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The Journal of Neuroscience, March 3, 2004, 24(9):2065-2076; doi:10.1523/JNEUROSCI.3887-03.2004
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Behavioral/Systems/Cognitive
Receptive Field Size in V1 Neurons Limits Acuity for Perceiving Disparity Modulation
Hendrikje Nienborg,1
Holly Bridge,2
Andrew J. Parker,2 and
Bruce G. Cumming1
1Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892, and 2University Laboratory of Physiology, University of Oxford, Oxford OX1 3PT, United Kingdom
Disparity selectivity in the striate cortex has generally been studied with uniform disparity fields covering the receptive field (RF). In four awake behaving monkeys, we quantitatively characterized the spatial three-dimensional structure of 55 V1 RFs using random dot stereograms in which disparity varied as a sinusoidal function of vertical position ("corrugations"). At low spatial frequencies, this produced a modulation in neuronal firing at the temporal frequency of the stimulus. As the spatial frequency increased, the modulation reduced. The mean response rate changed little and was close to that produced by a uniform stimulus at the mean disparity of the corrugation. In 48 of 55 (91%) neurons, the modulation strength was a lowpass function of spatial frequency. These results are compatible with a response determined only by the weighted mean of the disparities of the dots (the weights being set by the RF envelope) and suggest that there is no disparity-based surround inhibition or selectivity for disparity gradients. This simple weighting scheme predicts a relationship between RF size and the high-frequency cutoff. Comparison with independent measurements of RF size was compatible with this. All of this behavior closely matches the binocular energy model. The mean cutoff frequency, 0.5 cycles per degree, is similar to equivalent measures of decline in human psychophysical sensitivity for such depth corrugations as a function of frequency (Tyler, 1974; Prince and Rogers, 1998; Banks et al., 2004). This suggests that human cyclopean acuity for disparity modulations is limited by the selectivity of V1 neurons. This in turn is primarily limited by the RF size, because we find no sensitivity for disparity gradients or other disparity differences within the RFs.
Key words: vision; binocular disparity; awake behaving macaque; striate cortex; stereopsis; receptive field size
Received Aug 21, 2003;
revised December 24, 2003;
accepted January 6, 2004.
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