Binocular Visual Responses in the Primate Lateral Geniculate Nucleus

Abstract

The dorsal lateral geniculate nucleus (dLGN) in carnivores and primates is a laminated structure, where each layer gets visual input from only one eye [1, 2]. By contrast, in rodents such as mice and rats, the dLGN is not overtly laminated, the retinal terminals from the two eyes are only partially segregated [3, 4], and many cells in the binocular segment of dLGN get excitatory inputs from both eyes [5, 6]. Here, we show that the evolutionary ancient koniocellular (K) division of primate dLGN, like rodent dLGN, forms a subcortical site of binocular integration. We recorded single-cell activity in dLGN of anesthetized marmoset monkeys. As expected, cells in the parvocellular (P) and magnocellular (M) layers received monocular excitatory inputs. By contrast, many cells in the K layers received excitatory inputs from both eyes. The specialized properties of distinct K sub-populations (for example, blue-yellow color selectivity) were preserved across the two eye inputs, and where tested, the contrast sensitivity of each eye input was roughly matched. The results argue that evolutionarily widely separated orders such as rodents and primates have a shared strategy of integrating signals from the two eyes in subcortical circuits.

Mouse dLGN receives input from a diverse population of retinal ganglion cells with limited convergence

“…Instead, the high number of components points towards a larger diversity of visual features encoded by dLGN neurons than commonly appreciated, at least in mice. This interpretation is supported by recent studies reporting "non-classical" responses in rodent dLGN [25][26][27][58][59][60] , rabbit dLGN 61 and the koniocellular layers of primate dLGN [62][63][64] , such as direction and orientation selectivity, and binocularity. While our factorization approach reveals an elaborate visual representation at the level of the dLGN, it is still an open question how many distinct types of dLGN neurons exist.…”

Critical-Period Visual Deprivation Disrupts Binocular Integration but Spares Spatial Acuity in the Geniculocortical Pathway

“…Considering our results, future studies investigating ocular dominance plasticity and binocular matching will need to disambiguate the relative contributions of thalamic vs. cortical mechanisms for binocular integration. Finally, it will be important to determine whether binocular integration in the primate dLGN (Zeater et al, 2015) is also vulnerable to manipulations during the critical period of development, in order to assess the significance of these findings in the context of amblyopia.…”

“…A growing body of recent evidence indicates that significant binocular processing occurs in dLGN in mice (Howarth et al, 2014;Jaepel et al, 2017;Sommeijer et al, 2017) and marmosets (Zeater et al, 2015). A retrograde tracing study (Rompani et al, 2017) demonstrated that single dLGN neurons receive direct retinal inputs from both eyes, providing an anatomical substrate for binocular integration in the mouse dLGN.…”

Disparity processing in primary visual cortex

“…2 (ii) There are additional local maxima at other disparities (false matches). (iii) The response map is much smoother than the pixelation of the original image (reducing the number of false matches), which simply reflects the fact that the monocular RFs pool over a finite spatial extent.…”