Perceptual rivalry across animal species

Abstract

This review in memoriam of Jack Pettigrew provides an overview of past and current research into the phenomenon of multistable perception across multiple animal species. Multistable perception is characterized by two or more perceptual interpretations spontaneously alternating, or rivaling, when animals are exposed to stimuli with inherent sensory ambiguity. There is a wide array of ambiguous stimuli across sensory modalities, ranging from the configural changes observed in simple line drawings, such as the famous Necker cube, to the alternating perception of entire visual scenes that can be instigated by interocular conflict. The latter phenomenon, called binocular rivalry, in particular caught the attention of the late Jack Pettigrew, who combined his interest in the neuronal basis of perception with a unique comparative biological approach that considered ambiguous sensation as a fundamental problem of sensory systems that has shaped the brain throughout evolution. Here, we examine the research findings on visual perceptual alternation and suppression in a wide variety of species including insects, fish, reptiles, and primates. We highlight several interesting commonalities across species and behavioral indicators of perceptual alternation. In addition, we show how the comparative approach provides new avenues for understanding how the brain suppresses opposing sensory signals and generates alternations in perceptual dominance.

Keywords: Drosophila; binocular rivalry; fish; multistable; perception; primate; suppression.

Figure 1.

a) Human observers typically report perceptual alternations when viewing the Necker’s Cube, Duck-Rabbit and Face-vase illusions (from left to right). b) When two different images are simultaneously presented to each eye, one image will tend to dominate at a time while the other is suppressed.

Figure 2.

A) Flight arena concept for tethered Drosophila flies. Closed-loop control revealed rivalry-like alternating selection of competing visual objects (reproduced from van Swinderen, 2007). B) Independent and alternating eye movements can be seen in (a-d) the sand lance and (e-h) the chameleon (reproduced from Pettigrew, Collin, & Ott, 1999).

Figure 3.

Evidence for perceptual rivalry in macaque. Upper row: When a transparent sphere speckled with randomly placed black dots is illuminated in a way that it casts a shadow on a screen, observers perceive a two-dimensional, disk-shaped pattern of randomly distributed patches. However, if one rotates the sphere, say on a vertical axis, its two-dimensional projection is readily perceived as the shadow of a rotating three-dimensional sphere thanks to a phenomenon termed the kinetic depth effect, or structure-from-motion. Interestingly, though, the direction of rotation of this shadow-sphere (i.e., whether dots on the front surface of the sphere translate to the left or to the right) is inherently ambiguous. Human observers report random alternations in perceived rotation, accordingly. Lower row: Eye movements from a macaque monkey observing this stimulus. The purple trace depicts the horizontal displacement of one of the animal’s eyes in degrees of visual angle as a function of time. The black trace below shows the first derivative (i.e., velocity) of the same data. Note that the animal’s eye is moving back-and-forth either from left-to-right (in a stereotypical pattern termed optokinetic nystagmus). This is followed by repeated shifts from right-to-left, indicating that the animal perceives similar reversals in perceived rotation as humans (figure adapted from Leopold et al., 2003).