Natural stimulus statistics alter the receptive field structure of V1 neurons

Journal of Neuroscience

Volumn 24, Issue 31, 2004, Pages 6991-7006

  David, Stephen V ^a   Vinje, William E ^a   Gallant, Jack L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Inhibition; Natural vision; Nonlinear model; Receptive field; Reverse correlation; Striate cortex

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CELL STRUCTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; MACACA; MALE; MODEL; NONHUMAN; PREDICTION; PRIORITY JOURNAL; RECEPTIVE FIELD; STIMULUS RESPONSE; VISION; VISUAL CORTEX; VISUAL STIMULATION;

ANIMALS; FOURIER ANALYSIS; MACACA; MALE; MODELS, NEUROLOGICAL; PHOTIC STIMULATION; VISUAL CORTEX;

EID: 3843090696     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1422-04.2004     Document Type: Article

References (59)

1. Adelson EH, Bergen JR (1985) Spatiotemporal energy models for the perception of motion. J Opt Soc Am 2:284-299.
2. Aertsen AMHJ, Johannesma PIM (1981) A comparison of the spectrotemporal sensitivity of auditory neurons to tonal and natural stimuli. Biol Cybern 42:145-156.
3. Albrecht DG, Geisler WS (1991) Motion selectivity and the contrastresponse function of simple cells in the visual cortex. Vis Neurosci 7:531-546.
4. Barlow HB (1961) Possible principles underlying the transformation of sensory messages. In: Sensory communication (Rosenbluth WA, ed), pp 217-234. Cambridge, MA: MIT.
5. Bauman LA, Bonds AB (1991) Inhibitory refinement of spatial frequency selectivity in single cells of the cat striate cortex. Vision Res 31:933-944.
6. Bonds AB (1989) Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Vis Neurosci 2:41-55.
7. Brillinger DJ (1996) Some uses of cumulants in wavelet analysis. J Nonparametric Stat 6:93-114.
8. Carandini M, Heeger DJ, Movshon JA (1997) Linearity and normalization in simple cells of the macaque primary visual cortex. J Neurosci 17:8621-8644.
9. Chance FS, Nelson SB, Abbott LF (1998) Synaptic depression and the temporal response characteristics of V1 cells. J Neurosci 18:4785-4799.
10. Dan Y, Atick JJ, Reid RC (1996) Efficient coding of natural scenes in the lateral geniculate nucleus: experimental test of a computational theory. J Neurosci 16:3351-3362.
11. Daugman JG (1980) Two-dimensional spectral analysis of cortical receptive field profiles. Vision Res 20:847-856.
12. David SV, Vinje WE, Gallant JL (1999) Natural image reverse correlation in awake behaving primates. Soc Neurosci Abstr 25:767.22.
13. DeAngelis GC, Ohzawa I, Freeman RD (1993) Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. J Neurophysiol 69:1118-1135.
14. DeAngelis GC, Ohzawa I, Freeman RD (1995) Receptive field dynamics in the central visual pathways. Trends Neurosci 18:451-458.
15. DeBoer E, Kuyper P (1968) Triggered correlation. IEEE Trans Biomed Eng 15:159-179.
16. DeValois RL, Albrecht DG, Thorell LG (1982) Spatial frequency selectivity of cells in macaque visual cortex. Vision Res 22:545-559.
17. Efron B, Tibshirani R (1986) Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Stat Sci 1:54-77.
18. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck RR (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412:787-792.
19. Field DJ (1987) Relations between the statistics of natural images and the response properties of cortical cells. J Opt Soc Am [A] 4:2379-2394.
20. Field DJ (1993) Scale-invariance and self-similar "wavelet" transforms: an analysis of natural scenes and mammalian visual systems. In: Wavelets, fractals, and Fourier transforms (Farge M, Hunt JCR, Vascillicos JC, eds), pp 151-193. New York: Clarendon.
21. Gallant JL (2003) Neural mechanisms of natural scene perception. In: The visual neurosciences (Chalupa LM, Werner JS, eds), pp 1590-1602. Boston: MIT.
22. Gilbert CD, Wiesel TN (1990) The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Vision Res 30:1689-1701.
23. Hubel DH, Wiesel TN (1959) Receptive fields of single neurones in the cat's striate cortex. J Physiol (Lond) 148:574-591.
24. Jones JP, Stepnoski A, Palmer LA (1987) The two-dimensional spectral structure of simple receptive fields in cat striate cortex. J Neurophysiol 58:1212-1232.
25. Lesica NA, Boloori AS, Stanley GB (2003) Adaptive encoding in the visual pathway. Network 14:119-135.
26. Machens CK, Wehr MS, Zador AM (2004) Linearity of cortical receptive fields measured with natural sounds. I Neurosci 24:1089-1100.
27. Mancini M, Madden BC, Emerson RC (1990) White noise analysis of temporal properties in simple receptive fields of cat cortex. Biol Cybern 63:209-219.
28. Marmarelis PZ, Marmarelis VZ (1978) Analysis of physiological systems: the white noise approach. New York: Plenum.
29. Mazer JA, David SV, Gallant JL (2000) Spatiotemporal receptive field estimation during free viewing visual search in macaque striate and extrastriate cortex. Soc Neurosci Abstr 26:53.15.
30. Mazer JA, Vinje WE, McDermott J, Schiller PH, Gallant JL (2002) Spatial frequency and orientation tuning dynamics in area V1. Proc Natl Acad Sci USA 99:1645-1650.
31. Mechler F, Victor JD, Purpura KP, Shapley R (1998) Robust temporal coding of contrast by V1 neurons for transient but not steady-state stimuli. J Neurosci 18:6583-6598.
32. Movshon JA, Thompson ID, Tolhurst DJ (1978) Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J Physiol (Lond) 283:53-77.
33. Müller JR, Metha AB, Krauskopf J, Lennie P (1999) Rapid adaptation in visual cortex to the structure of images. Science 285:1405-1408.
34. Olshausen BA, Field DJ (1997) Sparse coding with an overcomplete basis set: a strategy employed by V1? Vision Res 23:3311-3325.
35. Olshausen BA, Field DJ (2004) What is the other 85% of V1 doing? In: Problems in systems neuroscience (Sejnowski TJ, van Hemmen L, eds). Oxford: Oxford UP, in press.
36. Pollen DA, Ronner SF (1983) Visual cortical neurons as localized spatial frequency filters. IEEE Trans System Man Cybern 13:907-916.
37. Reid RC, Victor JD, Shapley RM (1992) Broadband temporal stimuli decrease the integration time of neurons in cat striate cortex. Vis Neurosci 9:39-45.
38. Richmond BJ, Hertz JA, Gawne TJ (1999) The relation between human V1 neuronal responses and eye movements-like stimulus presentations. Neurocomputing 26:247-254.
39. Ringach DL, Sapiro G, Shapley R (1997) A subspace reverse-correlation technique for the study of visual neurons. Vision Res 17:2455-2464.
40. Ringach DL, Hawken MJ, Shapley R (2002) Receptive field structure of neurons in monkey primary visual cortex revealed by stimulation with natural image sequences. J Vision 2:12-24.
41. Schwartz O, Simoncelli EP (2001) Natural signal statistics and sensory gain control. Nat Neurosci 4:819-825.
42. Shapley R, Hawken M, Ringach DL (2003) Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition. Neuron 38:689-699.
43. Simoncelli EP, Olshausen BA (2001) Statistical properties of natural images. Annu Rev Neurosci 24:1193-1216.
44. Smyth D, Willmore B, Baker GE, Thompson ID, Tolhurst DJ (2003) The receptive-field organization of simple cells in primary visual cortex of ferrets under natural scene stimulation. J Neurosci 23:4746-4759.
45. Theunissen FE, Sen K, Doupe AJ (2000) Spectral-temporal receptive fields of non-linear auditory neurons obtained using natural sounds. J Neurosci 20:2315-2331.
46. Theunissen FE, David SV, Singh NC, Hsu A, Vinje WE, Gallant JL (2001) Estimating spatial temporal receptive fields of auditory and visual neurons from their responses to natural stimuli. Network 12:289-316.
47. Tolhurst DJ, Walker NS, Thompson ID, S. DA (1980) Non-linearities of temporal summation in neurones in area 17 of the cat. Exp Brain Res 38:431-435.
48. Tolhurst DJ, Movshon JA, Dean AF (1983) The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res 23:775-785.
49. Touryan J, Lau B, Dan Y (2002) Isolation of relevant visual features from random stimuli for cortical complex cells. J Neurosci 22:10811-10818.
50. Troyer TW, Krukowski AE, Priebe NJ, Miller KD (1998) Contrast-invariant orientation tuning in cat visual cortex: thalamocortical input tuning and correlation-based intracortical connectivity. J Neurosci 18:5908-5927.
51. Vinje WE, Gallant JL (1998) Modeling complex cells in an awake macaque during natural image viewing. In: Advances in neural information processing systems, Vol 10 (Jordan MI, Kearns MJ, Solla SA, eds), pp 236-242. Cambridge, MA: MIT.
52. Vinje WE, Gallant JL (2000) Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287:1273-1276.
53. Vinje WE, Gallant JL (2002) Natural stimulation of the non-classical receptive field increases information transmission efficiency in V1. J Neurosci 22:2904-2915.
54. Walker GA, Ohzawa I, Freeman RD (1999) Asymmetric suppression outside the classical receptive field of the visual cortex. J Neurosci 19:10536-10553.
55. Weliky M, Fiser J, Hunt RH, Wagner DN (2003) Coding of natural scenes in primary visual cortex. Neuron 37:703-718.
56. Willmore B, Smyth D (2003) Methods for first-order kernel estimation: simple-cell receptive fields from responses to natural scenes. Network 14:533-577.
57. Wilson HR, Humanski R (1993) Spatial frequency adaptation and gain control. Vision Res 33:1133-1149.
58. Woods M, Stringer KM, Dong DW (2001) Visual input statistics during free-viewing of natural time-varying images: a comparison across viewers and scenes. Soc Neurosci Abstr 27:821.28.
59. Zetzsche C, Barth E, Wegmann B (1993) The importance of intrinsically two-dimensional image features in biological vision and picture coding. In: Digital images and human vision (Watson A, ed), pp 109-138. Boston: MIT.