Colour and pattern selectivity of receptive fields in superior colliculus of marmoset monkeys.

Key points •  In addition to supplying signals for conscious visual perception, the pathways from eye to brain serve visual functions such as reflex eye movements, which are controlled by a brain area called the superior colliculus (SC). •  It is known that short-wavelength sensitive (S or ‘blue’) cone photoreceptors serve an evolutionary ancient pathway for colour vision but whether S cones also contribute to reflex eye movements is poorly understood. •  We show that in recordings from anaesthetised marmoset monkeys, S cones do not contribute to visual responses in the SC. Thus, although S cones are a primitive part of the visual system their signals are selectively directed to thalamo-cortical pathways serving colour vision. •  The result also implies that colour-selective responses reported in SC of awake monkeys must arrive through indirect (non-retinal) inputs to the SC. Abstract  The main subcortical visual targets of retinal output neurones (ganglion cells) are the parvocellular and magnocellular layers of the dorsal lateral geniculate nucleus (LGN) in the thalamus. In addition, a small and heterogeneous collection of ganglion cell axons projects to the koniocellular layers of the LGN, to the superior colliculus (SC), and to other subcortical targets. The functional (receptive field) properties and target specificity of these non-parvocellular, non-magnocellular populations remain poorly understood. It is known that one population of koniocellular layer cells in the LGN (blue-On cells) receives dominant functional input from short-wavelength sensitive (S or ‘blue’) cones. Here we asked whether SC neurones also receive S cone inputs. We made extracellular recordings from single neurones (n= 38) in the SC of anaesthetised marmoset monkeys. Responses to drifting and flashed gratings providing defined levels of cone contrast were measured. The SC receptive fields we recorded were often binocular, showed ‘complex cell’ like responses (On–Off responses), strong bandpass spatial frequency tuning, direction selectivity, and many showed strong and rapid habituation to repeatedly presented stimuli. We found no evidence for dominant S cone input to any SC neurone recorded. These data suggest that S cone signals may reach cortical pathways for colour vision exclusively through the koniocellular division of the lateral geniculate nucleus.