Losses in Peripheral Colour Sensitivity Predicted from “Hit and Miss” Post-receptoral Cone Connections

Abstract

On the basis of the early primate neurophysiological recordings, it was thought that the different cone types of the primate retina project selectively into the centre and surround of the receptive fields of cone opponent neurons, and more recently this view has been reasserted on the basis of physiological results. An alternative idea is that these projections are in fact unselective for cone type, and, therefore, cone opponency arises from chance variations in the proportions of different cone types in centre and surround. The issue is presently controversial with anatomical or physiological support for both hypotheses. Our results show that there is a selective loss of red-green colour sensitivity across the human visual field. Furthermore, this selective loss occurs under low temporal frequency conditions (0.5 Hz) which were selected to favour the mediation of both colour and luminance detection by a common P cell pathway and to exclude an M cell contribution to detection threshold. We show that "hit and miss" post-receptoral cone projections will produce a decline in cone opponency that is sufficient to account for this selective loss, thus providing psychophysical evidence consistent with this hypothesis.

L and M Cone Contributions to the Midget and Parasol Ganglion Cell Receptive Fields of Macaque Monkey Retina

“…Finally, psychophysically measured red-green color sensitivity decreases more rapidly with increasing retinal eccentricity than would be expected from the loss of achromatic sensitivity (Mullen, 1991;Mullen andKingdom, 1996, 2002). These data are consistent with a "random connection" model of spectral opponency (Lennie, 1980;Paulus and Kroger-Paulus, 1983;Shapley and Perry, 1986;Lennie et al, 1991;Mullen and Kingdom, 1996), according to which horizontal and bipolar cells indiscriminately contact the L and M cones in the photoreceptor mosaic that lie adjacent to their dendritic fields. Red-green spectral opponency results when the single cone input to the receptive field centers of central midget cells is opposed by a surround that gets mixed L and M cone input.…”

“…The anatomical (Wässle et al, 1989;Boycott and Wässle, 1991;Goodchild et al, 1996;Calkins and Sterling, 1996), physiological (Dacheux and Raviola, 1990;Dacey et al, 1996Dacey et al, , 2000a, and psychophysical (Mullen and Kingdom, 2002) data from outer retina consistent with the random connection model (Lennie, 1980;Paulus and Kroger-Paulus, 1983;Shapley and Perry, 1986;Lennie et al, 1991;Mullen and Kingdom, 1996) might be reconciled with the selective connection model (Reid and Shapley, 1992;Dacey, 1993;Lee et al, 1998;Martin et al, 2001) by invoking inner retinal selectivity. However, selective connections are inconsistent with the covariance of horizontal and ganglion cell L/(L ϩ M) ratios at single retinal locations, as is the lack of peripheral midget opponency.…”

“…It also predicts that substantial individual variability in L and M cone input strength will result from the large range of relative L and M cone numbers in normal individuals (Vimal et al, 1989;Wesner et al, 1991;Roorda et al, 2001). Finally, it predicts a decline in opponency with increasing eccentricity as increasing numbers of cone inputs to center and surround drive the relative numbers of L and M cones toward that of the cone mosaic as a whole (Mullen and Kingdom, 1996).…”

Random Wiring in the Midget Pathway of Primate Retina

“…Other electrophysiological and psychophysical studies are consistent with spectral mixing (De Monasterio and Gouras, 1975;Derrington et al, 1984;De Valois and De Valois, 1993;Mullen and Kingdom, 1996;Diller et al, 2004;Mullen et al, 2005).…”

Contrast sensitivity perimetry tests along the cardinal directions in color space: Correlation with the properties of the neural mechanisms mediating detection of spatio-temporal patterns

“…Nuestros resultados muestran que la sensibilidad al contraste decrece con la excentricidad en cada uno de los puntos del domino espacio-temporal tanto para el mecanismo acromático como para cada uno de los mecanismos cromáticos, aunque lo hace de modo distinto en cada uno de ellos, lo cual es consistente con resultados previos de la literatura [35,39,[55][56][57][58][59]. Estas pérdidas de sensibilidad al contraste pueden ir ligadas tanto a una disminución de la densidad de células con la excentricidad como a una disminución de la sensibilidad de las células individuales.…”