Long-lasting afterimages caused by neural adaptation

doi:10.1016/0042-6989(77)90129-8

Vision Research

Volume 17, Issue 7, 1977, Pages 853-860

https://doi.org/10.1016/0042-6989(77)90129-8 Get rights and content

Abstract

If the retinal location of a sinusoidal grating alternates back and forth in half-period steps, the temporal average stimulation is equivalent to that produced by a homogeneous field of light. Adaptation to this stimulus causes strong patterned afterimages, however, and they last longer than 2 min in the dark. The afterimages appear as gratings but at twice the spatial frequency of the adaptation gratings even though only the fundamental frequency is seen during adaptation. The appearance of this illusory grating afterimage indicates that a nonlinear intensity scaling precedes the site of some afterimages, the origin of which is neural and not photochemical. The neural origin was confirmed by the results of various experiments in which the eye was pressure blinded during adaptation. Blinding eliminated all negative afterimages otherwise caused by weakly bleaching primary stimuli but left positive afterimages intact. Two classes of long-lasting afterimages, the “sensitivity images” and “bleaching images”, are required to explain our results.

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Psychosis—a cardinal symptom of schizophrenia—has been associated with a failure to appropriately create or use stored regularities about past states of the world to guide the interpretation of incoming information, which leads to abnormal perceptions and beliefs. The visual system provides a test bed for investigating the role of prior experience and prediction, as accumulated knowledge of the world informs our current perception. More specifically, the strength of visual aftereffects, illusory percepts that arise after prolonged viewing of a visual stimulus, can serve as a valuable measure of the influence of prior experience on current visual processing. In this paper, we review findings from a largely older body of work on visual aftereffects in schizophrenia, attempt to reconcile discrepant findings, highlight the role of antipsychotic medication, consider mechanistic interpretations for behavioral effects, and propose directions for future research.
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After viewing a stationary pattern for some time, replacing that pattern with a blank field can result in the illusory perception of the pattern's ‘photo negative’ in the retinal location previously exposed to the pattern. Such illusory percepts—referred to as negative afterimages (Fig. 1A)—result from adaptation of retinal receptors as well as neurons further along the visual processing hierarchy during exposure to the initial pattern (Anstis et al., 1978; Brindley, 1962; Craik, 1940; Sakitt, 1976; Shimojo et al., 2001; Virsu and Laurinen, 1977). The luminance adaptation task is presented in Fig. 2A, and full paradigm details regarding the are presented in the Supplemental methods.
Abnormalities in synaptic plasticity are argued to underlie the neural dysconnectivity observed in schizophrenia. One way to measure synaptic plasticity is through sensory adaptation, whereby sensory neurons exhibit reduced sensitivity after sustained stimulus exposure. Evidence for decreased adaptation in individuals with schizophrenia is currently inconclusive, possibly due to heterogeneity in clinical and medication status across samples. Here we circumvent these confounds by examining whether altered adaptation is represented sub-clinically in the general population. To test this we used three paradigms from visual perception research that provide a precise and non-invasive index of adaptation in the visual system. Two paradigms involve a class of illusory percepts termed visual aftereffects. The third relies on a visual phenomenon termed binocular rivalry, where incompatible stimuli are presented to the two eyes and observers alternate between perceiving exclusively one stimulus or a combination of the two (i.e. mixed perception). We analyzed the strength and dynamics of visual adaptation in these paradigms, in relation to schizotypy. Our results showed that increased schizotypal traits were related to reduced orientation, but not luminance, aftereffect strength (Exp. 1). Further, increased schizotypy was related to a greater proportion of mixed perception during binocular rivalry (Exp. 1 and 2). Given that visual adaption is well understood at cellular and computational levels, our data suggest that short-term plasticity in the visual system can provide important information about the disease mechanisms of schizophrenia.
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The motion-induced blindness can occur if a salient static target spontaneously fluctuates in and out of our visual awareness while surrounded by a random moving visual pattern [47]. The negative afterimage does not transfer between eyes [42], but Virsu and Laurinen [48] reported long-lasting afterimages caused by neural adaptation. All of these studies suggest that afterimages are also retinal phenomena.
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We explore attentional effects on afterimages in the framework of the FACADE model of visual perception. We first show that the FACADE model can account for the experimental findings of Suzuki and Grabowecky [Suzuki, S., & Grabowecky, M. (2003). Attention during adaptation weakens negative afterimages. Journal of Experimental Psychology: Human Perception and Performance 29, 793–807] that afterimages are weaker when the inducing stimulus is attended. We then analyze the model’s behavior with attentional influences on a two-stimulus afterimage studied by Francis and Rothmayer [Francis, G., & Rothmayer, M. (2003). Interactions of afterimages for orientation and color: Experimental data and model simulations. Perception & Psychophysics 65, 508–522]. The model predicts that attentional focus directed towards the first stimulus has little effect on afterimage strength. In contrast, the model predicts that attentional focus on the second stimulus should increase the strength of the afterimage compared to when attention is focused elsewhere. Moreover, the model predicts that the attentional effects on the second stimulus should vary with time after offset of the second inducing stimulus. All of the model predictions are validated in an experiment. The model and experimental results extend and clarify previous explanations of attentional effects and afterimages.

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Long-lasting afterimages caused by neural adaptation

Abstract

Vision Res.

Vision Res.

Vision Res.

Vision Res.

Vision Res.

Durations of the after-images of brief light flashes and the theory of the Broca and Sulzer phenomenon

J. opt. Soc. Am.

The size of rod signals

J. Physiol., Lond.

The role of after-images in dark adaptation

Science

Visual adaptation in monkey cones: recordings of late receptor potentials

Science

The discrimination of after-images

J. Physiol., Lond.

Two new properties of foveal afterimages and a photochemical hypothesis to explain them

J. Physiol., Lond.

The electroretinogram: its components and their origins

Vision Res.

Origin of visual after-images

Nature, Lond.