Evidence that Blue‐on Cells are Part of the Third Geniculocortical Pathway in Primates

Abstract

Colour vision in primates is mediated by cone opponent ganglion cells in the retina, whose axons project to the dorsal lateral geniculate nucleus in the visual thalamus. It has long been assumed that cone opponent ganglion cells project to the parvocellular layers of the geniculate. Here, we examine the role of a third subdivision of the geniculocortical pathway: the interlaminar or koniocellular geniculate relay cells. We made extracellular recordings in the dorsal lateral geniculate nucleus of the common marmoset Callithrix jacchus, a New World monkey in which the interlaminar cells are well segregated from the parvocellular layers. We found that one group of colour opponent cells, the blue-on cells, was largely segregated to the interlaminar zone. This segregation was common to dichromatic ('red-green colour-blind') and trichromatic marmosets. The result calls into question the traditional notion that all colour information passes through the parvocellular division of the retino-geniculo-cortical pathway in primates.

Geniculocortical relay of blue-off signals in the primate visual system

“…As described in ref. 6, blue-on cells are segregated to the koniocellular layers. Five of the seven blue-off cells were located in the koniocellular layer K3 (9,24,25).…”

“…A smaller proportion of neurons in the retina and LGN shows blue-on responses, as a result of excitatory input arising in short-wavelength-sensitive (S) cones (1)(2)(3)(4)(5). Blue-on ganglion cells in the retina show a distinct bistratified morphology (5), and blue-on signals reach the visual cortex via the koniocellular/intercalated layers of the LGN (6,7). Unlike cells in the parvocellular (PC) and ventral (magnocellular) layers, the constituent cells of koniocellular pathways show diverse functional properties and widespread cortical terminations and are considered to have arisen early in the evolutionary history of the visual system (7)(8)(9).…”

Slow intrinsic rhythm in the koniocellular visual pathway

“…Of 57 other pairs recorded from the same tetrode surfaces (so that we could not measure correlations within 1.5 ms), one P pair showed a significant correlation peak at time lags below 20 ms. Furthermore, synchronized activity was present in pairs of blue-on (color-selective) K cells (11,12) as well as between color-selective and patternselective K cells (Fig. 1E).…”

“…1 B and F). The K layers contained receptive fields with heterogeneous properties (25) including S cone-driven ("blue-on" and "blue-off") fields (11,12,26) (Fig. 1 C, E, and H).…”

“…1 A-D) (23, 25, 26). Recorded neurons were tested for spatial frequency selectivity, achromatic contrast selectivity, temporal frequency selectivity, and responsivity to specific modulation of short wavelength-sensitive (S or "blue") cone photoreceptors (11,26). The P layers contained receptive fields that were small, gave sustained responses to contrast steps, and showed low contrast sensitivity (Fig.…”