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The Journal of Neuroscience, November 15, 2002, 22(22):9945-9960

Processing of Natural Temporal Stimuli by Macaque Retinal Ganglion Cells

J. H. van Hateren¹, L. Rüttiger^{2, 3}, H. Sun⁴, and B. B. Lee^{2, 4}

¹ Department of Neurobiophysics, University of Groningen, 9747 AG Groningen, The Netherlands, ² Department of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, 37077 Göttingen, Germany, ³ Tübingen Hearing Research Center, University Clinics, 72076 Tübingen, Germany, and ⁴ State University of New York College of Optometry, New York, New York 10036

This study quantifies the performance of primate retinal ganglion cells in response to natural stimuli. Stimuli were confined to the temporal and chromatic domains and were derived from two contrasting environments, one typically northern European and the other a flower show. The performance of the cells was evaluated by investigating variability of cell responses to repeated stimulus presentations and by comparing measured to model responses. Both analyses yielded a quantity called the coherence rate (in bits per second), which is related to the information rate. Magnocellular (MC) cells yielded coherence rates of up to 100 bits/sec, rates of parvocellular (PC) cells were much lower, and short wavelength (S)-cone-driven ganglion cells yielded intermediate rates. The modeling approach showed that for MC cells, coherence rates were generated almost exclusively by the luminance content of the stimulus. Coherence rates of PC cells were also dominated by achromatic content. This is a consequence of the stimulus structure; luminance varied much more in the natural environment than chromaticity. Only approximately one-sixth of the coherence rate of the PC cells derived from chromatic content, and it was dominated by frequencies below 10 Hz. S-cone-driven ganglion cells also yielded coherence rates dominated by low frequencies. Below 2-3 Hz, PC cell signals contained more power than those of MC cells. Response variation between individual ganglion cells of a particular class was analyzed by constructing generic cells, the properties of which may be relevant for performance higher in the visual system. The approach used here helps define retinal modules useful for studies of higher visual processing of natural stimuli.

Key words: retinal ganglion cells; magnocellular; parvocellular; natural stimuli; information theory; macaque

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Copyright © 2002 Society for Neuroscience  0270-6474/02/22229945-16$05.00/0

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