Abstract
Many objects in natural visual scenes compete for attention. To identify the neural mechanisms necessary for visual attention, we made restricted lesions, affecting different quadrants of the visual field but leaving one quadrant intact, in extrastriate cortical areas V4 and TEO of two monkeys. Monkeys were trained to discriminate the orientation of a target grating surrounded by distracters. As distracter contrast increased, performance deteriorated in quadrants affected by V4 and TEO lesions, but not in the normal quadrant. Performance in affected quadrants was restored by increasing the contrast of the target relative to distracters. Thus, without V4 and TEO, visual attention is 'captured' by strong stimuli, regardless of their behavioral relevance.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Desimone, R. & Ungerleider, L. G. in Handbook of Neuropsychology Vol. 2 (eds. Boller, F. & Grafman, J.), 267– 296 (Elsevier, New York, 1989).
Zeki, S. M. The representation of colours in the cerebral cortex. Nature 284, 412–418 (1980).
Desimone, R. & Schein, S. J. Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. J. Neurophysiol. 57, 835–868 ( 1987).
Schein, S. J. & Desimone, R. Spectral properties of V4 neurons of the macaque. J. Neurosci. 10, 3369– 3389 (1990).
Gallant, J. L., Braun, J. & Van Essen, D. C. Selectivity for polar, hyperbolic and cartesian gratings in macaque visual cortex. Science 259, 100 –103 (1993).
Kobatake, E. & Tanaka, K. Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. J. Neurophysiol. 71, 856– 867 (1994).
Gross, C. G., Rocha-Miranda, C. E. & Bender, D. B. Visual properties of neurons in inferotemporal cortex of the macaque. J. Neurophysiol. 35, 96– 111 (1972).
Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. Stimulus selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051–2062 (1984).
Perrett, D. I., Rolls, E. T. & Caan, W. Visual neurons responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47, 329– 342 (1982).
Fujita, I., Tanaka, K., Ito, M. & Cheng, K. Columns for visual features of objects in monkey inferotemporal cortex. Nature 360, 343–346 (1992).
Komatsu, H. & Ideura, Y. Relationships between color, shape, and pattern selectivities of neurons in the inferior temporal cortex of the monkey. J. Neurophysiol. 70, 677– 694 (1993).
Miyashita, Y., Date, A. & Okuna, H. Configurational encoding of complex visual forms by single neurons of monkey temporal cortex. Neuropsychologia 31, 1119 –1131 (1993).
Sary, G., Vogels, R. & Orban, G. A. Cue-invariant shape selectivity of macaque inferior temporal neurons. Science 260, 995– 997 (1993).
Wild, H. M., Butler, S. R., Carden, D. & Kulikowski, J. J. Primate cortical area V4 important for colour constancy but not wavelength discrimination. Nature, 313, 133– 135 (1985).
Heywood, C. A., Gadotti, A. & Cowey, A. Cortical area V4 and its role in the perception of color. J. Neurosci. 12, 4056– 4065 (1992).
Schiller, P. H. & Lee, K. The role of the primate area V4 in vision. Science 251, 1251– 1253 (1991).
Schiller, P. H. The effects of V4 and middle temporal (MT) lesions on visual performance in the rhesus monkey. Vis. Neurosci. 10, 717 –746 (1993).
Walsh, V., Butler, S. R., Carden, D. & Kulikowski, J. J. The effects of V4 lesions on the visual abilities of macaques: shape discrimination. Behav. Brain Res. 50, 115– 126 (1992).
Merigan, W. H. Basic visual capacities and shape discrimination after lesions of extrastriate area V4 in macaques. Vis. Neurosci. 13, 51–60 (1996).
De Weerd, P., Desimone, R. & Ungerleider, L. G. Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques. Vis. Neurosci. 13, 529–538 (1996).
Iwai, E. & Mishkin, M. Further evidence on the locus of the visual area in the temporal lobe of the monkey. Exp. Neurol. 25, 585–594 ( 1969).
Cowey, A. & Gross, C. G. Effects of foveal prestriate and inferotemporal lesions on visual discrimination by rhesus monkeys. Exp. Brain Res. 11, 128–144 (1970).
Dean, P. Effects of inferotemporal lesions on the behavior of monkeys. Psychol. Bull. 83, 41–71 (1976).
Dean, P. Visual cortex ablation and thresholds for successively presented stimuli in rhesus monkeys: I. Orientation. Exp. Brain Res. 32, 445–458 (1978).
Gaffan, D., Harrison, S. & Gaffan, E. A. Visual identification following inferotemporal ablation in the monkey. Q. J. Exp. Psychol. B 38, 5–30 (1986).
Britten, K., Newsome, W. T. & Saunders, R. C. Effects of inferotemporal cortex lesions on form-from-motion discrimination in monkeys. Exp. Brain Res. 88, 292–302 (1992).
Driver, J. & Baylis, G. C. Movement and visual attention: the spotlight metaphor breaks down. J. Exp. Psychol. Hum. Percept. Perform. 15, 448–456 ( 1989).
Duncan, J. & Humphreys, G.W. Visual search and stimulus similarity. Psychol. Rev. 96, 433– 458 (1989).
Posner, M. I. Orienting of attention. Q. J. Exp. Psychol. 32, 3–25 (1980).
Treisman, A. M. Strategies and models of selective attention. Psychol. Rev. 76, 282–299 (1969).
Chelazzi, L., Miller, E. K., Duncan, J. & Desimone, R. A neural basis for visual search in inferior temporal cortex. Nature 363, 345–347 ( 1993).
Connor, C. E., Gallant, J. L., Preddie, D. C. & Van Essen, D. C. Responses in area V4 depend on the spatial relationship between stimulus and attention. J. Neurophysiol. 3, 1306– 1308 (1996).
Luck, S. J., Chelazzi, L., Hillyard, S. A. & Desimone, R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77, 24–42 (1997).
Moran, J. & Desimone, R. Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784 (1985).
Motter, B. C. Focal attention produces spatially selective processing in visual cortical areas V1, V2 and V4 in the presence of competing stimuli. J. Neurophysiol. 70, 909–919 ( 1993).
Reynolds, J. H. Chelazzi, L. & Desimone, R. Competitive mechanisms subserve attention in macaque areas V2 and V4. J. Neurosci. 19, 1736– 1753 (1999).
Groh, J. M., Seidemann, E. & Newsome, W. T. Neurophysiology: Neural fingerprints of visual attention. Curr. Biol. 16, 1406–1409 (1996).
Treue, S. & Maunsell, J. H. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382, 539–541 (1996).
Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193– 222 (1995).
Distler, C., Boussaoud, D., Desimone, R. & Ungerleider, L. G. Cortical connections of inferior temporal area TEO in macaque monkeys. J. Comp. Neurol. 334, 125–150 (1993).
Nakamura, H., Gattass, R., Desimone, R. & Ungerleider, L. G. The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques. J. Neurosci. 13, 3681– 3691 (1993).
Desimone, R., Fleming, J. & Gross, C. G. Prestriate afferents to inferior temporal cortex: an HRP study. Brain Res. 184, 41– 55 (1980).
Gattass, R., Sousa, A. P. & Gross, C. G. Visuotopic organization and extent of V3 and V4 of the macaque. J. Neurosci. 8, 1831– 1845 (1988).
Boussaoud, D., Desimone, R. & Ungerleider, L. G. Visual topography of area TEO in the macaque. J. Comp. Neurol. 306, 554–575 (1991).
Kastner, S., De Weerd, P., Desimone, R. & Ungerleider, L. G. Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. Science 282, 108– 111 (1998).
Julesz, B. Texton gradients: the texton theory revisited. Biol. Cybern. 54, 245–251 (1986).
Treisman, A. M. A feature-integration theory of attention. Cogn. Psychol. 12, 97–136 (1980).
Wolfe, J. M. Guided search: an alternative to the feature integration model for visual search. J. Exp. Psychol. Hum. Percept. Perform. 15, 419–433 (1989).
Robinson, D. A. A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans. Biomed. Eng. 10, 137– 145 (1963).
Wetherill, G. B. & Levitt, R. Sequential estimation of points on a psychometrical function. Br. J. Math. Stat. Psychol. 18, 1–10 (1965 ).
Acknowledgements
We are grateful to R. Hoag and M. Rogell for help with the behavioral testing of the monkeys, T. Galkin for help in reconstructing the lesions and G. Bertini, B. Jagadeesh, S. Kastne, and J. Reynolds for discussions of the data.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
DeWeerd, P., Peralta, M., Desimone, R. et al. Loss of attentional stimulus selection after extrastriate cortical lesions in macaques. Nat Neurosci 2, 753–758 (1999). https://doi.org/10.1038/11234
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/11234
This article is cited by
-
In Memory of Leslie G. Ungerleider
Neuroscience Bulletin (2021)
-
Rhythmic fluctuations of saccadic reaction time arising from visual competition
Scientific Reports (2018)
-
Thalamic functions in distributed cognitive control
Nature Neuroscience (2017)
-
Attention-dependent reductions in burstiness and action-potential height in macaque area V4
Nature Neuroscience (2013)
-
Stimulus detection after interruption of the feedforward response in a backward masking paradigm
Cognitive Neurodynamics (2012)