BOLD responses in human V1 to local structure in natural scenes: Implications for theories of visual coding

Journal of Vision

Volumn 13, Issue 2, 2013, Pages

  Rieger, Jochem W ^a   Gegenfurtner, Karl R ^b   Schalk, Franziska ^c   Koechy, Nick ^c   Heinze, Hans Jochen ^c   Grueschow, Marcus ^d  

^a UNIVERSITY OF OLDENBURG   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Contrast energy coding; fMRI; MEG; Natural scenes; Sparse coding

Indexed keywords

ARTICLE; COMPARATIVE STUDY; CONTRAST SENSITIVITY; FEMALE; HUMAN; MAGNETOENCEPHALOGRAPHY; MALE; METHODOLOGY; NERVE CELL; PHOTOSTIMULATION; PHYSIOLOGY; VISION; VISUAL CORTEX; VISUAL FIELD;

CONTRAST SENSITIVITY; FEMALE; HUMANS; MAGNETOENCEPHALOGRAPHY; MALE; NEURONS; PHOTIC STIMULATION; VISUAL CORTEX; VISUAL FIELDS; VISUAL PERCEPTION;

MLCS; MLOWN;

EID: 84878357026     PISSN: None     EISSN: 15347362     Source Type: Journal    
DOI: 10.1167/13.2.19     Document Type: Article

References (62)

1. Albrecht, D. G., & Hamilton, D. B. (1982). Striate cortex of monkey and cat: Contrast response function. Journal of Neurophysiology, 48(1), 217-237. [PubMed]
2. Atick, J. J., & Redlich, A. N. (1992). What does the retina know about natural scenes?. Neural Computation, 4(2), 196-210.
3. Attwell, D., & Laughlin, S. B. (2001). An energy budget for signaling in the grey matter of the brain. Journal of Cerebral Blood Flow & Metabolism, 21(10), 1133-1145. [PubMed]
4. Baddeley, R., Abbott, L. F., Booth, M. C. A., Sengpiel, F., Freeman, T., Wakeman, E. A., et al. (1997). Responses of neurons in primary and inferior temporal visual cortices to natural scenes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 264(1389), 1775-1783, doi:10. 1098/rspb.1997.0246. [PubMed]
5. Bell, A. J., & Sejnowski, T. J. (1997). The "independent components" of natural scenes are edge filters. Vision Research, 37(23), 3327-3338. [PubMed]
6. Bethge, M. (2006). Factorial coding of natural images: How effective are linear models in removing higherorder dependencies?. Journal of the Optical Society of America A, 23(6), 1253-1268, doi:10.1364/ JOSAA.23.001253.
7. Chklovskii, D. B., & Koulakov, A. A. (2004). Maps in the brain: What can we learn from them?. Annual Review of Neuroscience, 27, 369-392. [PubMed]
8. Dakin, S. C., Hess, R. F., Ledgeway, T., & Achtman, R. L. (2002). What causes non-monotonic tuning of fMRI response to noisy images?. Current Biology, 12(14), R476-R478. [PubMed]
9. Davis, T. L., Kwong, K. K., Weisskoff, R. M., & Rosen, B. R. (1998). Calibrated functional MRI: Mapping the dynamics of oxidative metabolism. Proceedings of the National Academy of Sciences, 95(4), 1834-1839. [PubMed]
10. De Valois, R. L., Albrecht, D. G., & Thorell, L. G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research, 22(5), 545-559, doi:10.1016/0042-6989(82)90113-4. [PubMed]
11. De Valois, R. L. D., & De Valois, K. K. D. (1990). Spatial vision. New York: Oxford University Press.
12. Dumoulin, S. O., Dakin, S. C., & Hess, R. F. (2008). Sparsely distributed contours dominate extra-striate responses to complex scenes. Neuroimage, 42(2), 890-901. [PubMed]
13. Engel, S. A., Rumelhart, D. E., Wandell, B. A., Lee, A. T., Glover, G. H., Chichilnisky, E. J., et al. (1994). fMRI of human visual cortex. Nature, 369(6481), 525, doi:10.1038/369525a0. [PubMed]
14. Felsen, G., Touryan, J., Han, F., & Dan, Y. (2005). Cortical sensitivity to visual features in natural scenes. PLoS Biology, 3(10), e342. [PubMed]
15. Field, D. J. (1987). Relations between the statistics of natural images and the response properties of cortical cells. Journal of the Optical Society of America A, 4(12), 2379-2394.
16. Field, D. J. (1993). Scale-invariance and self-similar 'wavelet' transforms: An analysis of natural scenes and mammalian visual systems. In M. Farge, J. Hunt, & J. C. Vassilicos (Eds.), Wavelets, fractals and Fourier transform: New developments and new applications (pp. 151-193). Oxford, U.K.: Oxford University Press.
17. Field, D. J. (1994). What is the goal of sensory coding?. Neural Computation, 6(4), 559-601.
18. Földiak, P. (2002). Sparse coding in the primate cortex. In M. A. Arbib (Ed.), The handbook of brain theory and neural networks, 2nd Ed. (pp. 1064-1068). Cambridge, MA: MIT Press.
19. Goense, J., & Logothetis, N. K. (2010). Physiological basis of the BOLD signal. In M. Ullsperger & S. Debener (Eds.), Simultaneous EEG and fMRI: Recording, analysis, and application (pp. 21-46). New York: Oxford University Press.
20. Graham, D. J., & Field, D. J. (2009). Natural images: Coding efficiency. Encyclopedia of Neuroscience (pp. 19-27). Oxford: Academic Press.
21. Griffeth, V. E. M., & Buxton, R. B. (2011). A theoretical framework for estimating cerebral oxygen metabolism changes using the calibrated-BOLD method: Modeling the effects of blood volume distribution, hematocrit, oxygen extraction fraction, and tissue signal properties on the BOLD signal. NeuroImage, 58(1), 198-212, doi:10.1016/j. neuroimage.2011.05.077. [PubMed]
22. Hancock, P., Baddeley, R., & Smith, L. (1992). The principal components of natural images. Network: Computation in Neural Systems, 3(1), 61-70, doi:10. 1088/0954-898X/3/1/008.
23. Heeger, D. J. (1992). Normalization of cell responses in cat striate cortex. Visual Neuroscience, 9(02), 181-197, doi:10.1017/S0952523800009640. [PubMed]
24. Honey, C., Kirchner, H., & VanRullen, R. (2008). Faces in the cloud: Fourier power spectrum biases ultrarapid face detection. Journal of Vision, 8(12):9, 1-13, http://www.journalofvision.org/content/8/12/9, doi:10.1167/8.12.9. [PubMed] [Article]
25. Hyvärinen, A., Hurri, J., & Hoyer, P. O. (2009). Sparse coding and simple cells. Natural Image Statistics: Computational Imaging and Vision, 39, 131-150.
26. Johnson, J. S., & Olshausen, B. A. (2003). Timecourse of neural signatures of object recognition. Journal of Vision, 3(7):4, 499-512, http://www.journalofvision.org/content/3/7/4, doi:10.1167/3.7. 4. [PubMed] [Article]
27. Kanowski, M., Rieger, J. W., Noesselt, T., Tempelmann, C., & Hinrichs, H. (2007). Endoscopic eye tracking system for fMRI. Journal of Neuroscience Methods, 160(1), 10-15. [PubMed]
28. Kersten, D. (1987). Predictability and redundancy of natural images. Journal of the Optical Society of America A, 4(12), 2395-2400, doi:10.1364/JOSAA. 4.002395. [PubMed]
29. Laughlin, S. B., & Sejnowski, T. J. (2003). Communication in neuronal networks. Science, 301(5641), 1870-1874, doi:10.1126/science.1089662. [PubMed]
30. Lennie, P. (2003). The cost of cortical computation. Current Biology, 13(6), 493-497, doi:10.1016/S0960-9822(03)00135-0. [PubMed]
31. Levy, W. B., & Baxter, R. A. (1996). Energy efficient neural codes. Neural Computation, 8(3), 531-543, doi:10.1162/neco.1996.8.3.531. [PubMed]
32. Logothetis, N. K., & Wandell, B. A. (2004). Interpreting the BOLD signal. Annual Review of Physiology, 66(1), 735-769, doi:10.1146/annurev. physiol.66.082602.092845. [PubMed]
33. Martínez, A., Di Russo, F., Anllo-Vento, L., & Hillyard, S. A. (2001). Electrophysiological analysis of cortical mechanisms of selective attention to high and low spatial frequencies. Clinical Neurophysiology, 112(11), 1980-1998, doi:10.1016/S1388-2457(01)00660-5. [PubMed]
34. Movshon, J. A., Thompson, I. D., & Tolhurst, D. J. (1978). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. The Journal of Physiology, 283(1), 53-77. [PubMed]
35. Miller, A. K., Alston, R. L. & Corsellis, J. A. (1980). Variation with age in the volumes of grey and white matter in the cerebral hemispheres of man: Measurements with an image analyser. Neuropathology and Applied Neurobiology, 6, 119-132. [PubMed]
36. Murakami, S., & Okada, Y. (2006). Contributions of principal neocortical neurons to magnetoencephalography and electroencephalography signals. The Journal of Physiology, 575(3), 925-936, doi:10. 1113/jphysiol.2006.105379. [PubMed]
37. Noesselt, T., Hillyard, S. A., Woldorff, M. G., Schoenfeld, A., Hagner, T., Jäncke, L., et al. (2002). Delayed striate cortical activation during spatial attention. Neuron, 35(3), 575-587, doi:16/S0896-6273(02)00781-X. [PubMed]
38. Nunez, P. L., & Silberstein, R. B. (2000). On the relationship of synaptic activity to macroscopic measurements: Does co-registration of EEG with fMRI make sense?. Brain Topography, 13(2), 79-96, doi:10.1023/A:1026683200895. [PubMed]
39. Olman, C. A., Ugurbil, K., Schrater, P., & Kersten, D. (2004). BOLD fMRI and psychophysical measurements of contrast response to broadband images. Vision Research, 44(7), 669-683, doi:10.1016/j. visres.2003.10.022. [PubMed]
40. Olshausen, B. A., & Field, D. J. (1996). Emergence of simple-cell receptive field properties by learning a sparse code for natural images. Nature, 381, 607-609, doi:10.1038/381607a0. [PubMed]
41. Olshausen, B. A., & Field, D. J. (2004). Sparse coding of sensory inputs. Current Opinion in Neurobiology, 14(4), 481-487, doi:10.1016/j.conb.2004.07.007. [PubMed]
42. Olshausen, B. A., & Field, D. J. (1997). Sparse coding with an overcomplete basis set: A strategy employed by V1?. Vision Research, 37(23), 3311-3325. [PubMed]
43. Perna, A., Tosetti, M., Montanaro, D., & Morrone, M. C. (2008). BOLD response to spatial phase congruency in human brain. Journal of Vision, 8(10):15, 1-15, http://www.journalofvision.org/content/8/10/15, doi:10.1167/8.10.15. [PubMed] [Article]
44. Philiastides, M. G., & Sajda, P. (2006). Temporal characterization of the neural correlates of perceptual decision making in the human brain. Cerebral Cortex, 16(4), 509-518, doi:10.1093/cercor/bhi130. [PubMed]
45. Rainer, G., Augath, M., Trinath, T., & Logothetis, N. K. (2001). Nonmonotonic noise tuning of BOLD fMRI signal to natural images in the visual cortex of the anesthetized monkey. Current Biology, 11(11), 846-854, doi:10.1016/S0960-9822(01)00242-1. [PubMed]
46. Rieger, J. W., Köchy, N., Schalk, F., Grüschow, M., & Heinze, H.-J. (2008). Speed limits: Orientation and semantic context interactions constrain natural scene discrimination dynamics. Journal of Experimental Psychology: Human Perception and Performance, 34(1), 56-76, doi:10.1037/0096-1523.34.1. 56. [PubMed]
47. Rieger, J. W., Reichert, C., Gegenfurtner, K. R., Noesselt, T., Braun, C., Heinze, H.-J., et al. (2008). Predicting the recognition of natural scenes from single trial MEG recordings of brain activity. NeuroImage, 42(3), 1056-1068, doi:10.1016/j. neuroimage.2008.06.014. [PubMed]
48. Rozell, C. J., Johnson, D. H., Baraniuk, R. G., & Olshausen, B. A. (2008). Sparse coding via thresholding and local competition in neural circuits. Neural Computation, 20(10), 2526-2563. [PubMed]
49. Sadr, J., & Sinha, P. (2004). Object recognition and random image structure evolution. Cognitive Science, 28(2), 259-287.
50. Schwartz, O., & Simoncelli, E. P. (2001). Natural signal statistics and sensory gain control. Nature Neuroscience, 4(8), 819-825, doi:10.1038/90526. [PubMed]
51. Sokoloff, L. (1977). Relation between physiological function and energy metabolism in the central nervous system. Journal of Neurochemistry, 29(1), 13-26, doi:10.1111/j.1471-4159.1977.tb03919.x. [PubMed]
52. Thomson, M. G. A., Foster, D. H., & Summers, R. J. (2000). Human sensitivity to phase perturbations in natural images: A statistical framework. Perception, 29(9), 1057-1069, doi:10.1068/p2867.
53. Tjan, B. S., Lestou, V., & Kourtzi, Z. (2006). Uncertainty and invariance in the human visual cortex. Journal of Neurophysiology, 96(3), 1556-1568, doi:10.1152/jn.01367.2005. [PubMed]
54. Tolhurst, D. J. (1972). Adaptation to square-wave gratings: Inhibition between spatial frequency channels in the human visual system. Journal of Physiology-London, 226, 231-248. [PubMed]
55. van Hateren, J. H., & van der Schaaf, A. (1998). Independent component filters of natural images compared with simple cells in primary visual cortex. Proceedings of the Royal Society of London. Series B: Biological Sciences, 265(1394), 359-366, doi:10. 1098/rspb.1998.0303. [PubMed]
56. VanRullen, R., & Thorpe, S. J. (2002). Surfing a spike wave down the ventral stream. Vision Research, 42, 2593-2615. [PubMed]
57. Vinje, W. E., & Gallant, J. L. (2002). Natural stimulation of the nonclassical receptive field increases information transmission efficiency in V1. The Journal of Neuroscience, 22(7), 2904-2915. [PubMed]
58. Vinje, W. E., & Gallant, J. L. (2000). Sparse coding and decorrelation in primary visual cortex during natural vision. Science, 287(5456), 1273. [PubMed]
59. Wandell, B. A. (1995). Foundations of vision. Sunderland, MA: Sinauer Associates.
60. Weliky, M., Fiser, J., Hunt, R. H., & Wagner, D. N. (2003). Coding of natural scenes in primary visual cortex. Neuron, 37(4), 703-718. [PubMed]
61. Wichmann, F. A., Braun, D. I., & Gegenfurtner, K. R. (2006). Phase noise and the classification of natural images. Vision Research, 46(8-9), 1520-1529, doi: 10.1016/j.visres.2005.11.008. [PubMed]
62. Willmore, B., & Tolhurst, D. J. (2001). Characterizing the sparseness of neural codes. Network: Computation in Neural Systems, 12(3), 255-270. [PubMed]