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Spatial frequency components influence cell activity in the inferotemporal cortex

Published online by Cambridge University Press:  01 July 2009

MARIA A. BERMUDEZ*
Affiliation:
Department of Physiology, School of Medicine, University of Santiago de Compostela, Santiago de Compostela, Spain
ANA F. VICENTE
Affiliation:
Department of Physiology, School of Medicine, University of Santiago de Compostela, Santiago de Compostela, Spain
MARIA C. ROMERO
Affiliation:
Department of Physiology, School of Medicine, University of Santiago de Compostela, Santiago de Compostela, Spain
ROGELIO PEREZ
Affiliation:
Department of Physiology, School of Medicine, University of Santiago de Compostela, Santiago de Compostela, Spain Service of Ophthalmology, Hospital of Monforte, Monforte de Lemos, Spain
FRANCISCO GONZALEZ
Affiliation:
Department of Physiology, School of Medicine, University of Santiago de Compostela, Santiago de Compostela, Spain Service of Ophthalmology, University Hospital, Santiago de Compostela, Spain
*
*Address correspondence and reprint requests to: Maria A. Bermudez, Department of Physiology, School of Medicine, University of Santiago de Compostela, c/San Francisco s/n, Santiago de Compostela E-15782, Spain. E-mail: [email protected]

Abstract

We studied the correlation between the spatial frequency of complex stimuli and neuronal activity in the monkey inferotemporal (IT) cortex while performing a task that required visual recognition. Single-cell activity was recorded from the right IT cortex. The frequency components of the images used as stimuli were analyzed by using a fast Fourier transform, and a modulus was obtained for 40 spatial frequency ranges from 0.3 to 11.1 cycles/deg. We recorded 82 cells showing statistically significant responses (analysis of variance, P < 0.05) to at least one of the images used as a stimulus. Seventy-eight percent of these cells (n = 64) showed significant responses to at least three images, and in two thirds of them (n = 42), we found a statistically significant correlation (P < 0.05) between cell response and the modulus amplitude of at least one frequency range present in the images. Our results suggest that information about spatial frequency of the visual images is present in the IT cortex.

Type
Brief Communication
Copyright
Copyright © Cambridge University Press 2009

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References

Baylis, G.C., Rolls, E.T. & Leonard, C.M. (1985). Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey. Brain Research 342, 91102.Google Scholar
Baylis, G.C., Rolls, E.T. & Leonard, C.M. (1987). Functional subdivisions of the temporal lobe neocortex. Journal of Neuroscience 7, 330347.CrossRefGoogle ScholarPubMed
Blakemore, C. & Campbell, F.W. (1969). On the existence of neurons in the human visual system selectively sensitive to the orientation and size of retinal images. Journal of Physiology 203, 237260.CrossRefGoogle Scholar
Campbell, F.W. & Robson, J.G. (1968). Application of Fourier analysis to the visibility of gratings. Journal of Physiology 197, 551566.Google Scholar
Connor, C.E., Brincat, S.L. & Pasupathy, A. (2007). Transformation of shape information in the ventral pathway. Current Opinion in Neurobiology 17, 140147.CrossRefGoogle ScholarPubMed
Cowey, A. & Stoerig, P. (1991). The neurobiology of blindsight. Trends in Neuroscience 14, 140145.CrossRefGoogle ScholarPubMed
Damasio, A.R., Damasio, H. & Van Hoesen, G.W. (1982). Prosopagnosia: Anatomic basis and behavioral mechanisms. Neurology 32, 331341.CrossRefGoogle ScholarPubMed
Dean, P. (1976). Effects of inferotemporal lesions on the behavior of monkeys. Psychological Bulletin 83, 4171.Google Scholar
Desimone, R., Albright, T.D., Gross, C.G. & Bruce, C. (1984). Stimulus-selective properties of inferior temporal neurons in the macaque. Journal of Neuroscience 4, 20512062.CrossRefGoogle ScholarPubMed
Desimone, R., Fleming, J. & Gross, C.G. (1980). Prestriate afferents to inferior temporal cortex: An HRP study. Brain Research 184, 4155.CrossRefGoogle ScholarPubMed
Desimone, R. & Gross, C.G. (1979). Visual areas in the temporal cortex of the macaque. Brain Research 178, 363380.CrossRefGoogle ScholarPubMed
De Valois, R.L. (1978). Spatial processing of luminance and color information. Investigative Ophthalmology & Visual Science 17, 834835.Google ScholarPubMed
De Valois, R.L., Albrecht, D.G. & Thorell, L.G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545559.CrossRefGoogle ScholarPubMed
De Valois, R.L. & De Valois, K.K. (1988). Spatial Vision. New York: Oxford University Press.Google Scholar
Edwards, R., Xiao, D., Keysers, C., Foldiak, P. & Perret, D. (2003). Color sensitivity of cells responsive to complex stimuli in the temporal cortex. Journal of Neurophysiology 90, 12451256.Google Scholar
Eifuku, S., De Souza, C., Tamura, R., Nishijo, H. & Ono, T. (2004). Neuronal correlates of face identification in the monkey anterior temporal cortical areas. Journal of Neurophysiology 91, 358371.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in the primate central cortex. Cerebral Cortex 1, 147.CrossRefGoogle Scholar
Fuster, J.M. & Jervey, J.P. (1982). Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task. Journal of Neuroscience 2, 361375.CrossRefGoogle Scholar
Georgeson, M.A. (1980). Spatial frequency analysis in early visual processing. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 290, 1122.Google ScholarPubMed
Gonzalez, F., Krause, F., Perez, R., Alonso, J.M. & Acuña, C. (1993). Binocular matching in monkeys visual cortex: Single cell responses to correlated and uncorrelated dynamic random dot stereograms. Neuroscience 52, 933939.CrossRefGoogle ScholarPubMed
Goodale, M.A. & Milner, A.D. (1992). Separate visual pathways for perception and action. Trends in Neuroscience 15, 2025.Google Scholar
Gross, C.G. (1994). How inferior temporal cortex became a visual area. Cerebral Cortex 4, 455469.CrossRefGoogle ScholarPubMed
Gross, C.G. (2005). Processing the facial image: A brief history. American Psychologist 60, 755763.Google Scholar
Gross, C.G., Rocha-Miranda, C.E. & Bender, D.B. (1972). Visual properties of neurons in inferotemporal cortex of the macaque. Journal of Neurophysiology 35, 96111.Google Scholar
Hernandez-Gonzalez, A., Cavada, C. & Reinoso-Suarez, F. (1994). The lateral geniculate nucleus projects to the inferior temporal cortex in the macaque monkey. Neuroreport 5, 26932696.CrossRefGoogle Scholar
Irvin, G.E., Casagrande, V.A. & Norton, T.T. (1993). Center/surround relationships of magnocellular, parvocellular, and koniocellular relay cells in primate lateral geniculate nucleus. Visual Neuroscience 10, 363373.CrossRefGoogle ScholarPubMed
Jones, J.P. & Palmer, L.A. (1987 a). An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 12331258.CrossRefGoogle ScholarPubMed
Jones, J.P. & Palmer, L.A. (1987 b). The two-dimensional spatial structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 11871211.CrossRefGoogle ScholarPubMed
Jones, J.P., Stepnoski, A. & Palmer, L.A. (1987). The two-dimensional spectral structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 12121232.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology 330, 125143.Google Scholar
Kayaert, G., Biederman, I., Op De Beek, H.P. & Vogels, R. (2005). Tuning for shape dimensions in macaque inferior temporal cortex. European Journal of Neuroscience 22, 212224.CrossRefGoogle ScholarPubMed
Komatsu, H., Ideura, Y., Kaji, S. & Yamane, S. (1992). Color selectivity in the inferior temporal cortex of the awake macaque monkey. Journal of Neuroscience 12, 408424.Google Scholar
Kreiman, G., Hung, C.P., Kraskov, A., Quiroga, R.Q., Poggio, T. & Di Carlo, J.J. (2006). Object selectivity of local field potentials and spikes in the macaque inferior temporal cortex. Neuron 49, 433445.Google Scholar
Livingstone, M. & Hubel, D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740749.Google Scholar
Logothetis, N.K. (1998). Single unit and conscious vision. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353, 18011818.Google Scholar
Logothetis, N.K., Pauls, J. & Poggio, T. (1995). Shape representation in the inferior temporal cortex of monkeys. Current Biology 5, 552563.CrossRefGoogle ScholarPubMed
Logothetis, N.K. & Sheinberg, D.L. (1996). Visual object recognition. Annual Review of Neuroscience 19, 577621.CrossRefGoogle ScholarPubMed
Merigan, W.H., Katz, L.M. & Maunsell, J.H. (1991). The effects of parvocellular lateral geniculate lesions on the acuity and contrast of macaque monkeys. Journal of Neuroscience 11, 9941001.Google Scholar
Nakamura, K., Matsumoto, K., Mikami, A. & Kubota, K. (1994). Visual response properties of single neurons in the temporal pole of behaving monkeys. Journal of Neurophysiology 71, 12061221.CrossRefGoogle ScholarPubMed
Nakashima, T., Kaneko, K., Goto, Y., Abe, T., Mitsudo, T., Ogata, K., Makinouchi, A. & Tobimatsu, S. (2008). Early ERP components differentially extract facial features: Evidence for spatial frequency-and-contrast detectors. Neuroscience Research 62, 225235.CrossRefGoogle ScholarPubMed
Oppenheim, A.V. & Lim, J.S. (1981). The importance of phase in signals. Proceedings of the IEEE 69, 529541.Google Scholar
Pasik, T. & Pasik, P. (1973). Extrageniculostriate vision in the monkey. IV. Critical structures for light vs. no-light discrimination. Brain Research 56, 165182.CrossRefGoogle ScholarPubMed
Perez, R., Castro, A.F., Justo, M.S., Bermudez, M.A. & Gonzalez, F. (2005). Retinal correspondence of monocular receptive fields in disparity-sensitive complex cells from area V1 in the awake monkey. Investigative Ophthalmology & Visual Science 46, 15331539.CrossRefGoogle ScholarPubMed
Perrett, D., Mistlin, A. & Chitty, A. (1989). Visual neurones responsive to faces. Trends in Neuroscience 10, 358364.Google Scholar
Perrett, D.I. & Oram, M.W. (1993). The neurophysiology of shape processing. Image and Vision Computing 11, 317333.CrossRefGoogle Scholar
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 11011123.CrossRefGoogle Scholar
Pourtois, G., Dan, E.S., Grandjean, D., Sander, D. & Vuilleumier, P. (2005). Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: Time course and topographic evoked-potentials mapping. Human Brain Mapping 26, 6579.CrossRefGoogle ScholarPubMed
Riesenhuber, M. & Poggio, T. (1999). Hierarchical models of object recognition in cortex. Nature Neuroscience 2, 10191025.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583601.CrossRefGoogle ScholarPubMed
Rolls, E.T., Baylis, G.C. & Hasselmo, M.E. (1987). The responses of neurons in the cortex in the superior temporal sulcus of the monkey to band-pass spatial frequency filtered faces. Vision Research 27, 311326.CrossRefGoogle ScholarPubMed
Rolls, E.T., Baylis, G.C. & Leonard, C.M. (1985). Role of low and high spatial frequencies in the face-selective responses of neurons in the cortex in the superior temporal sulcus. Vision Research 25, 10211035.CrossRefGoogle ScholarPubMed
Rotshtein, P., Vuilleumier, P., Winston, J., Driver, J. & Dolan, R.J. (2007). Distinct and convergent visual processing of high and low spatial frecuency information in faces. Cerebral Cortex 17, 27132724.Google Scholar
Schwartz, E.L., Desimone, R., Albright, T.D. & Gross, C.G. (1983). Shape recognition and inferior temporal neurons. Proceedings of the National Academy of Sciences of the United States of America 80, 57765778.CrossRefGoogle ScholarPubMed
Sugase, Y., Yamane, S., Ueno, S. & Kawano, K. (1999). Global and fine information coded by single neurons in the temporal visual cortex. Nature 400, 869873.Google Scholar
Tanaka, K., Saito, H., Fukada, Y. & Moriya, M. (1991). Coding visual images of objects in the inferotemporal cortex of the macaque monkey. Journal of Neurophysiology 66, 170189.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two cortical visual systems. In The Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W., pp. 549586. Cambridge, MA: MIT Press.Google Scholar
Webster, M.J., Bachevalier, J. & Ungerleider, L.G. (1993). Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys. Journal of Comparative Neurology 335, 7391.CrossRefGoogle ScholarPubMed
Young, M.P. & Yamane, S. (1992). Sparse population coding of faces in the inferotemporal cortex. Science 256, 13271331.CrossRefGoogle ScholarPubMed