Multistability in Perception Dynamics
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In: Jaeger D., Jung R. (Ed.) Encyclopedia of Computational Neuroscience: SpringerReference (www.springerreference.com). Springer-Verlag Berlin Heidelberg, 2014. M 1780 Multistability in Perception Dynamics Thomson AM (2000) Molecular frequency filters at cen- interpretations, a phenomenon known as percep- tral synapses. Prog Neurobiol 62:159–196 tual multistability. Treves A, Rolls ET (1994) A computational analysis of the role of the hippocampus in memory. Hippocampus In perceptual multistability, while the subject 4:373–391 is aware of one percept, the others appear Tsodyks M, Markram H (1997) The neural code between suppressed from consciousness. Moreover, the neocortical pyramidal neurons depends on the trans- subject experiences constant switches from mitter release probability. Proc Natl Acad Sci U S A 94:719–723 being aware to being unaware of a given percept. Tsodyks M, Uziel A, Markram H (2000) Synchrony gen- This phenomenon is thought to provide eration in recurrent networks with frequency- a powerful method to search for neural correlates dependent synapses. J Neurosci 20(1–5):RC50 of conscious awareness, since it allows to disen- tangle the neural response related to the physical properties of the stimulus, which is continuously present, from that related to the conscious percept Multistability in Perception (Rees et al. 2002; Sterzer et al. 2009). Dynamics Perceptual multistability, and especially per- ceptual bistability (two interpretations), has been Gemma Huguet1 and John Rinzel2 extensively studied in the visual modality (see 1Departament de Matemàtica Aplicada I, Leopold and Logothetis 1999; Blake and Universitat Polite`cnica de Catalunya, Barcelona, Logothetis 2002; Tong et al. 2006 for reviews). Spain The paradigmatic example of perceptual 2Center for Neural Science & Courant Institute of multistability in the visual system is the Mathematical Sciences, New York University, so-called binocular rivalry, for which there exists New York, NY, USA a vast literature (see, for instance, Blake 1989; Tong and Engel 2001). In binocular rivalry two drastically different images (face and house, for Synonyms instance; see Fig. 1a) are presented to the two eyes simultaneously, and perception alternates Ambiguous stimuli; Binocular/monocular between these two images. Other examples of rivalry; Multistable perception; Perceptual alter- perceptual bistability in the visual system include nations; Perceptual bistability/tristability; Per- the Necker cube (alternation of two depth orga- ceptual rivalry; Perceptual switching; Visual nizations; Fig. 1b), Rubin’s vase-face (alternation rivalry of two figure-ground organizations; Fig. 1c), bistable apparent motion (alternation of two arrangements of moving objects, Wallach 1935; Definition Hupe´ and Rubin 2003; Rubin and Hupe´ 2004; see http://cerco.ups-tlse.fr/~hupe/plaid_demo/demo_ Multistability in Perception Dynamics is the plaids.html for a demonstration), etc. phenomenon of spontaneous switching in the Typically associated to the visual system, subject’s perception between different interpreta- multistable perception has been reported in tions of an ambiguous sensory stimulus. other sensory systems: auditory (Deutsch 1974; Pressnitzer and Hupe´ 2006; Bregman 1990), olfactory (Zhou and Chen 2009), and tactile Detailed Description (Carter et al. 2008). Recent studies suggest some common characteristics of perceptual When subjects are confronted with an ambiguous multistability (Leopold and Logothetis 1999) sensory stimulus for an extended time, instead of across sensory modalities (Pressnitzer and Hupe´ experiencing a fixed percept, they report sponta- 2006; see also Schwartz et al. 2012; Denham neous switching between the different et al. 2012), namely: Multistability in Perception Dynamics 1781 M ab c Multistability in Perception Dynamics, between a house and a face. (b) Necker cube; it can be Fig. 1 Examples of visually ambiguous patterns (a) perceived as a cube with the lower-left face or the upper- Face-house rival image created by Frank Tong and used right face in front. (c) Rubin’s face-vase; it can be per- in his fMRI study of binocular rivalry (reproduced from ceived as a white vase or the silhouette of two black faces. Tong et al. 1998 with permission from Elsevier); when Figures (b) and (c) from wikimedia commons viewed with green-red 3D glasses, perception alternates • Exclusivity. Conflicting visual representations (I) Increasing the stimulus strength in one eye are not simultaneously present. will increase the predominance of the • Inevitability. Given sufficient time, switching stimulus. will ultimately occur. Some factors such as (II) Increasing the stimulus strength in one eye attention (van Ee et al. 2005; Meng and Tong will affect the mean dominance duration of 2004) and strong intrinsic or extrinsic biases the eye with highest contrast (Brascamp towards one of the percepts (Lack 1978; et al. 2006; Boxtel et al. 2007; Klink Moreno-Bote et al. 2010) can slow switching et al. 2008; Moreno-Bote et al. 2010). M down but do not eliminate it. (III) Increasing the stimulus strength in one eye • Randomness. Durations of perceptual bouts fol- will increase the alternation rate. low log-normal (or gamma) distributions (Levelt (IV) Increasing the stimulus strength in both 1968;Lehky1995; Logothetis et al. 1996; eyes will increase the alternation rate. Brascamp et al. 2005). Correlations between Although these propositions were originally durations of successive perceptual bouts are described for the domain of binocular rivalry, absent or insignificant (Lehky 1995; Logothetis dynamic properties for some stimulus manipula- et al. 1996; Pastukhov and Braun 2011). tions in other bistable paradigms also satisfy them Since alternations occur not only when the (Rubin and Hupe´ 2004; van Ee 2005; Klink inputs to the competing percepts are equal but et al. 2008; Moreno-Bote et al. 2010). also when they are largely unbalanced, one can study how changes in the stimulus’ parameters affect perceptual dominance durations. For the Neural Correlates of Perception domain of binocular rivalry, Levelt introduced a set of four “propositions” that summarize the Experimental results in the visual system for sub- effects of stimulus contrast of the monocular jects experiencing rivalry – imaging in humans images on the switching dynamics (Levelt and electrophysiology in awake, behaving 1968). These properties, which are based on monkeys – have revealed traces of neural activity experimental observations, have been object of that correlates with subject’s perception at ana- study in several works on perceptual bistability. tomically lower areas of visual processing (Tong Based on the existing literature, there is a general and Engel 2001; Polonsky et al. 2000; Parkkonen agreement on the reformulation of the second et al. 2008), higher areas of visual processing proposition. Thus, Levelt’s updated set of binoc- (Leopold and Logothetis 1996; Tong ular rivalry propositions state that: et al. 1998; Leopold and Logothetis 1999; M 1782 Multistability in Perception Dynamics Sheinberg and Logothetis 1997), as well as Tempo (Tones/Sec) 20 10 5 3 nonvisual parietal and frontal areas (Sterzer and 20 Kleinschmidt 2007). Moreover, monkey electro- physiology (Leopold and Logothetis 1996) revealed that the proportion of neurons firing in 15 time with perception increases along the visual Always pathway. Thus, while evidence of alternations is Segregated seen in different brain areas, the origin, which 10 may involve interacting multiple areas, is still unknown. 5 Temporal Coherence Boundary Ambiguous Region Always Frequency Separation (Semitones) Coherent Fission Boundary Perceptual Multistability in Different 0 Sensory Modalities: Auditory Streaming 0 50 100 150 200 250 300 350 400 Tone Repetition Time (msec) Perceptual multistability has been extensively Multistability in Perception Dynamics, Fig. 2 Van studied in the visual system. However, Noorden diagram for the auditory streaming paradigm multistable perception has been reported in (Reproduced from McAdams and Bregman 1979 and other sensory systems, in particular in the audi- adapted from Van Noorden (1975) with permission from the author) tory system (see Schwartz et al. 2012 for a short review). Examples of multistability in the audi- tory system are found in binaural rivalry (Deutsch http://auditoryneuroscience.com/topics/streaming- 1974), in the verbal transformation effect alternating-tones for a demonstration that illus- observed during word repetition (Warren and trates auditory streaming. Gregory 1958; Warren 1961) and, especially, in As in visual multistability, perceptual correla- the auditory streaming paradigm (Pressnitzer and tions of neural activity have been observed in Hupe´ 2006; Schnupp et al. 2010). different brain areas. Recent studies indicate For the auditory streaming paradigm, the stim- that perceptual auditory object formation, or ulus consists of a high-frequency tone A and a “streaming,” may be based on neural activity low-frequency tone B that are played alternately within the auditory cortex and beyond (Cusack (AB-AB pattern) or in triplets (ABA-ABA pat- 2005; Micheyl et al. 2005), as well as in early tern). For a slow presentation rate, the melody is stages of the auditory pathway, such as the perceived as a single stream that resembles cochlear nucleus (Pressnitzer et al. 2008). a galloping (for the triplet pattern). However, if Some models have been developed for the the presentation rate is fast enough and the fre-