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Right Parietal Brain Activity Precedes Perceptual Alternation During Binocular Rivalry

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Right Parietal Brain Activity Precedes Perceptual Alternation During Binocular Rivalry r Human Brain Mapping 32:1432–1442 (2011) r Right Parietal Brain Activity Precedes Perceptual Alternation During Binocular Rivalry Juliane Britz,1* Michael A. Pitts,2 and Christoph M. Michel2 1Department of Fundamental Neuroscience, University of Geneva, Geneva, Switzerland 2Department of Neurosciences, University of California, San Diego, California r r Abstract: We investigated perceptual reversals for intermittently presented stimuli during binocular ri- valry and physical alternation while the ongoing EEG was recorded from 64 channels. EEG topogra- phies immediately preceding stimulus-onset were analyzed and two topographies doubly dissociated perceptual reversals from non-reversals. The estimated intracranial generators associated with these topographies were stronger in right inferior parietal cortex and weaker bilaterally in the ventral stream before perceptual reversals. No such differences were found for physical alternation of the same stim- uli. These results replicate and extend findings from a previous study with the Necker cube and sug- gest common neural mechanisms associated with perceptual reversals during binocular rivalry and ambiguous figure perception. For both types of multi-stable stimuli, the dorsal stream is more active preceding perceptual reversals. Activity in the ventral stream, however, differed for binocular rivalry compared to ambiguous figures. The results from the two studies suggest a causal role for the right in- ferior parietal cortex in generating perceptual reversals regardless of the type of multi-stable stimulus, while activity in the ventral stream appears to depend on the particular type of stimulus. Hum Brain Mapp 32:1432–1442, 2011. VC 2010 Wiley-Liss, Inc. Key words: EEG; EEG mapping; binocular rivalry; inverse solution; LORETA; right inferior parietal r r INTRODUCTION every few seconds between the two rivaling percepts. Because these perceptual alternations happen spontane- Binocular rivalry arises when two dissimilar images are ously and randomly and without any changes in the phys- presented simultaneously to the two eyes. The resulting ical input, binocular rivalry and other forms of multi- percept is not a stable composite of the two competing stable perception such as bi-stable ambiguous figures are images, but perceptual awareness alternates stochastically powerful tools for dissociating perceptual awareness from sensory processing [Sterzer et al., 2009]. Both the mechanisms and timing of perceptual domi- Contract grant sponsor: National Institutes of Health; Contract nance/suppression remain a matter of debate. The effects grant numbers: 5 T32 MH20002, 2 R01 EY016984-35; Contract grant of binocular rivalry occur in many areas along the visual sponsor: The Swiss National Science Foundation; Contract grant number: 32003B-118315; Contract grant sponsors: The Center for stream. For example, functional imaging studies in Biomedical Imaging (CIBM) of the Geneva and Lausanne humans suggest that rivalry is already resolved at the ear- Universities, EPFL, The Leenaards and Louis-Jeantet foundations. liest stages of visual processing, namely the LGN and V1 *Correspondence to: Juliane Britz, Ph.D., Department of Funda- [Haynes et al., 2005; Lee et al., 2005; Polonsky et al., 2000; mental Neuroscience, Centre Me´dical Universitaire, 1 Rue Michel Wunderlich et al., 2005] and extrastriate areas [Haynes Servet, CH-1211 Gene`ve, Switzerland. and Rees, 2005; Meng et al., 2005; Tong et al., 1998]. On E-mail: [email protected] the other hand, electrophysiological studies in non-human Received for publication 18 May 2010; Accepted 5 June 2010 primates have failed to show the resolution of binocular DOI: 10.1002/hbm.21117 rivalry at these early stages; they found that local field Published online 5 August 2010 in Wiley Online Library potentials (LFPs) in extrastriate visual areas and in inferior (wileyonlinelibrary.com). temporal cortex reflect the currently active percept VC 2010 Wiley-Liss, Inc. r State Dependent Alternations in Binocular Rivalry r [Leopold and Logothetis, 1996; Logothetis et al., 1996; Log- topography of the scalp potential field remains stable for othetis and Schall, 1989; Sheinberg and Logothetis, 1997]. short periods of time (100 ms), presumably reflecting the In addition to visual areas, activity in frontal and parietal momentary mind state [Lehmann et al., 1993, 2010]. We areas is also modulated as a function of subjective visual have recently shown that these different topographies (so- awareness [Lumer et al., 1998; Lumer and Rees, 1999]. called microstates) correlate with some of the well-known Thus, many of the brain areas involved in binocular resting states, indicating that different networks might be rivalry have been identified, but much less is known about momentarily active when the stimulus is presented [Britz the exact timing underlying the suppression of a percept et al., 2010]. Since this activation pattern changes about ev- and the emergence of its rivaling counterpart. ery 100 ms, we assume that the momentary state just Recent ERP studies have begun to investigate the timing within the 100 ms around the stimulus is most crucial for of perceptual alternations during ambiguous figure per- determining the fate of the stimulus. Previous studies sup- ception [Britz et al., 2009; Kornmeier and Bach, 2004, 2005, port this hypothesis [Britz et al., 2009; Kondakor et al., 2006; Pitts et al., 2009]. These studies identified ERP com- 1995, 1997; Lehmann et al., 1998; Mohr et al., 2005]. ponents associated with perceptual reversals of a Necker We contrasted internally generated perceptual reversals cube (or Necker lattice) during intermittent presentation, during binocular rivalry with physical alternations of the which allows precise time-locking of the EEG with stimu- same stimuli when presented monocularly and according lus onsets. These reversal-related components occurred to our hypothesis, only the internally generated, but not during two time periods after stimulus onset: an occipital the physically driven perceptual alternations should mani- negativity at 250 ms (‘‘Reversal Negativity’’) and a parie- fest in different EEG topographies immediately before tal positivity at 340 ms (‘‘Late Positive Component’’). stimulus onset. Under both conditions, we assessed the Both of these components were also elicited by physical momentary topography of the pre-stimulus state and their reversals of an unambiguous lattice [Kornmeier and Bach, concomitant source differences by means of distributed 2004]. Although these ERP studies indicate rather late source localization procedures. Differences in topography effects that are similar for physical and endogenous alter- necessarily imply different generators [Helmholtz, 1853; nations, we recently demonstrated differences in electro- Vaughan, 1982], whereas the opposite is not necessarily cortical activity between reversal and non-reversal true: identical topographies can be generated by different perception immediately before stimulus onset [Britz et al., sources. Like all EEG and MEG source localization meth- 2009]. This dissociation of perceptual reversals from non- ods, the distributed inverse solutions are non-unique and reversals was evident in the global momentary brain state depend on the implemented constraints and regularization reflected by the EEG topography at the time of stimulus parameters of the source model. However, numerous stud- arrival. The sources of the concomitant generators of these ies provide compelling evidence that distributed linear EEG topographies differed in the right inferior parietal inverse solutions provide reasonable source estimates lobe, suggesting a role for the parietal cortex in initiating [Groening et al., 2009; James et al., 2009; Laganaro et al., in perceptual alternations. Although binocular rivalry and press; Michel et al., 2004; Murray et al., 2006; Schulz et al., ambiguous figure perception arise from different proc- 2008; Vulliemoz et al., 2009; Zumsteg et al., 2006]. esses—namely the suppression/dominance of two monoc- On the basis of previous findings for the Necker cube ular stimuli and the mutually exclusive interpretations of [Britz et al., 2009], we further hypothesized that spontane- the same ambiguous stimulus—they share a common phe- ous perceptual reversals for binocular rivalry would mani- nomenology, namely spontaneous alternations of percep- fest in increased activity in right inferior parietal cortex. tion despite constant sensory stimulation. It is thus Because this reversal-related activity is assumed to be possible that these internally generated alternations arise internally generated, we also predicted no such effects for from a common process that may be reflected by common the physical alternation of the same stimuli. pre-stimulus brain states that cause perceptual change. In the present study, we used Electrical Neuroimaging [Michel et al., 2009; Murray et al., 2008] to investigate METHODS spontaneous perceptual alternations in binocular rivalry Subjects using an intermittent stimulus presentation [Kornmeier and Bach, 2004]. We hypothesized that perceptual alterna- Fourteen healthy adults (8 female, mean age 20 years, tions in binocular rivalry are generated internally and range 18–23) participated in the two experiments (binocu- spontaneously and that the momentary state of the brain lar rivalry and physical alternation) on separate days; the should determine the fate of the incoming rivaling stimu- order of experiments was counterbalanced across subjects.
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