Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys

Non-technical summary  Colour gets a free ride, according to our study of visual nerve cell responses in marmoset monkeys. All male marmosets are red–green colour-blind (dichromatic), but most female marmosets have normal trichromatic colour vision. It is known that signals for high-acuity daytime vision are carried in the parvocellular (P) pathway, and the P pathway also carries signals for red–green colour vision in trichromats. Here we compared P cell responses with patterned stimuli in dichromatic and trichromatic marmosets, and found no detectable difference in resolving power for fine patterns. These results indicate that red–green colour vision does not come at a cost for spatial vision. The ‘piggyback ride’ for colour signals in the P pathway may have encouraged the evolution of full colour vision in primates, including great apes, monkeys and humans.

Abstract  The red–green axis of colour vision evolved recently in primate evolutionary history. Signals serving red–green colour vision travel together with signals serving spatial vision, in the parvocellular (PC) division of the subcortical visual pathway. However, the question of whether receptive fields of PC pathway cells are specialized to transmit red–green colour signals remains unresolved. We addressed this question in single-cell recordings from the lateral geniculate nucleus of anaesthetized marmosets. Marmosets show a high proportion of dichromatic (red–green colour-blind) individuals, allowing spatial and colour tuning properties of PC cells to be directly compared in dichromatic and trichromatic visual systems. We measured spatial frequency tuning for sine gratings that provided selective stimulation of individual photoreceptor types. We found that in trichromatic marmosets, the foveal visual field representation is dominated by red–green colour-selective PC cells. Colour selectivity of PC cells is reduced at greater eccentricities, but cone inputs to centre and surround are biased to create more selectivity than predicted by a purely ‘random wiring’ model. Thus, one-to-one connections in the fovea are sufficient, but not necessary, to create colour-selective responses. The distribution of spatial tuning properties for achromatic stimuli shows almost complete overlap between PC cells recorded in dichromatic and trichromatic marmosets. These data indicate that transmission of red–green colour signals has been enabled by centre–surround receptive fields of PC cells, and has not altered the capacity of PC cells to serve high-acuity vision at high stimulus contrast.