Two S-cone pathways in the visual system that are evolutionarily conserved between rodents and primates

Abstract

In a comparative study, the neural circuit underlying blue-yellow color vision was investigated in rats (Rattus norvegicus) and squirrel monkeys (Saimiri sciureus) using ultrahigh resolution (9.4T) functional magnetic resonance imaging (fMRI). Molecular genetic evidence indicates that S-cone pathways are evolutionarily ancient. This predicts that all mammals with S-cones would share evolutionarily conserved neural circuits for comparing the output of two spectrally distinct photoreceptors. In this study, we explored the properties of the S-cone pathways using S-cone isolating stimuli in animals with and without blockade of ON-pathways by intravitreal injections of the agonist of metabotropic glutamate receptors, 2-amino-4-phosphonobutyric acid (AP4) to specifically interrupt input to S-cone ON-bipolar cells. Light from arrays of colored LEDs was delivered via fiber optic bundles to produce binocular stimulation. Regions analyzed in the functional images included the dorsal lateral geniculate nucleus (LGN), pregeniculate/ventral LGN, pretectal areas, superior colliculus and the visual cortex. Standard theory attributes S-cone mediated detection, discrimination and the perception of blueness to activity in the small bistratified ganglion cell/koniocellular pathway. However, when S-cone input to this pathway was blocked, both species continued to show robust cortical activation to S-cone isolating stimuli. We conclude from this that the small bistratified cell/koniocellular pathway is not responsible for excitatory aspects of S-cone vision but rather has an important inhibitory role at the level of the cortex. The results indicate that the sensation of blueness is mediated by OFF pathways that are evolutionarily conserved across rats and monkeys. Based on known circuitry, the best candidate for generating these OFF responses is horizontal cell feedback from S-cones onto neighboring M/L-cones.