Mechanisms for stable, robust, and adaptive development of orientation maps in the primary visual cortex

Journal of Neuroscience

Volumn 33, Issue 40, 2013, Pages 15747-15766

  Stevens, Jean Luc R ^a   Law, Judith S ^a   Antolík, Ján ^a,b   Bednar, James A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b Unite de Neurosciences Integratives et Computationnelles   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL EXPERIMENT; ARTICLE; CONNECTOME; EVOKED VISUAL RESPONSE; FERRET; GENETIC STABILITY; GENICULATE NUCLEUS; HOMEOSTASIS; LEARNING; NERVE CELL PLASTICITY; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA GANGLION CELL; SPATIAL ORIENTATION; SPIKE WAVE; VISUAL CORTEX; VISUAL DISCRIMINATION; VISUAL ORIENTATION; VISUAL STIMULATION;

ANIMALS; BRAIN MAPPING; CATS; FERRETS; GENICULATE BODIES; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEURONS; ORIENTATION; RETINAL GANGLION CELLS; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84884913611     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1037-13.2013     Document Type: Article

References (93)

1. Alitto HJ, Usrey WM (2004) Influence of contrast on orientation and temporal frequency tuning in ferret primary visual cortex. J Neurophysiol 91:2797-2808. CrossRef Medline
2. Alitto HJ, Usrey WM (2008) Origin and dynamics of extraclassical suppression in the lateral geniculate nucleus of the macaque monkey. Neuron 57:135-146. CrossRef Medline
3. Anderson JS, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84:909-926. Medline
4. Antolík J (2010) Unified developmental model of maps, complex cells and surround modulation in the primary visual cortex. PhD thesis, School of Informatics, The University of Edinburgh, Edinburgh, UK.
5. Antolík J, Bednar JA (2011) Development of maps of simple and complex cells in the primary visual cortex. Front Comput Neurosci 5:17. Medline
6. Baccus SA, Meister M (2002) Fast and slow contrast adaptation in retinal circuitry. Neuron 36:909-919. CrossRef Medline
7. Barrow HG, Bray AJ, Budd JM (1996) A self-organizing model of 'color blob' formation. Neural Comput 8:1427-1448. CrossRef Medline
8. Beckmann R, Albus K (1982) The geniculocortical system in the early postnatal kitten: an electrophysiological investigation. Exp Brain Res 47:49-56. Medline
9. Bednar JA, Miikkulainen R (2004) Prenatal and postnatal development of laterally connected orientation maps. Neurocomputing 58-60:985-992.
10. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32-48. Medline
11. Blakemore C, Cooper GF (1970) Development of the brain depends on the visual environment. Nature 228:477-478. CrossRef Medline
12. Blakemore C, Van Sluyters RC (1975) Innate and environmental factors in the development of the kitten's visual cortex. J Physiol 248:663-716. Medline
13. Blasdel GG (1992a) Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. J Neurosci 12:3115-3138. Medline
14. Blasdel GG (1992b) Orientation selectivity, preference, and continuity in monkey striate cortex. J Neurosci 12:3139-3161. Medline
15. Blasdel GG, Salama G (1986) Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321:579-585. CrossRef Medline
16. Bonin V, Mante V, Carandini M (2005) The suppressive field of neurons in lateral geniculate nucleus. J Neurosci 25:10844-10856. CrossRef Medline
17. Bosking WH, Zhang Y, Schofield B, Fitzpatrick D (1997) Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. J Neurosci 17:2112-2127. Medline
18. Burger T, Lang EW (1999) An incremental Hebbian learning model of the primary visual cortex with lateral plasticity and real input patterns. Z Naturforschung C 54:128-140. Medline
19. Burger T, Lang EW (2001) Self-organization of local cortical circuits and cortical orientation maps: a nonlinear Hebbian model of the visual cortex with adaptive lateral couplings. Z Naturforsch C 56:464-478. Medline
20. Carandini M, Heeger DJ (2012) Normalization as a canonical neural computation. Nat Rev Neurosci 13:51-62. CrossRef Medline
21. Carandini M, Heeger DJ, Senn W (2002) A synaptic explanation of suppression in visual cortex. J Neurosci 22:10053-10065. Medline
22. Chapman B, Bonhoeffer T (1998) Overrepresentation of horizontal and vertical orientation preferences in developing ferret area 17. Proc Natl Acad Sci U S A 95:2609-2614. CrossRef Medline
23. Chapman B, Gödecke I (2000) Cortical cell orientation selectivity fails to develop in the absence of ON-center retinal ganglion cell activity. J Neurosci 20:1922-1930. Medline
24. Chapman B, Stryker MP (1993) Development of orientation selectivity in ferret visual cortex and effects of deprivation. J Neurosci 13:5251-5262. Medline
25. Chapman B, Stryker MP, Bonhoeffer T (1996) Development of orientation preference maps in ferret primary visual cortex. J Neurosci 16:6443-6453. Medline
26. Coppola DM, White LE, Fitzpatrick D, Purves D (1998) Unequal representation of cardinal and oblique contours in ferret visual cortex. Proc Natl Acad Sci U S A 95:2621-2623. CrossRef Medline
27. Cragg BG (1975) The development of synapses in the visual system of the cat. J Comp Neurol 160:147-166. CrossRef Medline
28. Crair MC, Gillespie DC, Stryker MP (1998) The role of visual experience in the development of columns in cat visual cortex. Science 279:566-570. CrossRef Medline
29. Daoudal G, Debanne D (2003) Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 10:456-465. CrossRef Medline
30. Davis GW, Bezprozvanny I (2001) Maintaining the stability of neural function: a homeostatic hypothesis. Annu Rev Physiol 63:847-869. CrossRef Medline
31. Derrington AM, Lennie P (1984) Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J Physiol 357:219-240. Medline
32. Durbin R, Mitchison G (1990) A dimension reduction framework for understanding cortical maps. Nature 343:644-647. CrossRef Medline
33. Erwin E, Obermayer K, Schulten K (1995) Models of orientation and ocular dominance columns in the visual cortex: a critical comparison. Neural Comput 7:425-468. CrossRef Medline
34. Farley BJ, Yu H, Jin DZ, Sur M (2007) Alteration of visual input results in a coordinated reorganization of multiple visual cortex maps. J Neurosci 27:10299-10310. CrossRef Medline
35. Felisberti F, Derrington AM (1999) Long-range interactions modulate the contrast gain in the lateral geniculate nucleus of cats. Vis Neurosci 16: 943-956. Medline
36. Finn IM, Priebe NJ, Ferster D (2007) The emergence of contrast-invariant orientation tuning in simple cells of cat visual cortex. Neuron 54:137-152. CrossRef Medline
37. Geisler WS, Albrecht DG (1997) Visual cortex neurons in monkeys and cats: detection, discrimination, and identification. Vis Neurosci 14:897-919. CrossRef Medline
38. Gilbert CD, Hirsch JA, Wiesel TN (1990) Lateral interactions in visual cortex. Cold Spring Harb Symp Quant Biol 55:663-677. CrossRef Medline
39. Gödecke I, Kim DS, Bonhoeffer T, Singer W (1997) Development of orientation preference maps in area 18 of kitten visual cortex. Eur J Neurosci 9:1754-1762. CrossRef Medline
40. Goodhill GJ (2007) Contributions of theoretical modeling to the understanding of neural map development. Neuron 56:301-311. CrossRef Medline
41. Grubb MS, Burrone J (2010) Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 465:1070-1074. CrossRef Medline
42. Hirsch JA, Gilbert CD (1991) Synaptic physiology of horizontal connections in the cat's visual cortex. J Neurosci 11:1800-1809. Medline
43. Hooks BM, Chen C (2006) Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52:281-291. CrossRef Medline
44. Huberman AD, Speer CM, Chapman B (2006) Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in V1. Neuron 52:247-254. CrossRef Medline
45. Huberman AD, Feller MB, Chapman B (2008) Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 31: 479-509. CrossRef Medline
46. Kaschube M, Schnabel M, Löwel S, Coppola DM, White LE, Wolf F (2010) Universality in the evolution of orientation columns in the visual cortex. Science 330:1113-1116. CrossRef Medline
47. Keil W, Wolf F (2011) Coverage, continuity, and visual cortical architecture. Neural Syst Circuits 1:17. CrossRef Medline
48. Keil W, Schmidt KF, Löwel S, Kaschube M (2010) Reorganization of columnar architecture in the growing visual cortex. Proc Natl Acad Sci U S A 107:12293-12298. CrossRef Medline
49. Keil W, Kaschube M, Schnabel M, Kisvarday ZF, Lwel S, Coppola DM, White LE, Wolf F (2012) Response to comment on universality in the evolution of orientation columns in the visual cortex. Science 336:413. CrossRef
50. Kohonen T (1982) Self-organized formation of topologically correct feature maps. Biol Cybern 43:59-69. CrossRef
51. Kuba H, Oichi Y, Ohmori H (2010) Presynaptic activity regulates Na(+) channel distribution at the axon initial segment. Nature 465:1075-1078. CrossRef Medline
52. Law JS (2009) Modeling the development of organization for orientation preference in primary visual cortex. PhD thesis, School of Informatics, The University of Edinburgh, Edinburgh, UK.
53. Linsker R (1986) From basic network principles to neural architecture: Emergence of orientation columns. Proc Natl Acad Sci U S A 83:8779-8783. CrossRef Medline
54. Löwel S, Schmidt KE, Kim DS, Wolf F, Hoffsümmer F, Singer W, Bonhoeffer T (1998) The layout of orientation and ocular dominance domains in area 17 of strabismic cats. Eur J Neurosci 10:2629-2643. CrossRef Medline
55. Lütcke H, Margolis DJ, Helmchen F (2013) Steady or changing? long-term monitoring of neuronal population activity. Trends Neurosci 36:375-384. CrossRef Medline
56. Miikkulainen R, Bednar J, Choe Y, Sirosh J (2005) Computational maps in the visual cortex. New York: Springer.
57. Miller KD (1994) Amodel for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activitydependent competition between ON- and OFF-center inputs. J Neurosci 14:409-441. Medline
58. Müller T, Stetter M, Hübener M, Sengpiel F, Bonhoeffer T, Gödecke I, Chapman B, Löwel S, Obermayer K (2000) An analysis of orientation and ocular dominance patterns in the visual cortex of cats and ferrets. Neural Comput 12:2573-2595. CrossRef Medline
59. Nauhaus I, Benucci A, Carandini M, Ringach DL (2008) Neuronal selectivity and local map structure in visual cortex. Neuron 57:673-679. CrossRef Medline
60. Nauhaus I, Nielsen KJ, Disney AA, Callaway EM (2012) Orthogonal microorganization of orientation and spatial frequency in primate primary visual cortex. Nat Neurosci 15:1683-1690. CrossRef Medline
61. Obermayer K, Ritter H, Schulten K (1990) A principle for the formation of the spatial structure of cortical feature maps. Proc Natl Acad Sci U S A 87:8345-8349. CrossRef Medline
62. Ohki K, Chung S, Ch'ng YH, Kara P, Reid RC (2005) Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433:597-603. CrossRef Medline
63. Ritter H, Martinetz T, and Schulten KJ (1992) Neural computation and self-organizing maps: an introduction. Reading, MA: Addison-Wesley.
64. Rochester N, Holland JH, Haibt LH, Duda WL (1956) Tests on a cell assembly theory of the action of the brain, using a large digital computer. IRE Trans Inform Theory 2:80-93. CrossRef
65. Schulz DJ (2006) Plasticity and stability in neuronal output via changes in intrinsic excitability: it's what's inside that counts. J Exp Biol 209:4821-4827. CrossRef Medline
66. Schummers J, Mariño J, Sur M (2004) Local networks in visual cortex and their influence on neuronal responses and dynamics. J Physiol Paris 98: 429-441. CrossRef Medline
67. Sclar G (1987) Expression of "retinal" contrast gain control by neurons of the cat's lateral geniculate nucleus. Exp Brain Res 66:589-596. CrossRef Medline
68. Sclar G, Freeman RD (1982) Orientation selectivity in the cat's striate cortex is invariant with stimulus contrast. Exp Brain Res 46:457-461. Medline
69. Sengpiel F, Stawinski P, Bonhoeffer T (1999) Influence of experience on orientation maps in cat visual cortex. Nat Neurosci 2:727-732. CrossRef Medline
70. Shapley RM, Victor JD (1978) The effect of contrast on the transfer properties of cat retinal ganglion cells. J Physiol 285:275-298. Medline
71. Shouval H, Intrator N, Law CC, Cooper LN (1996) Effect of binocular cor- tical misalignment on ocular dominance and orientation selectivity. Neural Comput 8:1021-1040. CrossRef Medline
72. Sirosh J, Miikkulainen R (1994) Cooperative self-organization of afferent and lateral connections in cortical maps. Biol Cybern 71:66-78.
73. Sirosh J, Miikkulainen R (1997) Topographic receptive fields and patterned lateral interaction in a self-organizing model of the primary visual cortex. Neural Comput 9:577-594. CrossRef Medline
74. Skottun BC, Bradley A, Sclar G, Ohzawa I, Freeman RD (1987) The effects of contrast on visual orientation and spatial frequency discrimination: a comparison of single cells and behavior. J Neurophysiol 57:773-786. Medline
75. Sullivan TJ, de SaVR (2006) Homeostatic synaptic scaling in self-organizing maps. Neural Netw 19:734-743. CrossRef Medline
76. Swindale NV (1996) The development of topography in the visual cortex: a review of models. Network 7:161-247. CrossRef Medline
77. Swindale NV, Shoham D, Grinvald A, Bonhoeffer T, Hübener M (2000) Visual cortex maps are optimized for uniform coverage. Nat Neurosci 3:822-826. CrossRef Medline
78. Tanaka S, Ribot J, Imamura K, Tani T (2006) Orientation-restricted continuous visual exposure induces marked reorganization of orientation maps in early life. Neuroimage 30:462-477. CrossRef Medline
79. Tanaka S, Tani T, Ribot J, O'Hashi K, Imamura K (2009) A postnatal critical period for orientation plasticity in the cat visual cortex. PLoS ONE 4:e5380. CrossRef Medline
80. Tavazoie SF, Reid RC (2000) Diverse receptive fields in the lateral geniculate nucleus during thalamocortical development. Nat Neurosci 3:608-616. CrossRef Medline
81. Tetzlaff C, Kolodziejski C, Timme M, Wörgötter F (2011) Synaptic scaling in combination with many generic plasticity mechanisms stabilizes circuit connectivity. Front Comput Neurosci 5:47. Medline
82. Triesch J (2005) A gradient rule for the plasticity of a neuron's intrinsic excitability. In: International Conference on Artificial Neural Networks (ICANN) 2005, Lecture Notes in Computer Science, Vol 3696 (Duch W, et al., eds.), pp 65-70 Berlin: Springer-Verlag.
83. Truchard AM, Ohzawa I, Freeman RD (2000) Contrast gain control in the visual cortex: monocular versus binocular mechanisms. J Neurosci 20: 3017-3032. Medline
84. Turrigiano GG (1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22: 221-227. CrossRef Medline
85. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107. CrossRef Medline
86. von der Malsburg C (1973) Self-organization of orientation-sensitive cells in the striate cortex. Kybernetik 14:85-100. CrossRef Medline
87. Wang BS, Sarnaik R, Cang J (2010) Critical period plasticity matches binocular orientation preference in the visual cortex. Neuron 65:246-256. CrossRef Medline
88. Weliky M, Kandler K, Fitzpatrick D, Katz LC (1995) Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns. Neuron 15:541-552. CrossRef Medline
89. White LE, Fitzpatrick D (2007) Vision and cortical map development. Neuron 56:327-338. CrossRef Medline
90. White LE, Coppola DM, Fitzpatrick D (2001) The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 411:1049-1052. CrossRef Medline
91. Wiesel TN, Hubel DH (1963) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26:1003-1017. Medline
92. Wong RO (1999) Retinal waves and visual system development. Annu Rev Neurosci 22:29-47. CrossRef Medline
93. Zhang W, Linden DJ (2003) The other side of the engram: experiencedriven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4:885-900. CrossRef Medline