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

Abstract

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. AbstractThe 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.

Spatial frequency sensitivity in macaque midbrain

“…Of course, at near-foveal eccentricities, where higher resolution vision dominates, band-pass tuning curves were observed, but the overwhelming population result was low-pass, unlike in V1. In anesthetized marmosets, band-pass SC tuning was suggested 52 , although it is not clear how this may have depended on eccentricity in that study. These authors also observed low-pass tuning in some of their neurons like in our case.…”

Oculomotor inhibition covaries with conscious detection

“…Those sensory units are most likely in the visual cortex, where neurons are tuned for orientation, adapt selectively to stimuli like ours, and correlate strongly with perception (Fang et al 2005;Kohn 2007;Ress and Heeger 2003). Orientationspecific adaptation has not been found in subcortical neurons (Solomon et al 2004), and neurons in the superior colliculus have little if any orientation selectivity (White and Munoz 2012, but see Tailby et al 2012). Orientation tuning is weak in the human lateral geniculate nucleus (Ling et al 2015) and primate retinal ganglion cells (Passaglia et al 2002;Schall et al 1986) and most apparent for orientations that are cardinal or radial to the fovea, which our stimuli were not.…”

Binocular Visual Responses in the Primate Lateral Geniculate Nucleus

“…Anatomically, retinal inputs to K layers do not show the strict eye segregation that defines the P and M layers [16]. Additionally, subcortical inputs to dLGN from the superior colliculus and the parabigeminal nucleus selectively target K layers [17,18], and many neurons in those areas show binocular excitatory convergence [19][20][21]. Corticofugal axons likely carry binocular signals, but they make synapses in all layers of the dLGN and therefore should influence P cells and M cells as well as K cells.…”