Spatial properties of envelope-responsive cells in area 17 and 18 neurons of the cat

1. Many neurons in areas 17 and 18 respond to spatial contrast envelope stimuli whose Fourier components fall outside the cell's spatial-frequency-selective range. The spatial properties of such envelope responses are investigated here and compared with responses to conventional luminance-defined gratings to explore the underlying receptive-field mechanism. 2. Three spatial properties of envelope responses are reported more extensively in this paper. First, the envelope responses were selective to the carrier spatial frequency in a narrow range of frequencies higher than a given cell's luminance spatial frequency selective range (luminance passband). Second, a given cell's dependence on envelope spatial frequency often differed from its luminance passband. Last, the optimal carrier spatial frequency did not shift systematically with the envelope spatial frequency, supporting the hypothesis that the carrier and envelope spatial-frequency dependencies were mediated by distinct mechanisms. 3. In contrast to the direction selectivity to the envelope motion in many envelope-responsive cells, no direction preference to carrier motion was found for envelope responses. The direction of carrier motion did not alter the direction selectivity for envelope motion, further supporting the hypothesis that the carrier and envelope temporal properties were mediated by separate mechanisms. 4. The distributions of the optimal carrier and luminance spatial frequencies among envelope-responsive cells were analyzed. The optimal carrier spatial frequencies were randomly distributed from five times the cell's optimal luminance spatial frequency to the upper resolution limit of the X-retinal ganglion cells at the same retinal eccentricity, suggesting that the selective ranges of envelope responses and luminance responses are not strongly correlated over the population of envelope-responsive cells. 5. Our data support a "two-stream" receptive-field model for envelope-responsive cells. One stream is a conventional, spatially linear receptive-field mechanism, mediating luminance responses for the cell; the other mediates envelope responses and consists of a two-stage processing: a set of spatially small and distributed nonlinear neural subunits whose outputs are spatially pooled at the second stage. 6. In conclusion, this study indicates that envelope responses in area 17 and 18 neurons cannot be due to a nonlinearity that is common to all visual stimuli before narrowband spatial-frequency-selective filtering; instead, a specialized processing stream, parallel to the conventional luminance response stream, is needed to supplement the traditional luminance processing stream in these cells. This specialized stream responds to the envelope stimuli and is selective to their carrier and envelope spatial frequencies. The distributions of the optimal luminance and carrier spatial frequencies indicate a rich variety of possible integration between luminance and envelope information.