Binocular Suppression in the Macaque Lateral Geniculate Nucleus Reveals Early Competitive Interactions between the Eyes

Abstract

The lateral geniculate nucleus (LGN) of the dorsal thalamus is the primary recipient of the two eyes’ outputs. Most LGN neurons are monocular in that they are activated by visual stimulation through only one (dominant) eye. However, there are both intrinsic connections and inputs from binocular structures to the LGN that could provide these neurons with signals originating from the other (non-dominant) eye. Indeed, previous work introducing luminance differences across the eyes or using a single-contrast stimulus showed binocular modulation for single unit activity in anesthetized macaques and multiunit activity in awake macaques. Here, we sought to determine the influence of contrast viewed by both the non-dominant and dominant eyes on LGN single-unit responses in awake macaques. To do this, we adjusted each eye’s signal strength by independently varying the contrast of stimuli presented to the two eyes. Specifically, we recorded LGN single unit spiking activity in two awake macaques while they viewed drifting gratings of varying contrast. We found that LGN neurons of all types [parvocellular (P), magnocellular (M), and koniocellular (K)] were significantly suppressed when stimuli were presented at low contrast to the dominant eye and at high contrast to the non-dominant eye. Further, the inputs of the two eyes showed antagonistic interaction, whereby the magnitude of binocular suppression diminished with high contrast in the dominant eye, or low contrast in the non-dominant eye. These results suggest that the LGN represents a site of precortical binocular processing involved in resolving discrepant contrast differences between the eyes.

Short-term plasticity in the human visual thalamus

“…LGN cells are largely monocular ( Casagrande and Boyd, 1996 ), organized in layers based on cell type (magno- parvo-cellular layers with intermixed konio-cells) and eye-of-origin (ipsi- and contralateral). However, there are indications that interocular interactions are possible in LGN ( Dougherty et al, 2021 ; Zeater et al, 2015 ), either due to local interthalamic circuits ( Dougherty et al, 2019 ) or to the large contingent of corticothalamic fibers that feedback into LGN from striate and extrastriate visual areas ( Adusei et al, 2021 ; Briggs and Usrey, 2011 ; Fitzpatrick et al, 2009 ; Hendrickson et al, 1978 ; Lund et al, 1975 ). Whichever their origin, these interocular interactions could account for the oscillations of LGN BOLD responses during binocular rivalry, shown in seminal work by Wunderlich et al, 2005 and Haynes et al, 2005 .…”

Contextual Modulation of Feedforward Inputs to Primary Visual Cortex

“…While we did see wide variation in our experimental measurement of non-dominant eye effects, our results suggest that the net influence of non-dominant eye stimulation in the monkey LGN is negligible. It is worth noting that the range of contrasts predominantly used in our study is similar to the high-contrast and medium-contrast conditions of Dougherty et al (2021), in which little or no binocular modulation was observed.…”

“…Previous reports of binocular interaction in the primate LGN have been heterogeneous. Both multi-unit (Schroeder et al, 1990) and single-unit (Marrocco and McClurkin, 1979;Rodieck and Dreher, 1979;Dougherty et al, 2021) studies have described binocular interactions in the primate LGN, though as a mixture of excitatory and inhibitory effects. Potential circuitry for such effects exists, through monosynaptic or disynaptic inhibition between LGN layers, disynaptic inhibition from the thalamic reticular nucleus, and feedback from the cortex.…”

“…While it is generally agreed that cells in the LGN of the carnivore exhibit moderate binocular interaction, the question of whether signals from the two eyes interact in the LGN of the primate is less clear; roughly half of all published studies that have investigated binocular modulation of neuronal activity in the primate LGN have reported its occurrence, but the magnitude, stream specificity, and incidence are unclear (reviewed in Howard, 2012). Schroeder et al (1990) reported that almost all of their recording sites in the primate LGN showed some form of binocular modulation; other groups (Marrocco and McClurkin, 1979;Rodieck and Dreher, 1979;Dougherty et al, 2021) have also found instances of binocular modulation in the LGN, although the results are heterogeneous. Still, other groups have found no evidence of such interaction (e.g., Lehky and Maunsell, 1996).…”

A nasal visual field advantage in interocular competition

“…Experimental paradigms based on IOC have lent themselves as an excellent tool for many fields of research in vision and the cognitive sciences. On one end of the spectrum, IOC provides the means to investigate early stages of visual processing, where the information streams from the two eyes are still processed separately 5 – 7 . On the other end of the spectrum, IOC enables us to investigate the correlates of conscious perception, as it allows for changes in the observer’s conscious percept to occur, even though the visual input remains constant 8 , 9 .…”