The modulation sensitivity of visual neurons can be influenced by remote stimuli which, when presented alone, cause no change in the ongoing discharge rate of the neuron. We show here that the extraclassical surrounds that underlie these effects are present in magnocellular-pathway (MC) but not in parvocellular-pathway (PC) retinal ganglion cells of the macaque. The response of MC cells to drifting gratings and flashing spots was halved by drifting or contrast-reversing gratings surrounding their receptive fields, but PC cell responses were unaffected. The suppression cannot have arisen from the classical receptive field, or been caused by scattered light, because it could be evoked by annuli that themselves caused little or no response from the cell, and is consistent with the action of a divisive suppressive mechanism. Suppression in MC cells was broadly tuned for spatial and temporal frequency and greater at high contrast. If perceptual phenomena with similar stimulus contexts, such as the "shift effect" and saccadic suppression, have a retinal component, then they reflect the activity of the MC pathway.

The specificity of cone inputs to ganglion cells has implications for the development of retinal connections and the nature of information transmitted to higher areas of the brain. We introduce a rapid and precise method for measuring signs and magnitudes of cone inputs to visual neurons. Colors of stimuli are modulated around circumferences of three color planes in clockwise and counterclockwise directions. For each neuron, the projection of the preferred vector in each plane was estimated by averaging the response phases to clockwise and counterclockwise modulation. The signs and weights of cone inputs were derived directly from the preferred vectors. The efficiency of the method enables us to measure cone inputs at different temporal frequencies and short-wavelength-sensitive (S) cone adaptation levels. The results show that S-cone inputs to the parvocellular and magnocellular ganglion cells are negligible, which implies underlying connectional specificity in the retinal circuitry.

The size III stimulus was superior to the frequency-doubling stimulus in preferentially stimulating M cells versus P cells.

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...

Interactions between receptor-isolating rod and long (L)- or middle (M)-wavelength-sensitive cone modulations at 2 Hz and 10 Hz were analyzed in terms of underlying inferred magnocellular (MC) and parvocellular (PC) postreceptoral pathways. Stimuli originated from a colorimeter with 4 primaries in both the center and surround fields. The first experiment employed a phase paradigm in which the thresholds for mixed rod and cone modulations were measured as a function of relative phase. The amplitudes of the rod and cone modulations, equated in threshold units, were varied in tandem. In the second experiment, thresholds for mixed rod and cone modulations were measured as a function of the ratio of the rod and cone modulation amplitudes for 2 fixed phase offsets. Both experiments yielded similar interpretations of rod and L- (or M-) cone interactions. At 1 and 10 troland (td), rod and L- (or M-) cone interactions varied depending on the postreceptoral pathways underlying the detection. When cone thresholds were mediated by the inferred MC pathway, rod and cone thresholds showed almost linear summation. When cone thresholds were mediated by the inferred PC pathway, rod and cone thresholds showed probability summation. Assuming that signals within the same pathway follow linear summation, and signals traveling in different pathways follow probability summation, we concluded that the rod thresholds were mediated by the inferred MC pathway for both the 2-Hz and 10-Hz conditions.