cell Dev Biol 20:698-711.
54. Medina L, Reiner A. 2000. Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:1-12.
55. Medina L, Bupesh M, Abellan A. 2011. Contribution of genoarchitecture to understanding forebrain evolution and development, with particular emphasis on the amygdala. Brain Behav Evol 78:216-236.
56. 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.
57. 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.
58. Mello CV, Vicario DS, Clayton DF. 1992. Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci U S A 89:6818-6822.
59. Molnar Z, Butler AB. 2002. Neuronal changes during forebrain evolution in amniotes: an evolutionary developmental perspective. Prog Brain Res 136:21-38.
60. Molnar Z, Cheung AF. 2006. Towards the classification of subpopulations of layer V pyramidal projection neurons. Neurosci Res 55:105-115.
61. Mouritsen H, Feenders G, Liedvogel M, Wada K, Jarvis ED. 2005. Night-vision brain area in migratory songbirds. Proc Natl Acad Sci U S A 102:8339-8344.
62. Nixdorf-Bergweiler BE, Bischof H-J. 2007. A stereotaxic atlas of the brain of the zebra finch, Taeniopygia guttata. Bethesda, MD: National Center for Biotechnology Information (US).
63. Nomura T, Hattori M, Osumi N. 2009. Reelin, radial fibers and cortical evolution: insights from comparative analysis of the mammalian and avian telencephalon. Dev Growth Differ 51:287-297.
64. Pettigrew JD. 1979. Binocular visual processing in the owl's telencephalon. Proc R Soc Lond B Biol Sci 204:435-454.
65. Puelles L. 2011. Pallio-pallial tangential migrations and growth signaling: new scenario for cortical evolution. Brain Behav Evol 78:108-127.
66. Puelles L, Kuwana E, Puelles E, Rubenstein JLR. 1999. Comparison of the mammalian and avian telencephalon from the perspective of gene expression data. Eur J Morphol 37:139-150.
67. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein J. 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.
68. Puelles E, Martinez-de-la-Torre M, Paxinos G, Watson C, Martinez S. 2008. The chick brain in stereotaxic coordinates: an atlas featuring neuromeric subdivisions and mammalian homologies. New York: Academic Press.
69. Reiner A, Perkel DJ, Bruce L, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter GF, Wild M, Ball GF, Durand S, Güntürkün O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED. 2004a. The Avian Brain Nomenclature Forum: a new century in comparative neuroanatomy. J Comp Neurol 473:E1-E6.
70. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Guturkun O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED. 2004b. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414.
71. Remedios R, Huilgol D, Saha B, Hari P, Bhatnagar L, Kowalczyk T, Hevner RF, Suda Y, Aizawa S, Ohshima T, Stoykova A, Tole S. 2007. A stream of cells migrating from the caudal telencephalon reveals a link between the amygdala and neocortex. Nat Neurosci 10:1141-1150.
72. Replogle K, Arnold AP, Ball GF, Band M, Bensch S, Brenowitz EA, Dong S, Drnevich J, Ferris M, George JM, Gong G, Hasselquist D, Hernandez AG, Kim R, Lewin HA, Liu L, Lovell PV, Mello CV, Naurin S, Rodriguez-Zas S, Thimmapuram J, Wade J, Clayton DF. 2008. The Songbird Neurogenomics (SoNG) initiative: community-based tools and strategies for study of brain gene function and evolution. BMC Genomics 9:131.
73. Shimizu T, Bowers AN. 1999. Visual circuits of the avian telencephalon: evolutionary implications. Behav Brain Res 98:183-191.
74. Shimizu T, Karten HJ. 1990. Immunohistochemical analysis of the visual wulst of the pigeon (Columba livia). J Comp Neurol 300:346-369.
75. Shimizu T, Cox K, Karten HJ. 1995. Intratelencephalic projections of the visual wulst in pigeons (Columba livia). J Comp Neurol 359:551-572.
76. Shimizu T, Patton TB, Husband SA. 2010. Avian visual behavior and the organization of the telencephalon. Brain Behav Evol 75:204-217.
77. Smith-Fernandez AS, Pieau C, Reperant J, Boncinelli E, Wassef M. 1998. Expression of the Emx-1 and Dlx-1 homeobox genes define three molecularly distinct domains in the telencephalon of mouse, chick, turtle and frog embryos: implications for the evolution of telencephalic subdivisions in amniotes. Development 125:2099-2111.
78. Soderstrom K, Tian Q, Valenti M, Di Marzo V. 2004. Endocannabinoids link feeding state and auditory perceptionrelated gene expression. J Neurosci 24:10013-10021.
79. Soma M, Aizawa H, Ito Y, Maekawa M, Osumi N, Nakahira E, Okamoto H, Tanaka K, Yuasa S. 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.
80. Suh A, Paus M, Kiefmann M, Churakov G, Franke FA, Brosius J, Kriegs JO, Schmitz J. 2011. Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nat Commun 2:443.
81. Suzuki R, Shimodaira H. 2006. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540-1542.
82. 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.
83. Swanson LW. 2000. Cerebral hemisphere regulation of motivated behavior. Brain Res 886:113-164.
84. Tanaka DH, Oiwa R, Sasaki E, Nakajima K. 2011. Changes in cortical interneuron migration contribute to the evolution of the neocortex. Proc Natl Acad Sci U S A 108:8015-8020.
85. Tramontina F, Tramontina AC, Souza DF, Leite MC, Gottfried C, Souza DO, Wofchuk ST, Goncalves CA. 2006. Glutamate uptake is stimulated by extracellular S100B in hippocampal astrocytes. Cell Mol Neurobiol 26:81-86.
86. Uchida S, Imagawa T, Shinozaki A, Furue M, Ali S, Hosaka Y, Uehara M. 2010. Distribution of astroglial lineage cells in developing chicken telencephalon from embryo to young chick. J Vet Med Sci 72:1597-1602.
87. Vates GE, Broome BM, Mello CV, Nottebohm F. 1996. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches. J Comp Neurol 366:613-642.
88. 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.
89. Velho TA, Pinaud R, Rodrigues PV, Mello CV. 2005. Co-induction of activity-dependent genes in songbirds. Eur J Neurosci 22:1667-1678.
90. Vyssotski AL, Dell'Omo G, Dell'Ariccia G, Abramchuk AN, Serkov AN, Latanov AV, Loizzo A, Wolfer DP, Lipp HP. 2009. EEG responses to visual landmarks in flying pigeons. Curr Biol 19:1159-1166.
91. 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.
92. Wada K, Howard JT, McConnell P, Whitney O, Lints T, Rivas MV, Horita H, Patterson MA, White SA, ScharffC, Haesler S, Zhao S, Sakaguchi H, Hagiwara M, Shiraki T, Hirozane-Kishikawa T, Skene P, Hayashizaki Y, Carninci P, Jarvis ED. 2006. A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc Natl Acad Sci U S A 103:15212-15217.
93. Wang Y, Brzozowska-Prechtl A, Karten HJ. 2010. Laminar and columnar auditory cortex in avian brain. Proc Natl Acad Sci U S A 107:12676-12681.
94. 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.
95. Wild JM, Williams MN. 1999. Rostral wulst of passerine birds: II. Intratelencephalic projections to nuclei associated with the auditory and song systems. J Comp Neurol 413: 520-534.
96. Wild JM, Williams MN. 2000. Rostral wulst in passerine birds. I. Origin, course, and terminations of an avian pyramidal tract. J Comp Neurol 416:429-450.
97. Xu J, Liu Y, Zhang GY. 2008. Neuroprotection of GluR5-containing kainate receptor activation against ischemic brain injury through decreasing tyrosine phosphorylation of N-methyl-D-aspartate receptors mediated by Src kinase. J Biol Chem 283:29355-29366.
98. Yamamoto K, Reiner A. 2005. Distribution of the limbic system-associated membrane protein (LAMP) in pigeon forebrain and midbrain. J Comp Neurol 486:221-242.
99. 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.
100. Zapka M, Heyers D, Hein CM, Engels S, Schneider NL, Hans J, Weiler S, Dreyer D, Kishkinev D, Wild JM, Mouritsen H. 2009. Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461: 1274-1277.
101. 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.
102. Zeigler HP, Marler P (eds). 2004. Behavioral neurobiology of birdsong. New York Academy of Science.