Processing of Natural Temporal Stimuli by Macaque Retinal Ganglion Cells

Abstract

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; macaqueThere is growing interest in the way the visual system processes natural stimuli. Theoretical studies have used the statistical properties of stimuli from natural environments to predict spatial, temporal, and chromatic properties of various stages in visual processing (Srinivasan et al., 1982;Field, 1987;Atick, 1992;van Hateren, 1993;Dong and Atick, 1995;Olshausen and Field, 1997;van Hateren and Ruderman, 1998; for review, see Simoncelli and Olshausen, 2001). Natural, or at least naturalistic, stimuli have been used to physiologically investigate system function under normal environmental conditions. Species studied have ranged from invertebrates (Laughlin, 1981;van Hateren, 1992;Passaglia et al., 1997;Kern et al., 2001;Lewen et al., 2001;van Hateren and Snippe, 2001) through nonmammalian vertebrates (Vu et al., 1997;Berry, 2000) to mammals (Dan et al., 1996;Baddeley et al., 1997;Stanley et al., 1999;Vinje and Gallant, 2000). Study of primates is of particular interest in that they are the only mammals with trichromatic vision (Jacobs, 1993), and the visual capabilities of Old World primates are close to those of human. The macaque retina is a suitable locus for such a study, because ganglion cel...

Different Circuits for ON and OFF Retinal Ganglion Cells Cause Different Contrast Sensitivities

“…The response to white noise resembles the response to natural stimuli (Meister and Berry, 1999;Reinagel and Reid, 2000;Reinagel, 2001;van Hateren et al, 2002). Thus, on the basis of the white noise response, we propose that under natural viewing conditions, an ON cell would respond well at low contrast, whereas an OFF cell would respond poorly (Fig.…”

The Spatiotemporal Frequency Tuning of LGN Receptive Field Facilitates Neural Discrimination of Natural Stimuli

“…To compare neural discrimination for visual stimuli with different statistics, we measured LGN responses using two types of spatially uniform temporal stimuli (van Hateren et al, 2002;Butts et al, 2007), one natural and one artificial. The natural stimulus was created by selecting a pixel from a 32 ϫ 32 natural scenes movie (1500 frames) in the database (van Hateren and Ruderman, 1998).…”

Virtual Retina: A biological retina model and simulator, with contrast gain control

“…There is evidence that a divisive invariance also exists at the level of the OPL [31,1], probably between horizontal cells and light receptors. We suggest that horizontal cells provide shunting feedbacks to receptor cells in a way similar to that proposed here at the level of amacrine cells.…”

“…Furthermore, the Victor model does not consider the spatial extent, and thus perceptual consequences, of the gain control. It is a direct influence to more recent models, such as the Y cell model of Enroth-Cugell and Freeman [9], or the Van Hateren model for primate Parasol cells [31].…”