Separability and Commonality of Auditory and Visual Bistable Perception

Hirohito M. Kondo 2 3 Norimichi Kitagawa 2 3 Miho S. Kitamura 1 2 3 Ai Koizumi 0 2 3 Michio Nomura 2 3 4 7 Makio Kashino 2 3 5 6 0 Department of Psychology, The University of Tokyo , Tokyo 113-0033, Japan 1 Research Center for Advanced Science and Technology, The University of Tokyo , Tokyo 153-8904, Japan 2 The Author 2011. Published by Oxford University Press. All rights reserved. For permissions , please 3 NTT Communication Science Laboratories , NTT Corporation, Atsugi, Kanagawa 243-0198, Japan 4 Current address: Department of Cognitive Psychology in Education, Graduate School of Education, Kyoto University , Kyoto 606-8501, Japan 5 Department of Information Processing, Interdisciplinary Graduate School of Science and Engineering, Tokyo Institute of Technology , Yokohama, Kanagawa 226-8503, Japan 6 ERATO Shimojo Implicit Brain Function Project, Japan Science and Technology Agency , Atsugi, Kanagawa 243-0198, Japan and 7 Division of Human Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima University , Higashi-Hiroshima, Hiroshima 739-8521, Japan It is unclear what neural processes induce individual differences in perceptual organization in different modalities. To examine this issue, the present study used different forms of bistable perception: auditory streaming, verbal transformations, visual plaids, and reversible figures. We performed factor analyses on the number of perceptual switches in the tasks. A 3-factor model provided a better fit to the data than the other possible models. These factors, namely the ''auditory,'' ''shape,'' and ''motion'' factors, were separable but correlated with each other. We compared the number of perceptual switches among genotype groups to identify the effects of neurotransmitter functions on the factors. We focused on polymorphisms of catechol-O-methyltransferase (COMT) Val158Met and serotonin 2A receptor (HTR2A) -1438G/A genes, which are involved in the modulation of dopamine and serotonin, respectively. The number of perceptual switches in auditory streaming and verbal transformations differed among COMT genotype groups, whereas that in reversible figures differed among HTR2A genotype groups. The results indicate that the auditory and shape factors reflect the functions of the dopamine and serotonin systems, respectively. Our findings suggest that the formation and selection of percepts involve neural processes in cortical and subcortical areas. Introduction We perceive the world as stable, although sensory inputs are often ambiguous due to spatial and temporal occluders. This raises an important question regarding how stable percepts are formed in the brain. Bistable perception phenomena provide us with clues enabling us to investigate that issue because constant physical stimulation leads to spontaneous switching between different stable percepts. Although in the past, the formation and selection of percepts have been investigated with binocular rivalry, reversible figures, and visual plaids in the visual domain (Kleinschmidt et al. 1998; Tong et al. 1998; CasteloBranco et al. 2002; Haynes et al. 2005; Wunderlich et al. 2005), more recently, they have been studied with auditory streaming and verbal transformations in the auditory domain (Gutschalk et al. 2005; Kondo and Kashino 2007, 2009; Schadwinkel and Gutschalk 2011). However, individual variation in perceptual switching has been overlooked in favor of averaging differences to focus on stimulus-specific commonalities. An early study found a wide range of individual differences in the rate of binocular rivalry (Pettigrew and Miller 1998), where monocular images are presented to different eyes. The authors also pointed out that the rate of binocular rivalry is slow in patients with bipolar disorder, which is strongly heritable. This suggests that genetic factors influence the formation and selection of visual percepts. A large-sample twin heritability study has demonstrated that an approximately 50% variance in binocular rivalry rate is accounted for by additive genetic factors (Miller et al. 2010). In addition, a recent twin study confirmed that genetic factors affect the switching rate of the reversible figure as well as that of binocular rivalry (Shannon et al. 2011). These findings indicate that there is a substantial genetic contribution to bistable perception, particularly in the visual domain. However, it is unclear what neural processes are involved in individual differences in bistable perception and whether auditory bistability is functionally linked with visual bistability. The present study elucidated the above issues using different forms of ambiguous stimuli. Perceptual switches in auditory streaming and verbal transformations are caused by prolonged listening to a sound sequence consisting of a triplet tone (van Noorden 1975; Bregman 1990) and word (Warren and Gregory 1958; Warren 1961). Perceptual switches in visual plaids and reversible figures are produced by observing moving gratings (Wallach 1935; Adelson and Movshon 1982; Hupe and Rubin 2003) and static figures (Long and Toppino 2004). There is still some controversy as to whether spontaneous perceptual switching is modulated by distributed processes within the sensory cortices (Pressnitzer and Hupe 2006) or a central oscillator within the subcortical areas (Pettigrew and Miller 1998). The present study employed 2 different approaches to clarify the relationship between auditory and visual bistability. First, we performed factor analyses of the number of the perceptual switches in the tasks and compared the fit indices of 1-factor and multifactor models. A factor analysis estimates the degree to which the variances of the observed variables can be explained by a small number of latent variables called factors. Thus, the analysis allows us to specify the underlying structure among observed and latent variables: The observed variables are modeled as linear combinations of the common factors and error terms. If perceptual switching in different modalities is governed by a single rhythm generator, the 1-factor model should provide a better fit to the data. Conversely, if different forms of bistable perception are implemented in several brain modules, the multifactor model should fit the data. However, a factor analysis provides a heuristic interpretation of the results and cannot identify the functional linkage between the factors and neural processes. Second, we used a genotype group comparison to examine which neurotransmitter functions are associated with the factors. Previous studies have argued that the timing of perceptual switching is modulated by the autonomic nervous system via noradrenaline (Einha user et al. 2008) and by drugs affecting the functions of the serotonin receptors (Carter et al. 2005, 2007; Nagamine et al. 2008). Thus, the dopamine and serotonin systems may be involved in the underlying neural processes of bistable perception. We focused on the functional p (...truncated)