Activity in early visual areas predicts interindividual differences in binocular rivalry dynamics

Abstract

When dissimilar images are presented to the two eyes, binocular rivalry (BR) occurs, and perception alternates spontaneously between the images. Although neural correlates of the oscillating perception during BR have been found in multiple sites along the visual pathway, the source of BR dynamics is unclear. Psychophysical and modeling studies suggest that both low- and high-level cortical processes underlie BR dynamics. Previous neuroimaging studies have demonstrated the involvement of high-level regions by showing that frontal and parietal cortices responded time locked to spontaneous perceptual alternation in BR. However, a potential contribution of early visual areas to BR dynamics has been overlooked, because these areas also responded to the physical stimulus alternation mimicking BR. In the present study, instead of focusing on activity during perceptual switches, we highlighted brain activity during suppression periods to investigate a potential link between activity in human early visual areas and BR dynamics. We used a strong interocular suppression paradigm called continuous flash suppression to suppress and fluctuate the visibility of a probe stimulus and measured retinotopic responses to the onset of the invisible probe using functional MRI. There were ∼130-fold differences in the median suppression durations across 12 subjects. The individual differences in suppression durations could be predicted by the amplitudes of the retinotopic activity in extrastriate visual areas (V3 and V4v) evoked by the invisible probe. Weaker responses were associated with longer suppression durations. These results demonstrate that retinotopic representations in early visual areas play a role in the dynamics of perceptual alternations during BR.

A population study of binocular function

“…Test-retest reliabilities 114 for average percept duration are moderate to high, with past stud-115 ies reporting r s = 0.69 (Whittle, 1963), r p = 0.7 (Miller et al, 2010) 116 and r p = 0.8 (Pettigrew & Miller, 1998, in bipolar patients and 117 controls). 118 Variability in rate of rivalry has been found to correlate with 119 patterns of saccadic eye movements (Hancock et al, 2012), with 120 level of dichoptic masking (Baker & Graf, 2009), with retinotopic 121 activity in extrastriate visual cortex triggered by the suppressed 122 image (Yamashiro et al, 2014), and with variability in the structure 123 of parietal cortex (Kanai, Bahrami, & Rees, 2010). Rate of rivalry is 124 faster in children than adults (Hudak et al, 2011;Kovacs & 125 Eisenberg, 2004) and declines with increasing age in adulthood 126 (Jalavisto, 1964;Ukai, Ando, & Kuze, 2003).…”

Frequency of alpha oscillation predicts individual differences in perceptual stability during binocular rivalry

“…Past work has identified neural factors unrelated to oscillatory activity that predicts percept duration. These include the strength of response to the suppressed stimulus (Yamashiro et al, 2014), cortical thickness of the superior parietal lobule (Kanai et al, 2010), and the number of energy minima in visual cortex (Watanabe et al, 2014). Transcranial magnetic stimulation disruption of parietal cortex has also been shown to alter of percept durations, though past studies have found both increased and decreased durations (Carmel, Walsh, Lavie, & Rees, 2010;Zaretskaya, Thielscher, Logothetis, & Bartels, 2010).…”

“…Relatively little is known about the neural bases for these individual differences (Kleinschmidt, Sterzer, & Rees, 2012). A few studies using structural and functional magnetic resonance imaging have examined brain regions underlying individual differences in perceptual stability (Kanai, Bahrami, & Rees, 2010;Watanabe, Masuda, Megumi, Kanai, & Rees, 2014;Yamashiro et al, 2014). However, despite perceptual durations being a time-domain measure, little is known about how they relate to dynamic neural processes.…”

Personality Measures Link Slower Binocular Rivalry Switch Rates to Higher Levels of Self-Discipline

“…The few studies that have explored individual differences in the dynamics of binocular rivalry identify a number of interesting associated factors (for a review see Kleinschmidt et al, 2012). For example, differences in rivalry rate have been linked to variations in density and thickness of the parietal cortex (Kanai et al, 2010), activity in early visual area (Yamashiro et al, 2014), gaze movements using static binocular rivalry gratings (Hancock et al, 2012; however, when using drifting binocular gratings the results was not replicated by Law et al (2015) and GABA concentration in visual cortex (van Loon et al, 2013). Studies have also suggested a genetic basis for this variability, supported by identical twins showing greater similarity in rivalry dynamics than non-identical twins (Miller et al, 2010).…”