The dusp1 immediate early gene is regulated by natural stimuli predominantly in sensory input neurons

Journal of Comparative Neurology

Volumn 518, Issue 14, 2010, Pages 2873-2901

  Horita, Haruhito ^a,b   Wada, Kazuhiro ^c   Rivas, Miriam V ^a   Hara, Erina ^a,d   Jarvis, Erich D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b KEIO UNIVERSITY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d CHIBA UNIVERSITY   (Japan)

Author keywords

auditory; bird; brain evolution; brain organization; cl100; hummingbird; hvh1; mkp 1; mkp1; motor behavior; motor pathways; neural activity; parrot; primary sensory; ptpn10; ring dove; somatosensory; songbird; vision; ZENK

Indexed keywords

COMPLEMENTARY DNA; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BIRD; BRAIN CORTEX; BRAIN NERVE CELL; FOREBRAIN; GENE EXPRESSION; IMMEDIATE EARLY GENE; IN SITU HYBRIDIZATION; MOTOR PERFORMANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REGULATORY MECHANISM; SENSORY NERVE CELL; SENSORY STIMULATION; SINGING; SOMATOSENSORY SYSTEM; SONGBIRD; TELENCEPHALON; THALAMUS; VISUAL STIMULATION;

ANIMALS; AUDITORY PERCEPTION; AVIAN PROTEINS; BRAIN; COLUMBIDAE; DUAL SPECIFICITY PHOSPHATASE 1; EARLY GROWTH RESPONSE PROTEIN 1; GENE EXPRESSION REGULATION; MALE; MELOPSITTACUS; MICE; MOTOR ACTIVITY; NEURONS, AFFERENT; SONGBIRDS; SPECIES SPECIFICITY; TELENCEPHALON; THALAMUS; VISUAL PERCEPTION;

EID: 77954576982     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22370     Document Type: Article

References (92)

1. Adret P, Margoliash D. 2002. Metabolic and neural activity in the song system nucleus robustus archistriatalis: effect of age and gender. J Comp Neurol 454:409-423.
2. Bauer EE, Coleman MJ, Roberts TF, Roy A, Prather JF, Mooney R. 2008. A synaptic basis for auditory-vocal integration in the songbird. J Neurosci 28:1509-1522.
3. Bengtson CP, Osborne PB. 2000. Electrophysiological properties of cholinergic and noncholinergic neurons in the ventral pallidal region of the nucleus basalis in rat brain slices. J Neurophysiol 83:2649-2660.
4. Benowitz LI, Karten HJ. 1976. Organization of the tectofugal visual pathway in the pigeon: a retrograde transport study. J Comp Neurol 167:503-520.
5. Bigalke-Kunz B, Rubsamen R, Dorrscheidt GJ. 1987. Tonotopic organization and functional characterization of the auditory thalamus in a songbird, the European starling. J Comp Physiol [A] 161:255-265.
6. Bisler S, Schleicher A, Gass P, Stehle JH, Zilles K, Staiger JF. 2002. Expression of c-Fos, ICER, Krox-24 and JunB in the whisker-to-barrel pathway of rats: time course of induction upon whisker stimulation by tactile exploration of an enriched environment. J Chem Neuroanat 23:187-198.
7. Boutros T, Chevet E, Metrakos P. 2008. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol Rev 60:261-310.
8. 14C-2-deoxyglucose uptake in the brain of the zebra finch. I.Auditory and vocal motor systems. Cell Tissue Res 240:101-115.
9. 14C-2-deoxyglucose uptake in the brain of the zebra finch. II.Visual system. Cell Tissue Res 240:117-127.
10. Cardin JA, Schmidt MF. 2004. Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. J Neurophysiol 91:2148-2163.
11. Cardin JA, Raksin JN, Schmidt MF. 2005. Sensorimotor nucleus NIf is necessary for auditory processing but not vocal motor output in the avian song system. J Neurophy-siol 93:2157-2166.
12. Cheng HY, Clayton DF. 2004. Activation and habituation of extracellular signal-regulated kinase phosphorylation in zebra finch auditory forebrain during song presentation. J Neurosci 24:7503-7513.
13. Chew SJ, Mello C, Nottebohm F, Jarvis E, Vicario DS. 1995. Decrements in auditory responses to a repeated conspe-cific song are long-lasting and require two periods of protein synthesis in the songbird forebrain. Proc Natl Acad Sci USA 92:3406-3410.
14. Clayton DF. 2004. Songbird genomics: methods, mechanisms, opportunities, and pitfalls. Ann N Y Acad Sci 1016:45-60.
15. Csillag A, Montagnese CM. 2005. Thalamotelencephalic organization in birds. Brain Res Bull 66:303-310.
16. Deng C, Rogers LJ. 1998a. Bilaterally projecting neurons in the two visual pathways of chicks. Brain Res 794: 281-290.
17. Deng C, Rogers LJ. 1998b. Organisation of the tectorotundal and SP/IPS-rotundal projections in the chick. J Comp Neu-rol 394:171-185.
18. Di Benedetto B, Hitz C, Holter SM, Kuhn R, Vogt Weisenhorn DM, Wurst W. 2007. Differential mRNA distribution of components of the ERK/MAPK signalling cascade in the adult mouse brain. J Comp Neurol 500:542-556.
19. Doi M, Cho S, Yujnovsky I, Hirayama J, Cermakian N, Cato AC, Sassone-Corsi P. 2007. Light-inducible and clock-controlled expression of MAP kinase phosphatase 1 in mouse central pacemaker neurons. J Biol Rhythms 22:127-139.
20. Doupe AJ, Perkel DJ, Reiner A, Stern EA. 2005. Birdbrains could teach basal ganglia research a new song. Trends Neurosci 28:353-363.
21. Farooq A, Zhou MM. 2004. Structure and regulation of MAPK phosphatases. Cell Signal 16:769-779
22. 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.
23. Flavell SW, Greenberg ME. 2008. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 31:563-590.
24. Freund N, Gunturkun O, Manns M. 2008. A morphological study of the nucleus subpretectalis of the pigeon. Brain Res Bull 75:491-493.
25. Gerfen CR. 2000. Molecular effects of dopamine on striatal-projection pathways. Trends Neurosci 23:S64-70.
26. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Scham-bra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N. 2003. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925.
27. Greenberg ME, Hermanowski AL, Ziff EB. 1986. Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription. Mol Cell Biol 6:1050-1057.
28. Guillery RW, Herrup K. 1997. Quantification without pontifica-tion: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386:2-7.
29. Gunturkun O, Hellmann B, Melsbach G, Prior H. 1998. Asymmetries of representation in the visual system of pigeons. Neuroreport 9:4127-4130.
30. Guzowski JF, Timlin JA, Roysam B, McNaughton BL, Worley PF, Barnes CA. 2005. Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr Opin Neurobiol 15:599-606
31. 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.
32. Heyers D, Manns M, Luksch H, Gunturkun O, Mouritsen H. 2008. Calcium-binding proteins label functional streams of the visual system in a songbird. Brain Res Bull 75:348-355.
33. Hu S, Ying Z, Gomez-Pinilla F, Frautschy SA. 2009. Exercise can increase small heat shock proteins (sHSP) and pre-and post-synaptic proteins in the hippocampus. Brain Res 1249:191-201
34. Jarvis ED. 2004a. Brains and birdsong. In: Marler P, Slabbekoorn H, editors. Nature's music: the science of birdSong. San Diego: Elsevier-Academic Press. p 226-271
35. Jarvis ED. 2004b. Learned birdsong and the neurobiology of human language. Ann N Y Acad Sci 1016:749-777
36. Jarvis ED. 2009. Evolution of the pallium in birds and reptiles. In: Binder MD, Hirokawa N, Windhorst U, Butler As-e, editors. Encyclopedia of neuroscience. Berlin: Springer-Verlag. p 1390-1400.
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 USA 94:4097-4102.
39. Jarvis ED, Scharff C, Grossman MR, Ramos JA, Nottebohm F. 1998. For whom the bird sings: context-dependent gene expression. Neuron 21:775-788.
40. 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.
41. Kaczmarek L, Chaudhuri A. 1997. Sensory regulation of immediate-early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity. Brain Res Brain Res Rev 23:237-256.
42. Karten HJ. 1991. Homology and evolutionary origins of the 'neocortex'. Brain Behav Evol 38:264-272.
43. Kerner JA, Standaert DG, Penney JB Jr, Young AB, Landwehrmeyer GB. 1998. Simultaneous isotopic and nonisotopic in situ hybridization histochemistry with cRNA probes. Brain Res Brain Res Protoc 3:22-32.
44. Knapska E, Kaczmarek L. 2004. A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK? Prog Neurobiol 74:183-211.
45. Kodama M, Russell DS, Duman RS. 2005. Electroconvulsive seizures increase the expression of MAP kinase phospha-tases in limbic regions of rat brain. Neuropsychopharma-cology 30:360-371.
46. Krutzfeldt NO, Wild JM. 2004. Definition and connections of the entopallium in the zebra finch (Taeniopygia guttata). J Comp Neurol 468:452-465
47. Kubikova L, Wada K, Jarvis ED. 2010. Dopamine receptors in a songbird brain. J Comp Neurol 518:741-769.
48. Liu Y, Shepherd EG, Nelin LD. 2007. MAPK phosphatases\reg-ulating the immune response. Nat Rev Immunol 7:202-212.
49. Liu YX, Wang J, Guo J, Wu J, Lieberman HB, Yin Y. 2008. DUSP1 is controlled by p53 during the cellular response to oxida-tive stress. Mol Cancer Res 6:624-633.
50. Machado HB, Vician LJ, Herschman HR. 2008. The MAPK pathway is required for depolarization-induced "promiscuous" immediate-early gene expression but not for depolarization-restricted immediate-early gene expression in neurons. J Neurosci Res 86:593-602.
51. Maczko KA, Knudsen PF, Knudsen EI. 2006. Auditory and visual space maps in the cholinergic nucleus isthmi pars par-vocellularis of the barn owl. J Neurosci 26:12799-12806.
52. Manger PR, Elston GN, Pettigrew JD. 2002. Multiple maps and activity-dependent representational plasticity in the anterior Wulst of the adult barn owl (Tyto alba). Eur J Neurosci 16:743-750.
53. Medina L, Reiner A. 2000. Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:1-12.
54. 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.
55. 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
56. Mello CV, Jarvis ED. 2008. Behavior-dependent expression of inducible genes in vocal learning birds. In: Zeigler HP, Mar-ler P, editors. Neuroscience of birdsong. Cambridge: Cambridge University Press. p 381-397.
57. Mello CV, Vicario DS, Clayton DF. 1992. Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci USA 89:6818-6822.
58. Mello CV, Vates GE, Okuhata S, Nottebohm F. 1998. Descending auditory pathways in the adult male zebra finch (Taeniopygia guttata). J Comp Neurol 395:137-160.
59. Miceli D, Reperant J. 1982. Thalamo-hyperstriatal projections in the pigeon (Columbia livia) as demonstrated by retrograde double-labeling with fluorescent tracers. Brain Res 245:365-371.
60. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD. 2007. Neu-ronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427-437
61. 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.
62. Nambu A. 2008. Seven problems on the basal ganglia. Curr Opin Neurobiol 18:595-604.
63. Nottebohm F. 1972. The origins of vocal learning. Am Naturalist 106:116-140.
64. Person AL, Gale SD, Farries MA, Perkel DJ. 2008. Organization of the songbird basal ganglia, including area X. J Comp Neurol 508:840-866.
65. Pinaud R, Vargas CD, Ribeiro S, Monteiro MV, Tremere LA, Vianney P, Delgado P, Mello CV, Rocha-Miranda CE, Vol-chan E. 2003. Light-induced Egr-1 expression in the striate cortex of the opossum. Brain Res Bull 61:139-146
66. Pinaud R, Osorio C, Alzate O, Jarvis ED. 2008. Profiling of experience-regulated proteins in the songbird auditory fore-brain using quantitative proteomics. Eur J Neurosci 27: 1409-1422.
67. Pizzio GA, Golombek DA. 2008. Photic regulation of map ki-nase phosphatases MKP1/2 and MKP3 in the hamster suprachiasmatic nuclei. J Mol Neurosci 34:187-192.
68. Qian Z, Gilbert M, Kandel ER. 1994. Temporal and spatial regulation of the expression of BAD2, a MAP kinase phospha-tase, during seizure, kindling, and long-term potentiation. Learn Mem 1:180-188
69. 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. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414.
70. Roberts TF, Brauth SE, Hall WS. 2001. Distribution of iron in the parrot brain: conserved (pallidal) and derived (nigral) labeling patterns. Brain Res 921:138-149.
71. Rossler OG, Henss I, Thiel G. 2008. Transcriptional response to muscarinic acetylcholine receptor stimulation: regulation of Egr-1 biosynthesis by ERK, Elk-1, MKP-1, and calcineurin in carbachol-stimulated human neuroblastoma cells. Arch Biochem Biophys 470:93-102.
72. Sgambato V, Pages C, Rogard M, Besson MJ, Caboche J. 1998. Extracellular signal-regulated kinase (ERK) controls immediate early gene induction on corticostriatal stimulation. J Neurosci 18:8814-8825.
73. Shimizu T, Bowers AN. 1999. Visual circuits of the avian telen-cephalon: evolutionary implications. Behav Brain Res 98: 183-191.
74. Shipp S. 2007. Structure and function of the cerebral cortex. Curr Biol 17:R443-449.
75. Soares JG, Pereira AC, Botelho EP, Pereira SS, Fiorani M, Gat-tass R. 2005. Differential expression of Zif268 and c-Fos in the primary visual cortex and lateral geniculate nucleus of normal Cebus monkeys and after monocular lesions. J Comp Neurol 482:166-175.
76. Takahata T, Higo N, Kaas JH, Yamamori T. 2009. Expression of immediate-early genes reveals functional compartments within ocular dominance columns after brief monocular inactivation. Proc Natl Acad Sci USA 106:12151-12155.
77. Takaki M, Ujike H, Kodama M, Takehisa Y, Nakata K, Kuroda S. 2001. Two kinds of mitogen-activated protein kinase phosphatases, MKP-1 and MKP-3, are differentially activated by acute and chronic methamphetamine treatment in the rat brain. J Neurochem 79:679-688.
78. Theiss MP, Hellmann B, Gunturkun O. 2003. The architecture of an inhibitory sidepath within the avian tectofugal system. Neuroreport 14:879-882.
79. Thompson I. 2000. Cortical development: binocular plasticity turned outside-in. Curr Biol 10:R348-R350.
80. Tischmeyer W, Grimm R. 1999. Activation of immediate early genes and memory formation. Cell Mol Life Sci 55:564-574.
81. Velho TA, Pinaud R, Rodrigues PV, Mello CV. 2005. Co-induction of activity-dependent genes in songbirds. Eur J Neuro-sci 22:1667-1678.
82. 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
83. Wada K, Howard JT, McConnell P, Whitney O, Lints T, Rivas MV, Horita H, Patterson MA, White SA, Scharff C, 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 USA 103:15212-15217.
84. Warren WC, Clayton DF, Ellegren H, Arnold, AP, Hillier LW, Kunstner A, Searle S, White S, Vilella AJ, Fairley S, Heger A, Kong L, Ponting CP, Jarvis ED, et al. 2010. The genome of a songbird. Nature, in press.
85. Weidner C, Reperant J, Miceli D, Haby M, Rio JP. 1985. An anatomical study of ipsilateral retinal projections in the quail using radioautographic, horseradish peroxidase, fluorescence and degeneration techniques. Brain Res 340: 99-108.
86. Wild JM. 1987. The avian somatosensory system: connections of regions of body representation in the forebrain of the pigeon. Brain Res 412:205-223.
87. Wild JM. 1989. Avian somatosensory system: II. Ascending projections of the dorsal column and external cuneate nuclei in the pigeon. J Comp Neurol 287:1-18.
88. Wild JM, Farabaugh SM. 1996. Organization of afferent and efferent projections of the nucleus basalis prosencephali in a passerine, Taeniopygia guttata. J Comp Neurol 365: 306-328.
89. 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.
90. 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.
91. Young WS, 3rd. 1989. Simultaneous use of digoxigenin-and radiolabeled oligodeoxyribonucleotide probes for hybridization histochemistry. Neuropeptides 13:271-275.
92. Zeigler HP, Bischof H-J. 1993. Vision, brain, and behavior in birds. Cambridge, MA: MIT Press.