Cortical and subcortical projections to primary visual cortex in anophthalmic, enucleated and sighted mice

European Journal of Neuroscience

Volumn 36, Issue 7, 2012, Pages 2949-2963

  Charbonneau, Valérie ^a   Laramée, Marie Eve ^a   Boucher, Virginie ^a   Bronchti, Gilles ^a   Boire, Denis ^a,b  

^a UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Blind; Feedback; Heteromodal corticocortical; Retrograde; ZRDCT An

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOPHTHALMIA; ARTICLE; AUDITORY STIMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENUCLEATION; MOUSE; NERVE CELL NETWORK; NERVE PROJECTION; NERVE SPROUTING; NEWBORN; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; RESPONSE TIME; SENSORY NERVE; STRIATE CORTEX; TACTILE STIMULATION; VISUAL IMPAIRMENT;

ANIMALS; ANOPHTHALMOS; AUDITORY CORTEX; BLINDNESS; EYE ENUCLEATION; MICE; MICE, INBRED C57BL; NEURONS; SOMATOSENSORY CORTEX; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84867007457     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08215.x     Document Type: Article

References (93)

1. Ahissar, M., Nahum, M., Nelken, I. & Hochstein, S. (2009) Reverse hierarchies and sensory learning. Philos. Trans. R. Soc. Lond. B Biol. Sci., 364, 285-299.
2. Allman, B.L., Bittencourt-Navarrete, R.E., Keniston, L.P., Medina, A.E., Wang, M.Y. & Meredith, M.A. (2008) Do cross-modal projections always result in multisensory integration?Cereb. Cortex, 18, 2066-2076.
3. Amedi, A., Raz, N., Pianka, P., Malach, R. & Zohary, E. (2003) Early 'visual' cortex activation correlates with superior verbal memory performance in the blind. Nat. Neurosci., 6, 758-766.
4. Bavelier, D. & Neville, H.J. (2002) Cross-modal plasticity: where and how?Nat. Rev. Neurosci., 3, 443-452.
5. Berezovskii, V.K., Nassi, J.J. & Born, R.T. (2011) Segregation of feedforward and feedback projections in mouse visual cortex. J. Comp. Neurol., 519, 3672-3683.
6. Bizley, J.K. & King, A.J. (2008) Visual-auditory spatial processing in auditory cortical neurons. Brain Res., 1242, 24-36.
7. Bizley, J.K., Nodal, F.R., Bajo, V.M., Nelken, I. & King, A.J. (2007) Physiological and anatomical evidence for multisensory interactions in auditory cortex. Cereb. Cortex, 17, 2172-2189.
8. 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.
9. Brosch, M., Selezneva, E. & Scheich, H. (2005) Nonauditory events of a behavioral procedure activate auditory cortex of highly trained monkeys. J. Neurosci., 25, 6797-6806.
10. Buchel, C., Price, C., Frackowiak, R.S. & Friston, K. (1998) Different activation patterns in the visual cortex of late and congenitally blind subjects. Brain, 121, 409-419.
11. Budinger, E. & Scheich, H. (2009) Anatomical connections suitable for the direct processing of neuronal information of different modalities via the rodent primary auditory cortex. Hear. Res., 258, 16-27.
12. Budinger, E., Heil, P. & Scheich, H. (2000a) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). III. Anatomical subdivisions and corticocortical connections. Eur. J. Neurosci., 12, 2425-2451.
13. Budinger, E., Heil, P. & Scheich, H. (2000b) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. Eur. J. Neurosci., 12, 2452-2474.
14. 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.
15. Budinger, E., Laszcz, A., Lison, H., Scheich, H. & Ohl, F.W. (2008) Non-sensory cortical and subcortical connections of the primary auditory cortex in Mongolian gerbils: bottom-up and top-down processing of neuronal information via field AI. Brain Res., 1220, 2-32.
16. Burton, H. (2003) Visual cortex activity in early and late blind people. J. Neurosci., 23, 4005-4011.
17. Callaway, E.M. & Katz, L.C. (1990) Emergence and refinement of clustered horizontal connections in cat striate cortex. J. Neurosci., 10, 1134-1153.
18. Calvert, P.D., Krasnoperova, N.V., Lyubarsky, A.L., Isayama, T., Nicolo, M., Kosaras, B., Wong, G., Gannon, K.S., Margolskee, R.F., Sidman, R.L., Pugh, E.N. Jr, Makino, C.L. & Lem, J. (2000) Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha -subunit. Proc. Natl. Acad. Sci. USA, 97, 13913-13918.
19. Campi, K.L., Bales, K.L., Grunewald, R. & Krubitzer, L. (2010) Connections of auditory and visual cortex in the prairie vole (Microtus ochrogaster): evidence for multisensory processing in primary sensory areas. Cereb. Cortex, 20, 89-108.
20. Cappe, C. & Barone, P. (2005) Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey. Eur. J. Neurosci., 22, 2886-2902.
21. Cappe, C., Rouiller, E.M. & Barone, P. (2009) Multisensory anatomical pathways. Hear. Res., 258, 28-36.
22. Caviness, V.S. (1975) Architectonic map of neocortex of the normal mouse. J. Comp. Neurol., 164, 247-263.
23. Chabot, N., Charbonneau, V., Laramee, M.E., Tremblay, R., Boire, D. & Bronchti, G. (2008) Subcortical auditory input to the primary visual cortex in anophthalmic mice. Neurosci. Lett., 433, 129-134.
24. Chabot, N., Robert, S., Tremblay, R., Miceli, D., Boire, D. & Bronchti, G. (2007) Audition activates differently the visual system in neonatally enucleated mice compared to anophthalmic mutant. Eur. J. Neurosci., 26, 2334-2348.
25. 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.
26. Clavagnier, S., Falchier, A. & Kennedy, H. (2004) Long-distance feedback projections to area V1: implications for multisensory integration, spatial awareness, and visual consciousness. Cogn. Affect. Behav. Neurosci., 4, 117-126.
27. Cohen, L.G., Celnik, P., Pascual-Leone, A., Corwell, B., Faiz, L., Dambrosia, J., Honda, M., Sadato, N., Gerloff, C., Catalá, M.D. & Hallett, M. (1997) Functional relevance of cross-modal plasticity in blind humans. Nature, 389, 180-183.
28. 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.
29. Coogan, T.A. & Burkhalter, A. (1990) Conserved patterns of cortico-cortical connections define areal hierarchy in rat visual cortex. Exp. Brain Res., 80, 49-53.
30. Coogan, T.A. & Burkhalter, A. (1993) Hierarchical organization of areas in rat visual cortex. J. Neurosci., 13, 3749-3772.
31. Covic, E.N. & Sherman, S.M. (2011) Synaptic properties of connections between the primary and secondary auditory cortices in mice. Cereb. Cortex, 21, 2425-2441.
32. De Pasquale, R. & Sherman, S.M. (2011) Synaptic properties of corticocortical connections between the primary and secondary visual cortical areas in the mouse. J. Neurosci., 31, 16494-16506.
33. Dong, H., Shao, Z., Nerbonne, J.M. & Burkhalter, A. (2004) Differential depression of inhibitory synaptic responses in feedforward and feedback circuits between different areas of mouse visual cortex. J. Comp. Neurol., 475, 361-373.
34. Driver, J. & Noesselt, T. (2008) Multisensory interplay reveals crossmodal influences on 'sensory-specific' brain regions, neural responses, and judgments. Neuron, 57, 11-23.
35. Dursteler, M.R., Blakemore, C. & Garey, L.J. (1979) Projections to the visual cortex in the golden hamster. J. Comp. Neurol., 183, 185-204.
36. Falchier, A., Clavagnier, S., Barone, P. & Kennedy, H. (2002) Anatomical evidence of multimodal integration in primate striate cortex. J. Neurosci., 22, 5749-5759.
37. Felleman, D.J. & Van Essen, D.C. (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex, 1, 1-47.
38. Foxe, J.J., Morocz, I.A., Murray, M.M., Higgins, B.A., Javitt, D.C. & Schroeder, C.E. (2000) Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. Brain Res. Cogn. Brain Res., 10, 77-83.
39. Foxe, J.J., Wylie, G.R., Martinez, A., Schroeder, C.E., Javitt, D.C., Guilfoyle, D., Ritter, W. & Murray, M.M. (2002) Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. J. Neurophysiol., 88, 540-543.
40. Franklin, B.J. & Paxinos, G. (2008) The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego.
41. Fujii, T., Tanabe, H.C., Kochiyama, T. & Sadato, N. (2009) An investigation of cross-modal plasticity of effective connectivity in the blind by dynamic causal modeling of functional MRI data. Neurosci. Res., 65, 175-186.
42. Garrett, B., Sorensen, J.C. & Slomianka, L. (1992) Fluoro-Gold tracing of zinc-containing afferent connections in the mouse visual cortices. Anat. Embryol. (Berl), 185, 451-459.
43. Ghazanfar, A.A. & Schroeder, C.E. (2006) Is neocortex essentially multisensory?Trends Cogn. Sci., 10, 278-285.
44. Ghazanfar, A.A., Maier, J.X., Hoffman, K.L. & Logothetis, N.K. (2005) Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. J. Neurosci., 25, 5004-5012.
45. Giard, M.H. & Peronnet, F. (1999) Auditory-visual integration during multimodal object recognition in humans: a behavioral and electrophysiological study. J. Cogn. Neurosci., 11, 473-490.
46. Godement, P., Saillour, P. & Imbert, M. (1979) Thalamic afferents to the visual cortex in congenitally anophthalmic mice. Neurosci. Lett., 13, 271-278.
47. Hall, A.J. & Lomber, S.G. (2008) Auditory cortex projections target the peripheral field representation of primary visual cortex. Exp. Brain Res., 190, 413-430.
48. 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.
49. Hochstein, S. & Ahissar, M. (2002) View from the top: hierarchies and reverse hierarchies in the visual system. Neuron, 36, 791-804.
50. Innocenti, G.M., Berbel, P. & Clarke, S. (1988) Development of projections from auditory to visual areas in the cat. J. Comp. Neurol., 272, 242-259.
51. 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.
52. 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.
53. Kaiserman-Abramof, 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.
54. Karlen, S.J., Kahn, D.M. & Krubitzer, L. (2006) Early blindness results in abnormal corticocortical and thalamocortical connections. Neuroscience, 142, 843-858.
55. Kayser, C. & Logothetis, N.K. (2007) Do early sensory cortices integrate cross-modal information?Brain Struct. Funct., 212, 121-132.
56. Kingsbury, M.A., Lettman, N.A. & Finlay, B.L. (2002) Reduction of early thalamic input alters adult corticocortical connectivity. Dev. Brain Res., 138, 35-43.
57. Klinge, C., Eippert, F., Roder, B. & Buchel, C. (2010) Corticocortical connections mediate primary visual cortex responses to auditory stimulation in the blind. J. Neurosci., 30, 12798-12805.
58. Laramée, M.E., Kurotani, T., Rockland, K.S., Bronchti, G. & Boire, D. (2011) Indirect pathway between the primary auditory and visual cortices through layer V pyramidal neurons in V2L in mouse and the effects of bilateral enucleation. Eur. J. Neurosci., 34, 65-78.
59. Laramée, M.E., Rockland, K.S., Prince, S., Bronchti, G. & Boire, D. (2012) Principal component and cluster analysis of layer V pyramidal cells in visual and non-visual cortical areas projecting to the primary visual cortex of the mouse. Cereb. Cortex, doi: 10.1093/cercor/bhs060.
60. Larsen, D.D., Luu, J.D., Burns, M.E. & Krubitzer, L. (2009) What are the effects of severe visual impairment on the cortical organization and connectivity of primary visual cortex?Front. Neuroanat., 3, 30.
61. Laurienti, P.J., Burdette, J.H., Wallace, M.T., Yen, Y.F., Field, A.S. & Stein, B.E. (2002) Deactivation of sensory-specific cortex by cross-modal stimuli. J. Cogn. Neurosci., 14, 420-429.
62. Lemus, L., Hernandez, A., Luna, R., Zainos, A. & Romo, R. (2010) Do sensory cortices process more than one sensory modality during perceptual judgments?Neuron, 67, 335-348.
63. Liu, Y., Yu, C., Liang, M., Li, J., Tian, L., Zhou, Y., Qin, W., Li, K. & Jiang, T. (2007) Whole brain functional connectivity in the early blind. Brain, 130, 2085-2096.
64. Löwel, S. & Singer, W. (1992) Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science, 255, 209-212.
65. Merabet, L.B. & Pascual-Leone, A. (2010) Neural reorganization following sensory loss: the opportunity of change. Nat. Rev. Neurosci., 11, 44-52.
66. Miller, M.W. & Vogt, B.A. (1984a) Direct connections of rat visual cortex with sensory, motor and association cortices. J. Comp. Neurol., 226, 184-202.
67. Miller, M.W. & Vogt, B.A. (1984b) Heterotopic and homotopic callosal connections in rat visual cortex. Brain Res., 297, 75-89.
68. Molholm, S., Ritter, W., Murray, M.M., Javitt, D.C., Schroeder, C.E. & Foxe, J.J. (2002) Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. Brain Res. Cogn. Brain Res., 14, 115-128.
69. Muller-Paschinger, I.B. & Tombol, T. (1989) Cortico-cortical and subcortico-cortical afferent connection of the rabbit's primary visual cortex. A horseradish peroxidase study. Anat. Embryol. (Berl), 180, 81-88.
70. Murray, M.M., Molholm, S., Michel, C.M., Heslenfeld, D.J., Ritter, W., Javitt, D.C., Schroeder, C.E. & Foxe, J.J. (2005) Grabbing your ear: rapid auditory-somatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment. Cereb. Cortex, 15, 963-974.
71. 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.
72. Piché, M., Chabot, N., Bronchti, G., Miceli, D., Lepore, F. & Guillemot, J.P. (2007) Auditory responses in the visual cortex of neonatally enucleated rats. Neuroscience, 145, 1144-1156.
73. Rieck, R.W. & Carey, R.G. (1985) Organization of the rostral thalamus in the rat: evidence for connections to layer I of visual cortex. J. Comp. Neurol., 234, 137-154.
74. Rockland, K.S. & Ojima, H. (2003) Multisensory convergence in calcarine visual areas in macaque monkey. Int. J. Psychophysiol., 50, 19-26.
75. Rockland, K.S. & Pandya, D.N. (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res., 179, 3-20.
76. Ruthazer, E.S. & Stryker, M.P. (1996) The role of activity in the development of long-range horizontal connections in area 17 of the ferret. J. Neurosci., 16, 7253-7269.
77. Salin, P.A. & Bullier, J. (1995) Corticocortical connections in the visual system: structure and function. Physiol. Rev., 75, 107-154.
78. Sanchez-Vives, M.V., Nowak, L.G., Descalzo, V.F., Garcia-Velasco, J.V., Gallego, R. & Berbel, P. (2006) Crossmodal audio-visual interactions in the primary visual cortex of the visually deprived cat: a physiological and anatomical study. Prog. Brain Res., 155, 287-311.
79. Schroeder, C.E. & Foxe, J.J. (2002) The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. Brain Res. Cogn. Brain Res., 14, 187-198.
80. Schroeder, C.E. & Foxe, J. (2005) Multisensory contributions to low-level, 'unisensory' processing. Curr. Opin. Neurobiol., 15, 454-458.
81. Schroeder, C.E., Lindsley, R.W., Specht, C., Marcovici, A., Smiley, J.F. & Javitt, D.C. (2001) Somatosensory input to auditory association cortex in the macaque monkey. J. Neurophysiol., 85, 1322-1327.
82. Schroeder, C.E., Smiley, J., Fu, K.G., McGinnis, T., O'Connell, M.N. & Hackett, T.A. (2003) Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing. Int. J. Psychophysiol., 50, 5-17.
83. Senkowski, D., Talsma, D., Grigutsch, M., Herrmann, C.S. & Woldorff, M.G. (2007) Good times for multisensory integration: effects of the precision of temporal synchrony as revealed by gamma-band oscillations. Neuropsychologia, 45, 561-571.
84. Simmons, P.A., Lemmon, V. & Pearlman, A.L. (1982) Afferent and efferent connections of the striate and extrastriate visual cortex of the normal and reeler mouse. J. Comp. Neurol., 211, 295-308.
85. Sperdin, H.F., Cappe, C., Foxe, J.J. & Murray, M.M. (2009) Early, low-level auditory-somatosensory multisensory interactions impact reaction time speed. Front. Integr. Neurosci., 3, 2.
86. Toldi, J., Rojik, I. & Fehér, O. (1994) Neonatal monocular enucleation-induced cross-modal effects observed in the cortex of adult rat. Neuroscience, 62, 105-114.
87. 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.
88. Voss, P., Gougoux, F., Zatorre, R.J., Lassonde, M. & Lepore, F. (2008) Differential occipital responses in early- and late-blind individuals during a sound-source discrimination task. Neuroimage, 40, 746-758.
89. Wang, Q. & Burkhalter, A. (2007) Area map of mouse visual cortex. J. Comp. Neurol., 502, 339-357.
90. Werner, S. & Noppeney, U. (2010) Distinct functional contributions of primary sensory and association areas to audiovisual integration in object categorization. J. Neurosci., 30, 2662-2675.
91. Yamashita, A., Valkova, K., Gonchar, Y. & Burkhalter, A. (2003) Rearrangement of synaptic connections with inhibitory neurons in developing mouse visual cortex. J. Comp. Neurol., 464, 426-437.
92. Yu, C., Liu, Y., Li, J., Zhou, Y., Wang, K., Tian, L., Qin, W., Jiang, T. & Li, K. (2008) Altered functional connectivity of primary visual cortex in early blindness. Hum. Brain Mapp., 29, 533-543.
93. Zilles, K. & Wree, A. (1995). Cortex: areal and laminar structure. In Paxinos, G. (Ed.), The Rat Nervous System. Academic Press, Sydney, pp. 649-685.