Audition differently activates the visual system in neonatally enucleated mice compared with anophthalmic mutants

European Journal of Neuroscience

Volumn 26, Issue 8, 2007, Pages 2334-2348

  Chabot, Nicole ^a   Robert, Stéphane ^a   Tremblay, Robin ^a   Miceli, Dom ^a   Boire, Denis ^a   Bronchti, Gilles ^a  

^a UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

Author keywords

Auditory cortex; Blindness; c Fos; Cerebral cortex; Crossmodal plasticity

Indexed keywords

PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANOPHTHALMIA; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; ENUCLEATION; HEARING; IMMUNOHISTOCHEMISTRY; LATERAL GENICULATE BODY; MOUSE; MUTANT; NOISE; NONHUMAN; PRIORITY JOURNAL; VISUAL SYSTEM;

ACOUSTIC STIMULATION; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANOPHTHALMOS; AUDITORY CORTEX; AUDITORY PERCEPTION; BIOTIN; BLINDNESS; CELL COUNT; DEXTRANS; DISEASE MODELS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PROTO-ONCOGENE PROTEINS C-FOS; VISUAL PATHWAYS;

EID: 35448977682     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05854.x     Document Type: Article

References (69)

1. Amir, S. Stewart, J. (1999) Conditioned and unconditioned aversive stimuli enhance light-induced fos expression in the primary visual cortex. Neuroscience, 89, 323 327.
2. Asanuma, C. Stanfield, B.B. (1990) Induction of somatic sensory inputs to the lateral geniculate nucleus in congenitally blind mice and in phenotypically normal mice. Neuroscience, 39, 533 545.
3. Bai, W.Z., Ishida, M. Arimatsu, Y. (2004) Chemically defined feedback connections from infragranular layers of sensory association cortices in the rat. Neuroscience, 123, 257 267.
4. Bonaventure, N. Karli, P. (1968) Apparition au niveau du cortex visuel de potentiels évoqués d'origine auditive cheZ. la souris privée de photorécepteurs. J. Physiol. (Paris), 60, 407.
5. Bronchti, G., Heil, P., Sadka, R., Hess, A., Scheich, H. Wollberg, Z. (2002) Auditory activation of 'visual' cortical areas in the blind mole rat (Spalax ehrenbergi). Eur. J. Neurosci., 16, 311 329.
6. Bronchti, G., Heil, P., Scheich, H. Wollberg, Z. (1989) Auditory pathway and auditory activation of primary visual targets in the blind mole rat (Spalax ehrenbergi): I. A 2-deoxyglucose study of subcortical centers. J. Comp. Neurol., 284, 253 274.
7. Buchel, C., Price, C., Frackowiak, R.S.J. Friston, K. (1998) Different activation patterns in the visual cortex of late and congenitally blind subjects. Brain, 121, 409 419.
8. Budinger, E., Heil, P., Hess, A. Scheich, H. (2006) Multisensory processing via early cortical stages: connections of the primary auditory cortical field with other sensory systems. Neuroscience, 143, 1065 1083.
9. Carretta, D., Hervé-Minvielle, A., Bajo, V.M., Villa, A.E.P. Rouiller, E.M. (1999) c-Fos expression in the auditory pathways related to the significance of acoustic signals in rats performing a sensory-motor task. Brain Res., 841, 170 183.
10. Caviness, V.S. Jr. (1975) Architectonic map of neocortex of the normal mouse. J. Comp. Neurol., 164, 247 263.
11. Chase, H.B. (1945) Studies on an anophthalmic strain of mice. V. Associated cranial nerves and brain centers. J. Comp. Neurol., 83, 121 139.
12. Chase, H.B. Chase, E.B. (1941) Studies on an anophthalmic strain of mice. I. Embryology of the eye region. J. Morphol., 68, 279 401.
13. Clancy, B., Darlington, R.B. Finlay, B.L. (2001) Translating developmental time across mammalian species. Neuroscience, 105, 7 17.
14. Cohen, L.G., Weeks, R.A., Sadato, N., Celnik, P., Ishii, K. Hallett, M. (1999) Period of susceptibility for cross-modal plasticity in the blind. Ann. Neurol., 45, 451 460.
15. Correa-Lacarcel, J., Pujante, M.J., Terol, F.F., Menar-Garcia, V., Puchades-Orts, A., Ballesta, J.J., Lloret, J., Robles, J.A. Sanchez-del-Campo, F. (2000) Stimulus frequency affects c-fos expression in the rat visual system. J. Chem. Neuroanat., 18, 135 146.
16. Cüllen, M.J. Kaiserman-Abramov, I.R. (1976) Cytological organization of the dorsal lateral geniculate nuclei in mutant anophthalmic and postnatally enucleated mice. J. Neurocytol., 5, 407 424.
17. D'Aniello, S., d'Aniello, E., Locascio, A., Memoli, A., Corrado, M., Russo, M.T., Aniello, F., Fucci, L., Brown, E.R. Branno, M. (2006) The ascidian homolog of the vertebrate homeobox gene Rx is essential for ocellus development and function. Differentiation, 74, 222 234.
18. Doron, N. Wollberg, Z. (1994) Cross-modal neuroplasticity in the blind mole rat Spalax ehrenbergi: a WGA-HRP tracing study. Neuroreport, 5, 2697 2701.
19. Falchier, A., Clavagnier, S., Barone, P. Kennedy, H. (2002) Anatomical evidence of multimodal integration in primate striate cortex. J. Neurosci., 22, 5749 5759.
20. Faradji-Prevautel, H., Cespuglio, R. Jouvet, M. (1990) Circadian rest-activity rhythms in the anophthalmic, monocular and binocular ZRDCT/An mice. Retinal and serotoninergic (raphe) influences. Brain Res., 526, 207 216.
21. Friauf, E. Shatz, C.J. (1991) Changing patterns of synaptic input to subplate and cortical plate during development of visual cortex. J. Neurophysiol., 66, 2059 2071.
22. Gougoux, F., Zatorre, R.J., Lassonde, M., Voss, P. Lepore, F. (2005) A functional neuroimaging study of sound localization: visual cortex activity predicts performance in early-blind individuals. PLoS Biol., 3, e27.
23. Goyal, M.S., Hansen, P.J. Blakemore, C.B. (2006) Tactile perception recruits functionally related visual areas in the late-blind. Neuroreport, 17, 1381 1384.
24. Gundersen, H.J., Jensen, E.B., Kieu, K. Nielsen, J. (1999) The efficiency of systematic sampling in stereology - reconsidered. J. Microsc., 193, 199 211.
25. Hanganu, I.L., Ben-Ari, Y. Khazipov, R. (2006) Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J. Neurosci., 26, 6728 6736.
26. Hanganu, I.L., Kilb, W. Luhmann, H.J. (2002) Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J. Neurosci., 22, 7165 7176.
27. Heil, P., Bronchti, G., Wollberg, Z. Scheich, H. (1991) Invasion of the visual cortex by the auditory system in the naturally blind mole rat. Neuroreport, 2, 735 738.
28. Heil, P. Scheich, H. (1986) Effects of unilateral and bilateral cochlea removal on 2-deoxyglucose patterns in the chick auditory system. J. Comp. Neurol., 252, 279 301.
29. Heumann, D. Rabinowicz, T. (1980) Postnatal development of the dorsal lateral geniculate nucleus in the normal and enucleated albino mouse. Exp. Brain Res., 38, 75 85.
30. Higashi, S., Molnar, Z., Kurotani, T. Toyama, K. (2002) Prenatal development of neural excitation in rat thalamocortical projections studied by optical recording. Neuroscience, 115, 1231 1246.
31. Huberman, A.D., Speer, C.M. Chapman, B. (2006) Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in V1. Neuron, 52, 247 254.
32. Izraeli, R., Koay, G., Lamish, M., Heicklen-Klein, A.J., Heffner, H.E., Heffner, R.S. Wollberg, Z. (2002) Cross-modal neuroplasticity in neonatally enucleated hamsters: structure, electrophysiology and behaviour. Eur. J. Neurosci., 15, 693 712.
33. 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. Rev., 23, 237 256.
34. Kahn, D.M. Krubitzer, L. (2002) Massive cross-modal cortical plasticity and the emergence of a new cortical area in developmentally blind mammals. Proc. Natl Acad. Sci. USA, 99, 11429 11434.
35. Kaiserman-Abramov, I.R. (1979) Quantitative comparaison of spines in layer V neurons of the striate cortex in anophthalmic mutant and normal mice. Brain Res., 179, 385 389.
36. Kaiserman-Abramov, I.R. (1983) Intrauterine enucleation of normal mice mimics a structural compensatory response in the geniculate of eyeless mutant mice. Brain Res., 270, 149 153.
37. Kaiserman-Abramov, I.R., Graybiel, A.M. Nauta, W.J.H. (1980) The thalamic projection to cortical area 17 in a congenitally anophthalmic mouse strain. Neuroscience, 5, 41 52.
38. Karlen, S.J., Kahn, D.M. Krubitzer, L. (2006) Early blindness results in abnormal corticocortical and thalamocortical connections. Neuroscience, 142, 843 858.
39. Karlen, S.J. Krubitzer, L. (2006) The evolution of the neocortex in mammals: intrinsic and extrinsic contributions to the cortical phenotype. Novartis. Found. Symp., 270, 146 159.
40. Laemle, L.K. Ottenweller, J.E. (1998) Daily patterns of running wheel activity in male anophthalmic mice. Physiol. Rev., 64, 165 171.
41. Laemle, L.K. Rusa, R. (1992) VIP-like immunoreactivity in the suprachiasmatic nuclei of a mutant anophthalmic mouse. Brain Res., 589, 124 128.
42. Laemle, L.K., Strominger, N.L. Carpenter, D.O. (2006) Cross-modal innervation of primary visual cortex by auditory fibers in congenitally anophthalmic mice. Neurosci. Lett., 396, 108 112.
43. Mahlke, C. Wallhaüsser-Franke, E. (2004) Evidence for tinnitus-related plasticity in the auditory and limbic system, demonstrated by arg3.1 and c-fos immunocytochemistry. Hear. Res., 195, 17 34.
44. Molnar, Z., Higashi, S. Lopez-Bendito, G. (2003) Choreography of early thalamocortical development. Cereb. Cortex, 13, 661 669.
45. Necker, R., Rehkämper, G. Nevo, E. (1992) Electrophysiological mapping of body representation in the cortex of the blind mole rat. Neuroreport, 3, 505 508.
46. Ohuchi, H., Tomonari, S., Itoh, H., Mikawa, T. Noji, S. (1999) Identification of chick rax/rx genes with overlapping patterns of expression during early eye and brain development. Mech. Dev., 85, 193 195.
47. Olavarria, J.F. Van Sluyters, R.C. (1984) Callosal connections of the posterior neocortex in normal eyed, congenitally anophthalmic, and neonatally enucleated mice. J. Comp. Neurol., 230, 249 268.
48. Paperna, T. Malach, R. (1991) Patterns of sensory intermodality relationships in the cerebral cortex of the rat. J. Comp. Neurol., 308, 432 456.
49. Pascual-Leone, A., Amedi, A., Fregni, F. Merabet, L.B. (2005) The plastic human brain cortex. Annu. Rev. Neurosci., 28, 377 401.
50. Piché, M., Robert, S., Miceli, D. Bronchti, G. (2004) Environmental enrichment enhances auditory takeover of the occipital cortex in anophthalmic mice. Eur. J. Neurosci., 20, 3463 3472.
51. Qian, Y., Wu, M. Jen, P.H.S. (1996) Tracing the auditory pathways to electrophysiologically characterized neurons with HRP and Fos double-labeling technique. Brain Res., 731, 241 245.
52. Rauschecker, J.P. Korte, M. (1993) Auditory compensation for early blindness in cat cerebral cortex. J. Neurosci., 13, 4538 4548.
53. Sadato, N., Okada, T., Honda, M. Yonekura, Y. (2002) Critical period for cross-modal plasticity in blind humans: a functional MRI study. Neuroimage, 16, 389 400.
54. Scheich, H. Zuschratter, W. (1995) Mapping of stimulus features and meaning in gerbil auditory cortex with 2-deoxyglucose and c-Fos antibodies. Behav. Brain Res., 66, 195 205.
55. Schroeder, C.E. Foxe, J. (2005) Multisensory contributions to low-level, 'unisensory' processing. Curr. Opin. Neurobiol., 15, 454 458.
56. Silver, J. (1977) Abnormal development of the suprachiasmatic nuclei of the hypothalamus in a strain of genetically anophthalmic mice. J. Comp. Neurol., 176, 589 606.
57. Toldi, J., Farkas, T. Völgyi, B. (1994a) Neonatal enucleation induces cross-modal changes in the barrel cortex of rat. A behavioural and electrophysiological study. Neurosci. Lett., 167, 1 4.
58. Toldi, J., Feher, O., Joo, F., Antal, A. Wolff, J.R. (1990) Sodium bromide treatment influences the plasticity of somatosensory responses in the rat cortex as induced by enucleation. Neuroscience, 37, 675 683.
59. Toldi, J., Rojik, I. Fehér, O. (1994b) Neonatal monocular enucleation-induced cross-modal effects observed in the cortex of adult rat. Neuroscience, 62, 105 114.
60. Tucker, P., Laemle, L., Munson, A., Kanekar, S., Oliver, E.R., Brown, N., Schlecht, H., Vetter, M. Glaser, T. (2001) The eyeless mouse mutation (ey1) removes an alternative start codon from the Rx/rax homeobox gene. Genesis, 31, 43 53.
61. Voss, P., Gougoux, F., Lassonde, M., Zatorre, R.J. Lepore, F. (2006) A positron emission tomography study during auditory localization by late-onset blind individuals. Neuroreport, 17, 383 388.
62. Wallace, M.T., Ramachandran, R. Stein, B.E. (2004) A revised view of sensory cortical parcellation. Proc. Natl Acad. Sci. USA, 101, 2167 2172.
63. Wallhäusser-Franke, E., Braun, S. Langner, G. (1996) Salicylate alters 2-DG uptake in the auditory system: a model for tinnitus? Neuroreport, 7, 1585 1588.
64. Wallhaüsser-Franke, E., Mahlke, C., Oliva, R., Braun, S., Wenz, G. Langner, G. (2003) Expression of c-fos in auditory and non-auditory brain regions of the gerbil after manipulations that induce tinnitus. Exp. Brain Res., 153, 649 654.
65. Warton, S.S., Dyson, S.E. Harvey, A.R. (1988) Visual thalamocortical projections in normal and enucleated rats: HRP and fluorescent dye studies. Exp. Neurol., 100, 23 39.
66. Watkins, S., Shams, L., Tanaka, S., Haynes, J.D. Rees, G. (2006) Sound alters activity in human V1 in association with illusory visual perception. Neuroimage, 31, 1247 1256.
67. West, M.J., Slomianka, L. Gundersen, H.J. (1991) Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat. Rec., 231, 482 497.
68. Wittenberg, G.F., Werhahn, K.J., Wassermann, E.M., Herscovitch, P. Cohen, L.G. (2004) Functional connectivity between somatosensory and visual cortex in early blind humans. Eur. J. Neurosci., 20, 1923 1927.
69. Zuschratter, W., Gass, P., Herdegen, T. Scheich, H. (1995) Comparison of frequency-specific c-Fos expression and fluoro- 2-deoxyglucose uptake in auditory cortex of gerbils (Meriones unguiculatus). Eur. J. Neurosci., 7, 1614 1626.