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A Review of Visual Aftereffects in Schizophrenia T ⁎ Katharine N

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A Review of Visual Aftereffects in Schizophrenia T ⁎ Katharine N Neuroscience and Biobehavioral Reviews 101 (2019) 68–77 Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews journal homepage: www.elsevier.com/locate/neubiorev Review article A review of visual aftereffects in schizophrenia T ⁎ Katharine N. Thakkara,b, , Steven M. Silversteinc, Jan W. Brascampa a Department of Psychology, Michigan State University, East Lansing, MI, United States b Division of Psychiatry and Behavioral Medicine, Michigan State University, East Lansing, MI, United States c Departments of Psychiatry and Ophthalmology, Rutgers University, Piscataway, NJ, United States ARTICLE INFO ABSTRACT Keywords: Psychosis—a cardinal symptom of schizophrenia—has been associated with a failure to appropriately create or Schizophrenia use stored regularities about past states of the world to guide the interpretation of incoming information, which Vision leads to abnormal perceptions and beliefs. The visual system provides a test bed for investigating the role of prior Aftereffect experience and prediction, as accumulated knowledge of the world informs our current perception. More spe- Adaptation cifically, the strength of visual aftereffects, illusory percepts that arise after prolonged viewing ofavisualsti- Predictive coding mulus, can serve as a valuable measure of the influence of prior experience on current visual processing. Inthis Excitation/inhibition balance Plasticity paper, we review findings from a largely older body of work on visual aftereffects in schizophrenia, attemptto reconcile discrepant findings, highlight the role of antipsychotic medication, consider mechanistic interpreta- tions for behavioral effects, and propose directions for future research. 1. Background system for understanding the role of experience in how individuals perceive and interpret the world and holds a clear translational value in Understanding the computational and neural mechanisms that understanding abnormalities in psychosis. function abnormally in psychosis—a complex constellation of symp- One form of altered neural coding and perception due to prior sen- toms that reflect a separation from reality—has long been a challenge. sory input, in which continuous exposure to a stimulus leads to satura- This understanding is essential, however, to developing effective and tion in the responses of neurons coding the available stimulus features, is targeted pharmacological and psychological treatments for schizo- called adaptation. In the visual domain, there are well-established phrenia—the illness in which psychotic symptoms are most enduring, methods of quantifying the magnitude of sensory adaptation at the severe, and disabling. Implicit or explicit in many mechanistic accounts perceptual level and clear indications as to how these perceptual phe- of schizophrenia is that psychotic symptoms arise due to inappropriate nomena map onto neural sensitivity changes. Namely, the magnitude of creation or use of stored regularities to guide the interpretation of in- adaptation can be quantified by measuring the strength of what are coming information (Gray et al., 1991; Hemsley, 2005; Sterzer et al., known as visual aftereffects: illusory perceptions that follow continuous 2018). The idea here is that perception is sculpted by a combination of presentation of a real visual stimulus. Aftereffects are thought to be due current sensory input, context, and past experience, and that schizo- to extended firing, during the initial stimulus presentation, of neurons phrenia is associated with an abnormality in this integrative, mod- selective to the features of that initial stimulus, leading to inhibition/ ulatory, and inferential process, which leads to abnormal perceptions saturation of the response of those neurons and associated disinhibition and beliefs. of neurons that are selective to complementary features, as part of the The visual system provides a test bed for investigating the role of brain's effort to maintain homeostasis with regards to neuronal firing prior experience and prediction: accumulated knowledge of the world rates (Fig. 1; Bednar, 2012). The perceptual result, the aftereffect, is il- informs our current perception (Barlow, 1990; Clifford et al., 2000; Knil lusory perception of ‘the opposite’ of the initial stimulus (e.g., the com- and Richards, 1996; Rao and Ballard, 1999). Importantly, robust be- plementary color, opposite direction of motion, etc.). For example, stare havioral paradigms have been developed to precisely quantify predic- at the cross at the center of Fig. 2 for about one minute, then stare at a tions in the visual system, and parallel work in non-human primates blank wall. The image of a face you likely perceive while your eyes are provides a basis for interpretation at the level of single neurons. Ac- closed is an example of a negative afterimage and arises due to adapta- cordingly, the visual system holds a unique advantage as a model tion to luminance. Analogous aftereffects are found for other features, ⁎ Corresponding author at: 316 Physics Road, Room 110C, East Lansing, MI 48824, United States. E-mail address: [email protected] (K.N. Thakkar). https://doi.org/10.1016/j.neubiorev.2019.03.021 Received 12 November 2018; Received in revised form 13 March 2019; Accepted 24 March 2019 Available online 30 March 2019 0149-7634/ © 2019 Elsevier Ltd. All rights reserved. K.N. Thakkar, et al. Neuroscience and Biobehavioral Reviews 101 (2019) 68–77 global disease mechanisms, may also shed light on the origins of spe- cific aspects of clinical phenomenology. Despite this potential for visual aftereffects to inform current me- chanistic theories of schizophrenia, the bulk of the studies of visual aftereffects in schizophrenia were conducted prior to the 1970s. Our aim here is to revive and critically review this literature, reconcile discrepant findings, highlight the role of antipsychotic medication, consider mechanistic interpretations for behavioral effects, and propose directions for future research. 2. Experimental paradigms Fig. 1. Schematic depiction of how single neurons implement visual after- Before reviewing findings, we begin by describing the types ofvi- effects, in this case, the tilt aftereffect. The response of a neuron thatresponds sual aftereffects that have been investigated in schizophrenia, which are preferentially to leftward orientations is depicted in the solid line, and the re- depicted in Fig. 3, and the outcome measures that have been reported. sponse to a neuron that responds preferentially to rightward orientations is After that, we summarize how aftereffects are quantified experimen- depicted in the dotted line. Stimulus presentation is depicted on the x-axis. tally, as well as which factors are known to influence these aftereffects Upon presentation of a leftward orientation grating, the neuron with a preferred in healthy individuals. We will also briefly highlight what is known leftward direction begins to respond vigorously, but soon begins to adapt with repeated presentation of this stimulus (i.e. neural firing is attenuated). Upon the about the neuronal bases of these aftereffects. Common to all aftereffect offset of this leftward grating and onset of a blank screen, the neuron returnsto paradigms is an adapter stimulus that the subject views for some period a below-baseline level of firing. The neuron with a rightward orientation pre- of time, typically followed by a test stimulus on which the subject is ference remains at baseline, thus resulting in an increase in firing rate of the instructed to report. The influence of the adapter stimulus on the per- neuron with a rightward orientation preference relative to the neuron with a ception of the test stimulus is the general measure of interest. leftward orientation preference, which gives rise to the perceptual phenomenon of a rightward bias in the perception of stimulus orientation (i.e. aftereffect). 2.1. Negative afterimages (Craik, 1940; Kelly and Martinezuriegas, 1993; Adaptation is illustrated using orientation as an example here, but it transpires Virsu and Laurinen, 1977) in an analogous fashion with other stimulus properties. Upon adapting to a visual stimulus with a given color, subjects will report an illusory image that has the same spatial configuration, i.e. outlines, as the original stimulus but in which each location has a color that is complementary to that shown at the corresponding location in the original stimulus (e.g. green becomes red). Grayscale stimuli can also induce negative afterimages (cf. Fig. 2), and in that case each lo- cation in the illusory image has a brightness that is the complement of the corresponding location in the original stimulus (i.e. bright becomes dim and vice versa). 2.2. Tilt aftereffect (Gibson and Radner, 1937; Greenlee and Magnussen, 1987; Wolfe and O’Connell, 1986) Upon adapting to a grating (or other pattern) that is oriented at a Fig. 2. Negative afterimage. Stare at the crosshair for 30–60 s, then close your particular angle, subjects are presented with a similar grating that has a eyes. The inverse of this image should be visible and is an example of a visual slightly different orientation. The original adaptation period results ina aftereffect. perceptual bias so that the angle of the subsequent grating is perceived as farther removed from that of the original grating than it actually is. from basic ones such as color and orientation to more derived ones such as facial expression and gender. Importantly, primate neurophysiology 2.3. Movement aftereffect
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