Different rules for binocular combination of luminance flicker in cortical and subcortical pathways

Abstract

How does the human brain combine information across the eyes? It has been known for many years that cortical normalization mechanisms implement ‘ocularity invariance’: equalizing neural responses to spatial patterns presented either monocularly or binocularly. Here, we used a novel combination of electrophysiology, psychophysics, pupillometry, and computational modeling to ask whether this invariance also holds for flickering luminance stimuli with no spatial contrast. We find dramatic violations of ocularity invariance for these stimuli, both in the cortex and also in the subcortical pathways that govern pupil diameter. Specifically, we find substantial binocular facilitation in both pathways with the effect being strongest in the cortex. Near-linear binocular additivity (instead of ocularity invariance) was also found using a perceptual luminance matching task. Ocularity invariance is, therefore, not a ubiquitous feature of visual processing, and the brain appears to repurpose a generic normalization algorithm for different visual functions by adjusting the amount of interocular suppression.

Binocular combination in the autonomic nervous system

“…However, the current experiments involve temporal modulations, which are quite distinct from the spatial modulations used in (36). Our other recent work (5) has shown that temporal luminance modulations involve much weaker interocular suppression in the cortical response than do spatial luminance modulations (37). These different normalization processes might reflect different priorities for spatial and temporal vision.…”

“…To estimate the extent of interocular suppression for each photoreceptor pathway, we fitted each data set using a Bayesian hierarchical implementation of a simple binocular combination model (5, 33). Our primary objective was to compare posterior distributions of the weight of interocular suppression, which are shown in Figure 2e.…”

“…The VR headset modifications allowed for small adjustments to account for individual differences in interpupillary distance and focal length. The use of this set up allowed us to modulate the stimuli in three different ocular configurations, similar to the ones we used in our previous study (5): monocular, binocular and dichoptic. In the monocular configuration, the unstimulated eye still saw a non-flickering disc of mean luminance.…”

“…This is thought to be due to a process of interocular suppression that compensates for the additional excitatory drive caused by stimulating two eyes. Our recent work (5) has shown that cortical signal combination for luminance flicker is substantially more linear than for spatial patterns, whereas there is evidence of interocular suppression in the pupil pathway.…”

“…The anatomical segregation of the subcortical pathway from the rest of the brain means that this binocular combination of signals must occur independently of the cortical processes of binocular integration required for visual perception. Our recent work (5) has shown that the algorithm underlying binocular combination of light in the pupil pathway differs from that in the cortex. Here we extend this paradigm to compare binocular combination in different photoreceptor pathways that feed into the autonomic nervous system.…”