Caloric vestibular stimulation reveals discrete neural mechanisms for coherence rivalry and eye rivalry: A meta-rivalry model

Abstract

Binocular rivalry is an extraordinary visual phenomenon that has engaged investigators for centuries. Since its first report, there has been vigorous debate over how the brain achieves the perceptual alternations that occur when conflicting images are presented simultaneously, one to each eye. Opposing high-level/stimulus-representation models and low-level/eye-based models have been proposed to explain the phenomenon, recently merging into an amalgam view. Here, we provide evidence that during viewing of Díaz-Caneja stimuli, coherence rivalry -- in which aspects of each eye's presented image are perceptually regrouped into rivalling coherent images -- and eye rivalry operate via discrete neural mechanisms. We demonstrate that high-level brain activation by unilateral caloric vestibular stimulation shifts the predominance of perceived coherent images (coherence rivalry) but not half-field images (eye rivalry). This finding suggests that coherence rivalry (like conventional rivalry according to our previous studies) is mediated by interhemispheric switching at a high level, while eye rivalry is mediated by intrahemispheric mechanisms, most likely at a low level. Based on the present data, we further propose that Díaz-Caneja stimuli induce 'meta-rivalry' whereby the discrete high- and low-level competitive processes themselves rival for visual consciousness.

Balancing bistable perception during self-motion

“…The present findings on bistable perception of rotating stimuli can also be compared with previous studies, showing that vestibular stimulation, as induced by caloric vestibular stimulation, can influence binocular rivalry (Miller et al 2000;Ngo et al 2007Ngo et al , 2008. It was found for instance that left hemispheric caloric vestibular stimulation changes the predominance of subjects' perceptions in binocular rivalry using horizontal and vertical gratings and the Necker cube (Miller et al 2000).…”

Genetic contribution to individual variation in binocular rivalry rate

“…An influence of voluntary attention on binocular rivalry has been reported also, but such influence is limited (31,32) and is much less than the order of magnitude of individual variation reported here and in previous studies (3)(4)(5)(6)(7)(8). Nonetheless, the emerging genetics of attentional networks (33) may be relevant to the present finding, because mechanisms of involuntary attention are thought to be engaged during binocular rivalry (1,20,25). Few studies have examined the role of neurotransmitter systems and the effects of pharmacological agents on binocular rivalry; however, recent reports suggest involvement of serotonergic (34,35) and noradrenergic (30) systems.…”

“…Similarly, modulation of binocular rivalry can occur with brain stimulation applied at low (18) or high (19,20) levels. Proposed mechanistic models have included rivalry between specific populations of neurons (21), rivalry between stimulus representations at a high level of visual processing (22), hierarchical computational models (23,24), and rivalry between independent attentional selection mechanisms in each cerebral hemisphere (19,20,25).…”

Predictive coding explains binocular rivalry: An epistemological review

“…For interocular grouping of Díaz-Caneja stimuli (dichoptic viewing of two half-fields of concentric circles and vertical lines) perception alternates between rivalry between the half-fields and rivalry between the coherent stimuli (Ngo, Miller, Liu, & Pettigrew, 2000), and dominance times of the coherent but not the half-field percepts can be modulated with caloric vestibular stimulation (Ngo, Liu, Tilley, Pettigrew, & Miller, 2007). This suggests two pairs of attractors, at different hierarchical levels, that rival within each pair and among pairs (''meta-rivalry", Ngo et al, 2007).…”

“…This suggests two pairs of attractors, at different hierarchical levels, that rival within each pair and among pairs (''meta-rivalry", Ngo et al, 2007). This complex energy landscape could be explained by pairwise adaptation of attractors: once the attractors for half-fields have both been occupied the system begins to expect change in the environment away from half-fields.…”