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The Journal of Neuroscience, June 1, 2003, 23(11):4746-4759

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The Receptive-Field Organization of Simple Cells in Primary Visual Cortex of Ferrets under Natural Scene Stimulation

Darragh Smyth,¹ Ben Willmore,² Gary E. Baker,¹ Ian D. Thompson,¹ and David J. Tolhurst²

¹ Laboratory of Physiology, Oxford University, Oxford OX1 3PT, United Kingdom, and ² Department of Physiology, Cambridge University, Cambridge CB2 3EG, United Kingdom

The responses of simple cells in primary visual cortex to sinusoidal gratings can primarily be predicted from their spatial receptive fields, as mapped using spots or bars. Although this quasilinearity is well documented, it is not clear whether it holds for complex natural stimuli. We recorded from simple cells in the primary visual cortex of anesthetized ferrets while stimulating with flashed digitized photographs of natural scenes. We applied standard reverse-correlation methods to quantify the average natural stimulus that invokes a neuronal response. Although these maps cannot be the receptive fields, we find that they still predict the preferred orientation of grating for each cell very well (r = 0.91); they do not predict the spatial-frequency tuning. Using a novel application of the linear reconstruction method called regularized pseudoinverse, we were able to recover high-resolution receptive-field maps from the responses to a relatively small number of natural scenes. These receptive-field maps not only predict the optimum orientation of each cell (r = 0.96) but also the spatial-frequency optimum (r = 0.89); the maps also predict the tuning bandwidths of many cells. Therefore, our first conclusion is that the tuning preferences of the cells are primarily linear and constant across stimulus type. However, when we used these maps to predict the actual responses of the cells to natural scenes, we did find evidence of expansive output nonlinearity and nonlinear influences from outside the classical receptive fields, orientation tuning, and spatial-frequency tuning.

Key words: receptive fields; visual cortex; simple cells; V1; area 17; natural scenes; natural images; reverse correlation; linearity; linear summation

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Received Oct. 4, 2002; revised Mar. 4, 2003; accepted Mar. 13, 2003.

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