Elsevier

NeuroImage

Volume 46, Issue 4, 15 July 2009, Pages 1180-1186
NeuroImage

Understanding why patients with schizophrenia do not perceive the hollow-mask illusion using dynamic causal modelling

https://doi.org/10.1016/j.neuroimage.2009.03.033Get rights and content

Abstract

Patients suffering from schizophrenia are less susceptible to various visual illusions. For example, healthy participants perceive a hollow mask as a normal face, presumably due to the strength of constraining top-down influences, while patients with schizophrenia do not (Schneider, U., Leweke, F.M., Sternemann, U., Weber, M.M., Emrich, H.M., 1996. Visual 3D illusion: a systems-theoretical approach to psychosis. Eur. Arch. Psychiatry Clin. Neurosci. 246, 256–260; Scheider, U., Borsutzky, M., Seifert, J., Leweke, F.M., Huber, T.J., Rollnik J.D., Emrich, H.M., 2002. Reduced binocular depth inversion in schizophrenic patients. Schizophrenia Research 53, 101–108.; Emrich, H.M., Leweke, F.M., Schneider, U., 1997. Towards a cannabinoid hypothesis of schizophrenia: cognitive impairments due to a dysregulation of the endogenous cannabinoid system. Pharmacol. Biochem. Behav. 56, 803–807). However the neural mechanisms underpinning this effect remain poorly understood. We used functional magnetic resonance imaging to investigate the hollow-mask illusion in schizophrenic patients and healthy controls. The primary aim of this study was to use measures of effective connectivity arising from dynamic causal modelling (DCM) to explain differences in both the perception of the hollow-mask illusion and associated differences in neural responses between patients with schizophrenia and controls, which we hypothesised would be associated with difference in the influences of top-down and bottom-up processes between the groups. Consistent with this explanation, we identified differences between the two groups in effective connectivity. In particular, there was a strengthening of bottom-up processes, and weakening of top-down ones, during the presentation of ‘hollow’ faces for the patients. In contrast, the controls exhibited a strengthening of top-down processes when perceiving the same stimuli. These findings suggest that schizophrenic patients rely on stimulus-driven processing and are less able to employ conceptually-driven top-down strategies during perception, where incoming sensory data are constrained with reference to a generative model that entails stored information from past experience.

Introduction

In order to perceive the environment as meaningful the interaction between bottom-up and top-down processing has to be intact (Wallbott and Ricci-Bitti, 1993, Cauller, 1995). Visual illusions provide a useful tool to study the mechanisms by which top-down and bottom-up processes interact in perception; they can occur when the brain interprets sensory information on the basis of contextual information and previous experience, resulting in a percept that diverges substantially from the true sensory input. In this study we used the ‘hollow-mask illusion’ (Gregory, 1973) to investigate such an interaction. The hollow-mask illusion occurs when a hollow-mask is perceived (incorrectly) as a normal face. It is understood to be a process that involves the generation of hypotheses about the three-dimensional shape of faces by interpreting the bottom-up signals received from the eyes using conceptual and perceptual knowledge (top-down processing), as well as general rules of perception, such as Gestalt laws of organisation and perspective (Yellott, 1981, Ramachandran, 1988, Hill and Bruce, 1993, Gregory, 1998).

Almost a century ago Bleuler (1911) coined the term schizophrenia to represent the ‘splitting’ of different mental domains. This idea is still influential, but in recent years has been recast in terms of pathological connectivity between brain areas. In this framework, the symptoms of schizophrenia are not considered as a single deficit but can be seen as ‘resulting form the abnormal integration of two or more processes…and are expressed when two or more regions interact’ (Friston, 1998). Similarly, Emrich (1989) proposed that the pathogenesis of schizophrenia can be described as a functional disequilibrium within the human brain, and that an impairment of the bottom-up and top-down interaction may be a plausible explanation for the disintegrative and reality-impairing properties of psychotic disorders. Frith and Done, 1988, Frith and Done, 1989 and Malenka et al. (1982) suggested that internal correcting systems may be deficient in psychotic states, and that an imbalance occurs in systems responsible for concept formation, suggesting that schizophrenics are forced to rely on stimulus-driven processing, whereby fragments of stimuli are pieced together without reference to an expected or stored model (Hemsley, 1987).The insusceptibility of patients with schizophrenia to visual illusions is consistent with such theories. For example, it has been demonstrated that patients suffering from schizophrenia do not experience the hollow-mask illusion, i.e. the hollow stimulus is correctly perceived as hollow (Schneider et al., 1996, Scheider et al., 2002, Emrich et al., 1997), consistent with weakened top-down influences in schizophrenia.

While clear hypotheses relating to the integration of top-down and bottom-up processes arise from the theoretical positions discussed above, no study to date has investigated the neural mechanisms underpinning the failure to perceive visual illusions in schizophrenia. Understanding the interaction between top-down and bottom-up processes in schizophrenic patients is important in further understanding the pathology of schizophrenia. The primary aim of this study was therefore to use measures of effective connectivity arising from dynamic causal modelling (DCM) to explain differences in both the perception of hollow faces and associated neural responses between patients with schizophrenia and controls. We hypothesised that top-down influences from the fronto-parietal network give rise to the hollow-mask illusion in controls, and that normal or strengthened bottom-up influences from visual areas in the absence of top-down input from the fronto-parietal network prevent the patients from experiencing the illusion.

Section snippets

Subjects

Thirteen patients and 16 healthy controls matched for age, gender and educational level participated in the study (see Table 1). All schizophrenic patients fulfilled DSM-IV and ICD-10 criteria for schizophrenia and were taking atypical antipsychotic medication. Schizophrenic patients with other psychiatric disorders, including drug and or alcohol abuse and neurological disorders, were excluded. The Positive and Negative Syndrome Scale (PANSS) was used to evaluate the current symptomatology of

Behavioural data

We initially established that, as expected, patients and controls differed in terms of the susceptibility to the inverted-face illusion. Post-scan questionnaires revealed that none from the controls reported seeing a face as ‘hollow’, while all patients did (Fisher's exact test, p < 0.0001). Analysis of the response data collected during the task revealed that, due to the illusion, controls occasionally erroneously classified a 3D inverted face as flat (2D) (mean = 8.3% and std = 6.8%). Notably, the

Discussion

In this study we demonstrated that schizophrenic patients and healthy controls differ in terms of the modulation of neural connectivity during the presentation of illusory stimuli. More precisely, the data of the control group were best explained by a model where the dynamic modulation of connectivity according to face-type (normal or inverted) was placed on the backwards connections from IPS to LOC. This finding is consistent with the hypothesis that top-down influences from the

Acknowledgments

This research work was funded by a Marie Curie Early Stage Training Fellowship of the European Community's Sixth Framework Programme under the contract number MEST-CT-2005-021014. We thank our colleagues for helpful discussions, the Institute of Diagnostic and Interventional Neuroradiology, Medical School Hannover, for using their facilities to perform the fMRI scans, and Karl Friston for valuable comments on the manuscript as well as guidance in statistical and fMRI analysis. Finally, we would

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