SPATIAL PROPERTIES OF ENVELOPE-RESPONSIVE CELLS IN AREA-17 AND AREA-18 NEURONS OF THE CAT

1. Many neurons in areas 17 and 18 respond to spatial contrast envelop e stimuli whose Fourier components fall outside the cell's spatial-fre quency-selective range. The spatial properties of such envelope respon ses are investigated here and compared with responses to conventional luminance-defined gratings to explore the underlying receptive-field m echanism. 2. Three spatial properties of envelope responses are report ed more extensively in this paper. First, the envelope responses were selective to the carrier spatial frequency in a narrow range of freque ncies higher than a given cell's luminance spatial frequency selective range (luminance passband). Second, a given cell's dependence on enve lope spatial frequency often differed from its luminance passband. Las t, the optimal carrier spatial frequency did not shift systematically with the envelope spatial frequency, supporting the hypothesis that th e carrier and envelope spatial-frequency dependencies were mediated by distinct mechanisms. 3. In contrast to the direction selectivity to t he envelope motion in many envelope-responsive cells, no direction pre ference to carrier motion was found for envelope responses. The direct ion of carrier motion did not alter the direction selectivity for enve lope motion, further supporting the hypothesis that the carrier and en velope temporal properties were mediated by separate mechanisms. 4. Th e distributions of the optimal carrier and luminance spatial frequenci es 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 o f the X-retinal ganglion cells at the same retinal eccentricity, sugge sting that the selective ranges of envelope responses and luminance re sponses are not strongly correlated over the population of envelope-re sponsive cells. 5. Our data support a ''two-stream'' receptive-field m odel for envelope-responsive cells. One stream is a conventional, spat ially 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 nonline ar neural subunits whose outputs are spatially pooled at the second st age. 6. In conclusion, this study indicates that envelope responses in area 17 and 18 neurons cannot he due to a nonlinearity that is common to all visual stimuli before narrowband spatial-frequency-selective f iltering; instead, a specialized processing stream, parallel to the co nventional luminance response stream, is needed to supplement the trad itional luminance processing stream in these cells. This specialized s tream responds to the envelope stimuli and is selective to their carri er and envelope spatial frequencies. The distributions of the optimal luminance and carrier spatial frequencies indicate a rich variety of p ossible integration between luminance and envelope information.