Edited by: Olivier A. Coubard, CNS-Fed, France
Reviewed by: Daniel Calderone, New York University Langone Medical Center, USA; Ignacio Serrano-Pedraza, Complutense University of Madrid, Spain
*Correspondence: Charles-Edouard Notredame, Service de Psychiatrie de l'enfant et de l'adolescent, Hôpital Fontan, CHRU de Lille, CS 70001, 59037 Lille, France e-mail:
This article was submitted to the journal Frontiers in Integrative Neuroscience.
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Illusion, namely a mismatch between the objective and perceived properties of an object present in the environment, is a common feature of visual perception, both in normal and pathological conditions. This makes illusion a valuable tool with which to explore normal perception and its impairments. Although still debated, the hypothesis of a modified, and typically diminished, susceptibility to illusions in schizophrenia patients is supported by a growing number of studies. The current paper aimed to review how illusions have been used to explore and reveal the core features of visual perception in schizophrenia from a psychophysical, neurophysiological and functional point of view. We propose an integration of these findings into a common hierarchical Bayesian inference framework. The Bayesian formalism considers perception as the optimal combination between sensory evidence and prior knowledge, thereby highlighting the interweaving of perceptions and beliefs. Notably, it offers a holistic and convincing explanation for the perceptual changes observed in schizophrenia that might be ideally tested using illusory paradigms, as well as potential paths to explore neural mechanisms. Implications for psychopathology (in terms of positive symptoms, subjective experience or behavior disruptions) are critically discussed.
Vision has long been considered one of the main routes humans use to understand the world (Glezer,
Historically, the first scientific descriptions of misleading visual effects date back to the late 19th to early 20th century. Physiologists, such as Poggendorff, Herman, Müller-Lyer, Ponzo and Ebbinghaus, noticed that our appreciation of contrast, size or continuity can be distorted by contextual information (Zölner,
There is a strong tradition of considering as illusory every image that misleads perception into instability, insolubility, distortion or fiction (for an example of synthetic classification, please refer to Table
Ambiguity | Information is insufficient to result in a single interpretation. | |
Distortion | The visual context induces a distortion in size, contrast, motion or disposition appreciation. | |
In the |
||
Paradox | The figure appears to be an impossible object when viewed from a critical position. | |
The |
||
Fiction | The observer perceives visual elements absent in the figure because of the context. | |
The |
In this perspective, illusions, hallucinations and hallucinosis are experiences that share the property of being inconsistent with the actuality of the sensory environment. As such, they all belong to the category of false percepts. Nevertheless, the present review is based upon crucial points of the definition in order to distinguish illusions from other misperceptions. VIs originate from an object already present in the environment and occur frequently in “normal” visual processing, whether naturally induced or intentionally provoked. The vulnerability to VIs does not have any pathological significance
These particular precisions are important to understand how the abnormal patterns of illusory perception potentially identified in patients who suffer from schizophrenia differ from, but can be linked to, the other false percepts (e.g., hallucinations). Schizophrenia is a severe and disabling disorder that affects approximately 1% of the general population (McGrath et al.,
In a recent paper, Silverstein and Kean remind us that visual sciences have been invested since the 1950's to improve insight into the brain functioning of schizophrenia patients (Silverstein and Keane,
In this paper, we review recent VI experiments conducted in schizophrenia patients, with the aim of explaining how apparently composite findings may offer a holistic comprehension of visual perception in schizophrenia. Furthermore, we critically discuss how probabilistic theories of perception (e.g., Bayesian) are of interest to understand the singular pattern of illusion sensitivity in schizophrenia. We also demonstrate how the computational hypotheses of psychosis benefit from VIs to provide insights in the genesis of the positive symptoms and in other psychopathological properties in this disorder.
The physiological existence of VIs suggests that deceiving perception paradoxically requires the integrity of the different subcomponents of the visual system. At first sight, the corollary assumption appears to make sense: one could consider resistance to VIs as the expression an identifiable, specific and common disruption that affects the structures visual processing. However, trying to synthesize the studies that adopted this structural perspective led to two main limitations.
First, the structural approach conceptualizes the impairments of visual processing as potentially resulting from dysfunctions of the brain structures computing low-level sensory information. If this hypothesis is correct, this would result in poorer experimental performances of the patients compared with controls. To date, the findings based on VI paradigms in schizophrenia do not allow clear-cut conclusions. On the one hand, many authors, following Dakin, reported that patients who suffer from schizophrenia outperform controls in VI experiments. Dakin's findings were notably replicated using the same type of context-based illusion paradigms (Uhlhaas et al.,
Barch et al., |
SCZ-T (132) | Surround suppression (contrast discrimination) | The importance of the surround effect in patients was reduced compared with CTL. |
Bressan and Kramer, |
Non-clinical population (123) | Surround suppression (size discrimination) | |
Crawford et al., |
SCZ-T (21) | Apparent motion | The estimated total strength of the illusion was less important in patients compared with controls |
Dakin et al., |
SCZ-T (15) | Surround suppression (contrast discrimination) | The contrast-contrast effect was diminished compared with both the healthy and psychiatric control groups |
Psychiatric controls (20) | |||
Emrich et al., |
Volunteers exposed to Δ9-THC (7), SCZ (12) | Binocular Depth Inversion Illusion | Patients were more resistant to the illusion compared with CTL. For intoxicated volunteers, the strength of the illusion was negatively correlated with the plasma levels of Δ9-THC |
Keane et al., |
SCZ and SCZ-T (30) | Binocular Depth Inversion Illusion | Patients were less vulnerable to the illusion compared with CTL. |
Koethe et al., |
Volunteers exposed to Δ9-THC (16), FEP (16), IPS (16) | Binocular Depth Inversion Illusion | Vulnerability to the illusion was more important in CTL compared with the other groups. |
Koethe et al., |
SCZ (75), SCZ-T (75), IPS (22), MDD (35), BD (22), Alzheimer's (6) | Binocular Depth Inversion Illusion | SCZ, SCZ-T and IPS tended to be less prone to the illusion compared with CTL. The difference between the other groups and CTL did not reach significance. There was no difference between the clinical groups. |
Leweke et al., |
Volunteers exposed to Δ9-THC (17) | Binocular Depth Inversion Illusion | BDII was strongly reduced after Δ9-THC administration |
Must et al., |
SCZ (20) | Surround suppression (Facilitation effect of collinear flankers) | Collinear flankers had a smaller facilitation effect on contrast detection in SCZ compared with CTL. |
Robol et al., |
SCZ and SCZ-T (18) | Contour detection + Surround suppression | The contour detection was poorer and less susceptible to the influence of the surround effect in patients compared with CTL. Patients were also less affected by the influence of distractors in discriminating the orientation of contour elements. |
Sanders et al., |
SCZ and SCZ-T (34) | Apparent motion | Susceptibility to the illusion was significantly weakened for patients. |
Schallmo et al., |
SCZ (28), First-degree relatives of SCZ patients (15) | Contour detection + Surround suppression | Contour detection was impaired in patients. Context caused less of a performance decrement in patients compared with CTL or relatives |
Schmeider et al., |
SCZ (13), patients with alcohol withdrawal (10), Sleep-deprived volunteers (10) | Binocular Depth Inversion Illusion | SCZ and sleep-deprived volunteers were significantly less vulnerable to the illusion compared with CTL |
Schneider et al., |
Patients with alcohol withdrawal (10), | Binocular Depth Inversion Illusion | Patients were highly more resistant to the illusion compared with controls |
Schneider et al., |
SCZ-T (10), MDD (10) | Binocular Depth Inversion Illusion | The SCZ group was significantly less vulnerable to the illusion compared with both CTL and MDD during the first week of admission. Before the patients' discharge, the difference was not significant. A trend to resist the illusion was found in the MDD group but did not reach significance. |
Semple et al., |
Chronic cannabis users (10) | Binocular Depth Inversion Illusion | Cannabis users were less prone to the illusion compared with CTL, irrespective of the time since the last dose (which suggests the effects of chronic use). |
Silverstein et al., |
FEP (16), SCZ-T (21) | Surround suppression (size) | At hospital admission, the SCZ group was less biased by the context compared with the FEP and CTL groups. At hospital discharge, vulnerability to the illusion was comparable for the three groups. |
Sternemann et al., |
Sleep-deprived volunteers (10) | Binocular Depth Inversion Illusion | The strength of the illusion was negatively affected by sleep deprivation |
Tadin et al., |
SCZ-T (16) | Surround suppression (motion discrimination) | Center-surround interactions were weaker in SCZ-T compared with CTL. This led to greater performance in motion discrimination of large high-contrasted stimuli. |
Tschacher et al., |
SCZ-T (34) | Motion-induced blindness | The scores designed to reflect the strength of the illusion were higher in CTL compared with SCZ-T. |
Uhlhaas et al., |
Schizotypy (32) | Surround suppression (size) + contour detection | No impairment in visual context processing was found to be related to schizotypy overall. A subset of thought-disordered schizotypal participants demonstrated diminished performances in contour detection compared with CTL. |
Wang et al., |
SCZ (30), BD (13) | Binocular Depth Inversion Illusion | The SCZ group was less vulnerable to the illusion compared with both the CTL and BD groups (which were not different from each other). |
Yoon et al., |
SCZ and SCZ-T (17) | Surround suppression (Contrast discrimination) | The reduction of the surround-suppression found in SCZ (compared with CTL) was selective for stimulus orientation |
Chen et al., |
SCZ-T (24) | Surround suppression (motion discrimination) | The surround-induced bias was greater in patients compared with CTL. This was primarily because of a stronger inhibition, rather than a facilitation, effect |
Chen et al., |
SCZ-T (33) | Spatial frame illusion | The illusory effect was greater for patients compared with CTL in visual, visuomotor and delayed visuomotor conditions |
Kantrowitz et al., |
SCZ-T (38) | Surround suppression (size discrimination and Hermann grid illusion) | Patients showed different patterns of sensitivity depending on the illusion: increased for the Müller-Lyer illusion, unchanged for the Poggendorff illusion and Sander parallelogram, and decreased for the Ponzo illusion. These patterns depended on the contrasts of the stimuli |
Norton et al., |
SCZ-T (28) | Three-flash illusion | The illusion peaked at a longer inter-stimulus interval in SCZ compared with CTL. At 100 ms, patients' vulnerability was decreased. In contrast, for higher intervals, patients perceived the illusion more frequently. |
Tibber et al., |
SCZ and SCZ-T (24) | Surround suppression (discrimination of contrast, size, luminance and orientation) | Compared with CTL, patients were less biased by the context in their judgment regarding contrast and size but not luminance and orientation. |
Yang et al., |
SCZ-T (30) | Surround suppression (discrimination of contrast, size, luminance, motion and orientation) | Patients exhibited more accurate (less biased) performances in contrast detection compared with CTL. However, the magnitude of the contextual modulation for luminance, size, orientation and motion was similar in both groups |
Yang et al., |
BD (16), SCZ (30) | Surround suppression (discrimination of contrast, size, luminance, motion and orientation) | There was no difference in the surround effect influence between BD, SCZ and CTL groups for any task |
Second, several authors resorted to the structural approach to localize the specific disruption hypothetically responsible for the pattern of sensitivity to VIs observed in schizophrenia. However, these attempts led to apparent contradictions. This is notably the case when trying to assess, in a hierarchical perspective (from retina to high cortical areas), whether resistance to illusion is because of a high or a low-level disruption. For example, Norton et al. (
VIs, although polymorphic, pinpoint the limits of purely anatomoclinical or linear causal models and underline, in contrast, the complexity and specificity of visual perception in schizophrenia. The data on VIs in schizophrenia patients encourage opting for a more functional and translational point of view.
VIs are an illustration of the perceptual system's ability to bind and group visual elements into coherent patterns, which leads to a meaningful representation. According to Butler et al. (
Although not always labeled as such, many VIs refer to a basic perceptual phenomenon called the
Despite the fact that the stimuli used in
In complement to
Unraveling such disruption of
The links between probabilistic theories and perception can be illustrated by examining a now famous VI example: the
Starting from the Helmholtz's “unconscious inferences” theory (von Helmholtz,
The probabilistic approaches to perception consider sensory stimuli as inherently ambiguous. In order to build a coherent representation of the world, one has to combine uncertain sensory evidence with prior knowledge. Let us imagine that the task is to infer whether or not there is a tree (as summarized by a random binary variable theta). The Bayes theorem combines:
In order to compute:
p(θ|x) |
|
|
=Probability of tree θ given the retinal input x |
p(x|θ) |
|
= Probability of retinal input x given tree θ | |
p(θ) |
|
= Probability of the parameter θ before any evidence |
More generally, the Bayesian framework considers perception as a hierarchical inference process, with more abstract (higher) levels generating expectations and sending them down the cortical hierarchy (top-down process) toward sensory representation. Meanwhile, sensory evidence climbs up the hierarchy (bottom-up process) and activates these high levels representations. In this way, top-down expectations are constantly updated to account for new sensory evidence.
Several simplified framework have been proposed to describe hierarchical inference and relate it to the brain architecture.
In
The
Importantly, despite conceptual differences, these frameworks are algorithmically similar and may essentially differ in the type of variables considered (e.g., binary vs. continuous, see Jardri and Deneve,
A re-examination, in the light of the Bayesian theory, of the stimuli that could have been traditionally considered illusory enables a conceptual refinement. Importantly, resorting to such a theoretical framework will help to re-delimit what does, and what does not fit with our definition of VIs.
In the Bayesian framework, the perceptual uncertainty that characterizes the “misleading” stimuli arises from weak or conflicting sensory evidence (Sundareswara and Schrater,
A figure can be considered ambiguous when it provides sensory information equally supporting different interpretations. This results in a phenomenon called
Assessing whether ambiguous figures (considered physical stimuli) and their subsequently generated percept are dissociated, i.e., whether ambiguous figures fit with the definition of illusions that we propose, requires dissociating two conceptual levels. We will use the Necker Cube as support for our demonstration.
On the first level, the brain's propensity to derive a 3-dimensioned interpretation from a simple pattern of lines can be viewed as a basic discrepancy between sensation and perception. However, this discrepancy is inherent to the perceptual process, and thus irrelevant to specifying the ambiguous figure as an illusion.
The second level refers to the question of whether bistability can be considered an illusory percept that arises from ambiguity. If we suppose a hypothetical perfectly ambiguous figure, the answer would be negative. Indeed, the information provided by the stimulus would be only sufficient to support the two equally probable resulting percepts. Thus, the image would equally coincide with the two interpretations. Nevertheless, if the bistable perception tended to persist despite the introduction of a cue (for example, by shadowing one corner of the Necker Cube, see Figure
Note that we do not claim here that all perceptual illusions, without exceptions, fall in these categories. Rather, we propose a framework that can be applied to most of the perceptual illusions considered in this review.
A growing field of theoretical and experimental approaches have related psychotic features, such as hallucinations and delusions, to a general disruption in the inferential process (Friston,
For example, according to the
Predictive coding applies the Bayes rule while assuming that the prior and the likelihood have a Gaussian distribution. For example, if the prior has mean
Thus, the percept corresponds to the prior belief, corrected by a prediction error that corresponds to the difference between the sensation and its top-down prediction. The “salience” (Kalman gain) of the prediction error is a function of prior and sensory reliabilities. In a hierarchical network, this operation is repeated once for each layer, as schematized below (Figure
To properly compute the probability of perceptual variables, the prior and likelihood must be multiplied only once. In the brain's hierarchy, top-down and bottom-up beliefs should be propagated only once in each direction (see figure above). This can be achieved if equally strong inhibitory loops exist to cancel excitatory feedforward/feedback loops (green and black units). If these inhibitory loops are impaired, beliefs are propagated multiple times, or, equivalently, the prior and likelihood are multiplied multiple times. The result is illustrated below (Figure
In contrast, the hypotheses that have been proposed for the emergence of hallucinations in reference to the
Note that the conflict between apparently contradictory hypotheses (gains of prediction errors larger than normal or smaller than normal, over-trusted prior or over-counted sensory evidence) has never been fully resolved, which renders the experimental testing of these theories extremely difficult. Finally, the neurophysiological processes that cause this imbalance remain unclear.
The
Psychotic manifestations can be understood as resulting from such circular inferences, which cause overconfidence, surinterpretations of weak sensory data and dissociations between high-level and low-level representations. This would be aggravated by an asymmetric impairment predominantly affecting either the upward or downward loops. Depending on which loops are mostly impaired, the model predicts that either sensory information or priors will dominate the final percept. This assumption is in line with the idea that hallucinations and delusions are two sides of a same coin (Fletcher and Frith,
The
We previously discussed that schizophrenia might be primarily associated with a lack of sensitivity to VIs (see Section Discussing the Limits of the Structural Approach). Several authors have empirically interpreted this phenomenon as a sign of a reduced top-down influence in perception. Some representative examples support this assumption. (1) In
Aside from these behavioral findings, recent brain-imaging and electrophysiology studies have complementarily supported the assumption of an overweighting of sensory evidence in schizophrenia. In two recent papers, Dima et al. explored the neural mechanisms involved in the resistance to the
Interestingly, using magnetic resonance spectroscopy, Yoon et al. revealed that patients who suffer from schizophrenia exhibited a reduced GABA concentration in the visual cortex compared with healthy controls (Yoon et al.,
Overall, the heuristic value of VIs now appears clearer. Studying how patients cope with these simple stimuli provides access to underlying perceptual processes that could also account for the emergence of hallucinations and delusions (White and Shergill,
Importantly, while VIs provide a privileged access to the visual hallucinatory modality, readers should note that adult patients who suffer from schizophrenia are more concerned by auditory compared with visual hallucinations (Mueser et al.,
Positive symptoms are not specific to schizophrenia. The possible occurrence of hallucinations and delusions in various psychiatric and neurological conditions or even in non-clinical populations suggests the relevance of a dimensional approach. Nevertheless, the heuristic value of VIs may open a path toward a new categorization based on the computational model that offers the best fit with particular perceptual disruptions. We effectively illustrated how an overweighting of sensory evidence may explain both hallucinations and the reduced susceptibility to VIs in schizophrenia. Interestingly, a trend to resist VIs has also been identified in autism (Happé,
The resistance to VIs in schizophrenia patients leads to several etiopathological implications and may drive several new experiments. For example, it appears possible to examine the correlations between this lack of susceptibility and different clinical features. Despite an abundant literature dealing with this matter, frequent methodological issues (e.g., inter-group comparability) have made the findings difficult to interpret. Three main approaches may be individualized:
Examining the potential links between VI sensitivity and symptom severity (primarily using the PANSS scale) first provided discrepancies in the findings because these scores were computed as covariates. While some authors found no or only weak relationships between VIs and psychopathology (Koethe et al.,
A second question frequently raised by the resistance to VIs in schizophrenia is whether this property could be considered a trait or a state marker of the disorder. Using the
A compelling question derived from previous findings would be whether resistance to VIs is exclusively related to schizophrenia. If so, this would represent an argument for a new nosographic individualization of this condition as a result of a perceptual property, which is easy to assess. In this sense, studies that directly compared patients who suffered from schizophrenia with patients who suffered from bipolar or major depressive disorders found that the latter two groups were normally sensitive to
Considering the
This model may account for the cognitive deficits observed in schizophrenia, such as the patients' difficulties in correctly allocating attention and filtering out irrelevant information. This phenomenon can also be explained by the lack of prior influence on saliency. The weakening of the downward beliefs blurs the distinction between relevant and noisy items, which makes them almost equally surprising.
The question of whether the highlights provided by VIs help us understand behavioral features in schizophrenia requires one to consider both the complex links between perception and action and the possible common causes for their disturbances. In this regard, paradigms that test an illusory effect via visuomotor performances are thought to engage a complex cross-modal coordination and, thus, are of particular interest in schizophrenia (Pessoa et al.,
Moreover, several lines of evidence suggest that the tendency to resist illusions observed in schizophrenia is not limited to the visual modality. Shergill et al., for example, studied the
Overall, the Bayesian framework predicts that false inferences, which are biased by overweighted or insufficiently attenuated sensory evidence, may coherently (1) account for both the visual and proprioceptive perceptual changes in schizophrenia, (2) closely link these changes with action, and by extension, behavioral disruptions, (3) explain the emergence of hallucinations and delusional beliefs, and (4) provide an heuristic value to the vulnerability to illusions, which can be considered an indirect but valuable access to the global neural processing in this disorder.
Under the Bayesian scope, VIs acquire tremendous heuristic value by providing new insights into the perceptual processes that underlie misperceptions. The literature that pertains to VIs has paved the way for new hypotheses regarding psychiatric and neurological conditions (for example, overcounting of sensory evidence in schizophrenia vs. prominence of prior knowledge in Parkinson's disease). Moreover, through the probabilistic framework, VIs are an indirect but promising approach to understand several schizophrenia features as coherently emerging from the same inferential process. The research avenue may benefit from a more rigorous methodological approach, particularly by resorting to more precise classifications and conceptual definitions.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.