Neuronal activity is not required for the initial formation and maturation of visual selectivity

Nature Neuroscience

Volumn 18, Issue 12, 2015, Pages 1780-1788

  Hagihara, Kenta M ^a   Murakami, Tomonari ^a   Yoshida, Takashi ^a,b   Tagawa, Yoshiaki ^b,c   Ohki, Kenichi ^a,b,d  

^a KYUSHU UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; EVOKED VISUAL RESPONSE; FEMALE; IN VIVO STUDY; MALE; MOUSE; NERVE CELL STIMULATION; NERVE CONDUCTION; NONHUMAN; ORIENTATION; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRIATE CORTEX; VISUAL STIMULATION; ANIMAL; C57BL MOUSE; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; NERVE CELL; NEWBORN; PHOTOSTIMULATION; PHYSIOLOGY; PREGNANCY; PROCEDURES; VISION; VISUAL CORTEX; VISUAL SYSTEM;

ANIMALS; ANIMALS, NEWBORN; FEMALE; MALE; MICE; MICE, INBRED C57BL; NEURONS; ORIENTATION; PHOTIC STIMULATION; PREGNANCY; VISUAL CORTEX; VISUAL PATHWAYS; VISUAL PERCEPTION;

EID: 84949108483     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4155     Document Type: Article

References (59)

1. Hubel, D.H., & Wiesel, T.N. Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J. Neurophysiol. 26, 994-1002 (1963).
2. Wiesel, T.N., & Hubel, D.H. Ordered arrangement of orientation columns in monkeys lacking visual experience. J. Comp. Neurol. 158, 307-318 (1974).
3. Miller, K.D., Erwin, E., & Kayser, A Is the Development of Orientation Selectivity Instructed by Activity? J. Neurobiol. 41, 44-57 (1999).
4. Li, Y., et al. Clonally related visual cortical neurons show similar stimulus feature selectivity. Nature 486, 118-121 (2012).
5. Yu, Y.C., et al. Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly. Nature 486, 113-117 (2012).
6. Ohtsuki, G., et al. Similarity of visual selectivity among clonally related neurons in visual cortex. Neuron 75, 65-72 (2012).
7. Penn, A.A., Riquelme, P.A., Feller, M.B., & Shatz, C.J. Competition in retinogeniculate patterning driven by spontaneous activity. Science 279, 2108-2112 (1998).
8. Huberman, A.D., Feller, M.B., & Chapman, B. Mechanisms underlying development of visual maps and receptive fields. Annu. Rev. Neurosci. 31, 479-509 (2008).
9. Cang, J., et al. Development of precise maps in visual cortex requires patterned spontaneous activity in the retina. Neuron 48, 797-809 (2005).
10. Huberman, A.D., Speer, C.M., & Chapman, B. Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in v1. Neuron 52, 247-254 (2006).
11. Crair, M.C., Gillespie, D.C., & Stryker, M.P. The role of visual experience in the development of columns in cat visual cortex. Science 279, 566-570 (1998).
12. Sengpiel, F., Stawinski, P., & Bonhoeffer, T. Influence of experience on orientation maps in cat visual cortex. Nat. Neurosci. 2, 727-732 (1999).
13. Kreile, A.K., Bonhoeffer, T., & Hubener, M. Altered visual experience induces instructive changes of orientation preference in mouse visual cortex. J. Neurosci. 31, 13911-13920 (2011).
14. Rochefort, N.L., et al. Development of direction selectivity in mouse cortical neurons. Neuron 71, 425-432 (2011).
15. Kang, E., et al. Visual acuity development and plasticity in the absence of sensory experience. J. Neurosci. 33, 17789-17796 (2013).
16. Chapman, B., & Stryker, M.P. Development of orientation selectivity in ferret visual cortex and effects of deprivation. J. Neurosci. 13, 5251-5262 (1993).
17. White, L.E., Coppola, D.M., & Fitzpatrick, D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 411, 1049-1052 (2001).
18. Yuste, R., Peinado, A., & Katz, L.C. Neuronal domains in developing neocortex. Science 257, 665-669 (1992).
19. Garaschuk, O., Linn, J., Eilers, J., & Konnerth, A. Large-scale oscillatory calcium waves in the immature cortex. Nat. Neurosci. 3, 452-459 (2000).
20. Rochefort, N.L., et al. Sparsification of neuronal activity in the visual cortex at eye-opening. Proc. Natl. Acad. Sci. USA 106, 15049-15054 (2009).
21. Allene, C., & Cossart, R. Early NMDA receptor-driven waves of activity in the developing neocortex: physiological or pathological network oscillations? J. Physiol. (Lond.) 588, 83-91 (2010).
22. Ackman, J.B., Burbridge, T.J., & Crair, M.C. Retinal waves coordinate patterned activity throughout the developing visual system. Nature 490, 219-225 (2012).
23. Siegel, F., Heimel, J.A., Peters, J., & Lohmann, C. Peripheral and central inputs shape network dynamics in the developing visual cortex in vivo. Curr. Biol. 22, 253-258 (2012).
24. Weliky, M., & Katz, L.C. Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature 386, 680-685 (1997).
25. Chiu, C., & Weliky, M. Spontaneous activity in developing ferret visual cortex in vivo. J. Neurosci. 21, 8906-8914 (2001).
26. Ko, H., et al. The emergence of functional microcircuits in visual cortex. Nature 496, 96-100 (2013).
27. Ko, H., Mrsic-Flogel, T.D., & Hofer, S.B. Emergence of feature-specific connectivity in cortical microcircuits in the absence of visual experience. J. Neurosci. 34, 9812-9816 (2014).
28. Kuhlman, S.J., Tring, E., & Trachtenberg, J.T. Fast-spiking interneurons have an initial orientation bias that is lost with vision. Nat. Neurosci. 14, 1121-1123 (2011).
29. Li, Y.T., Ma, W.P., Pan, C.J., Zhang, L.I., & Tao, H.W. Broadening of cortical inhibition mediates developmental sharpening of orientation selectivity. J. Neurosci. 32, 3981-3991 (2012).
30. Wang, B.S., Feng, L., Liu, M., Liu, X., & Cang, J. Environmental enrichment rescues binocular matching of orientation preference in mice that have a precocious critical period. Neuron 80, 198-209 (2013).
31. Hoy, J.L., & Niell, C.M. Layer-specific refinement of visual cortex function after eye opening in the awake mouse. J. Neurosci. 35, 3370-3383 (2015).
32. Dräger, U.C. Receptive fields of single cells and topography in mouse visual cortex. J. Comp. Neurol. 160, 269-290 (1975).
33. Mank, M., et al. A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat. Methods 5, 805-811 (2008).
34. Girshick, A.R., Landy, M.S., & Simoncelli, E.P. Cardinal rules: visual orientation perception reflects knowledge of environmental statistics. Nat. Neurosci. 14, 926-932 (2011).
35. Coppola, D.M., Purves, H.R., McCoy, A.N., & Purves, D. The distribution of oriented contours in the real world. Proc. Natl. Acad. Sci. USA 95, 4002-4006 (1998).
36. Coppola, D.M., White, L.E., Fitzpatrick, D., & Purves, D. Unequal representation of cardinal and oblique contours in ferret visual cortex. Proc. Natl. Acad. Sci. USA 95, 2621-2623 (1998).
37. Johns, D.C., Marx, R., Mains, R.E., ORourke, B., & Marban, E. Inducible genetic suppression of neuronal excitability. J. Neurosci. 19, 1691-1697 (1999).
38. Mizuno, H., Hirano, T., & Tagawa, Y. Evidence for activity-dependent cortical wiring: formation of interhemispheric connections in neonatal mouse visual cortex requires projection neuron activity. J. Neurosci. 27, 6760-6770 (2007).
39. Ohki, K., Chung, S., Chng, Y.H., Kara, P., & Reid, R.C. Functional imaging with cellular resolution reveals precise micro-Architecture in visual cortex. Nature 433, 597-603 (2005).
40. Niculescu, D., & Lohmann, C. Gap junctions in developing thalamic and neocortical neuronal networks. Cereb. Cortex 24, 3097-3106 (2013).
41. Yamada, A., et al. Role of pre-And postsynaptic activity in thalamocortical axon branching. Proc. Natl. Acad. Sci. USA 107, 7562-7567 (2010).
42. Sohya, K., Kameyama, K., Yanagawa, Y., Obata, K., & Tsumoto, T. GABAergic neurons are less selective to stimulus orientation than excitatory neurons in layer II/III of visual cortex, as revealed by in vivo functional Ca2+ imaging in transgenic mice. J. Neurosci. 27, 2145-2149 (2007).
43. Kerlin, A.M., Andermann, M.L., Berezovskii, V.K., & Reid, R.C. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67, 858-871 (2010).
44. Hofer, S.B., et al. Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat. Neurosci. 14, 1045-1052 (2011).
45. Hooks, B.M., & Chen, C. Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52, 281-291 (2006).
46. Marshel, J.H., Kaye, A.P., Nauhaus, I., & Callaway, E.M. Anterior-posterior direction opponency in the superficial mouse lateral geniculate nucleus. Neuron 76, 713-720 (2012).
47. Li, Y.T., Ibrahim, L.A., Liu, B.H., Zhang, L.I., & Tao, H.W. Linear transformation of thalamocortical input by intracortical excitation. Nat. Neurosci. 16, 1324-1330 (2013).
48. Cruz-Martín, A., et al. A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. Nature 507, 358-361 (2014).
49. Elstrott, J., et al. Direction selectivity in the retina is established independent of visual experience and cholinergic retinal waves. Neuron 58, 499-506 (2008).
50. Smith, G.B., & Fitzpatrick, D. Specifying cortical circuits: a role for cell lineage. Neuron 75, 4-5 (2012).
51. Shcherbo, D., et al. Bright far-red fluorescent protein for whole-body imaging. Nat. Methods 4, 741-746 (2007).
52. Drobizhev, M., Makarov, N.S., Tillo, S.E., Hughes, T.E., & Rebane, A. Two-photon absorption properties of fluorescent proteins. Nat. Methods 8, 393-399 (2011).
53. Mizuno, H., Hirano, T., & Tagawa, Y. Pre-synaptic and post-synaptic neuronal activity supports the axon development of callosal projection neurons during different post-natal periods in the mouse cerebral cortex. Eur. J. Neurosci. 31, 410-424 (2010).
54. Hagihara, K.M., & Ohki, K. Long-Derm down-regulation of GABA decreases orientation selectivity without affecting direction selectivity in mouse primary visual cortex. Front. Neural Circuits 7, 28 (2013).
55. Peirce, J.W. PsychoPy-Psychophysics software in Python. J. Neurosci. Methods 162, 8-13 (2007).
56. Helmchen, F., Imoto, K., & Sakmann, B. Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. Biophys. J. 70, 1069-1081 (1996).
57. Kitamura, K., Judkewitz, B., Kano, M., Denk, W., & Hausser, M. Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat. Methods 5, 61-67 (2008).
58. Komai, S., Denk, W., Osten, P., Brecht, M., & Margrie, T.W. Two-photon targeted patching (TPTP) in vivo. Nat. Protoc. 1, 647-652 (2006).
59. Glass, G.V., Peckham, P.D., & Sanders, J.R. Consequences of failure to meet the assumptions underlying the fixed effects analysis of variance and covariance. Rev. Educ. Res. 42, 237-288 (1972).