Superior size–weight illusion performance in patients with schizophrenia: Evidence for deficits in forward models

When non-psychiatric individuals compare the weights of two similar objects of identical mass, but of different sizes, the smaller object is often perceived as substantially heavier. This size-weight illusion (SWI) is thought to be generated by a violation of the common expectation that the large object will be heavier, possibly via a mismatch between an efference copy of the movement and the actual sensory feedback received. As previous research suggests that patients with schizophrenia have deficits in forward model/efference copy mechanisms, we hypothesized that schizophrenic patients would show a reduced SWI. The current study compared the strength of the SWI in schizophrenic patients to matched non-psychiatric participants; weight discrimination for same-sized objects was also assessed. We found a reduced SWI for schizophrenic patients, which resulted in better (more veridical) weight discrimination performance on illusion trials compared to non-psychiatric individuals. This difference in the strength of the SWI persisted when groups were matched for weight discrimination performance. The current findings are consistent with a dysfunctional forward model mechanism in this population. Future studies to elucidate the locus of this impairment using variations on the current study are also proposed.

[1]  Melvyn A. Goodale,et al.  Dissociable neural mechanisms for determining the perceived heaviness of objects and the predicted weight of objects during lifting: An fMRI investigation of the size–weight illusion , 2009, NeuroImage.

[2]  D. Wolpert Computational approaches to motor control , 1997, Trends in Cognitive Sciences.

[3]  G. Gescheider Psychophysics: The Fundamentals , 1997 .

[4]  D. Westwood,et al.  Opposite perceptual and sensorimotor responses to a size-weight illusion. , 2006, Journal of neurophysiology.

[5]  H. Forssberg,et al.  Lighter or Heavier Than Predicted: Neural Correlates of Corrective Mechanisms during Erroneously Programmed Lifts , 2006, The Journal of Neuroscience.

[6]  N. Andreasen,et al.  The Role of the Cerebellum in Schizophrenia , 2008, Biological Psychiatry.

[7]  C. Frith,et al.  The positive and negative symptoms of schizophrenia reflect impairments in the perception and initiation of action , 1987, Psychological Medicine.

[8]  D M Wolpert,et al.  Multiple paired forward and inverse models for motor control , 1998, Neural Networks.

[9]  J. Ford,et al.  Neurophysiological evidence of corollary discharge dysfunction in schizophrenia. , 2001, The American journal of psychiatry.

[10]  D. Braff Information processing and attention dysfunctions in schizophrenia. , 1993, Schizophrenia bulletin.

[11]  J. Ford,et al.  Cortical responsiveness during inner speech in schizophrenia: an event-related potential study. , 2001, The American journal of psychiatry.

[12]  J. Flanagan,et al.  Independence of perceptual and sensorimotor predictions in the size–weight illusion , 2000, Nature Neuroscience.

[13]  S. Lederman,et al.  The role of haptic versus visual volume cues in the size-weight illusion , 1993, Perception & psychophysics.

[14]  D. Wolpert,et al.  Evidence for sensory prediction deficits in schizophrenia. , 2005, The American journal of psychiatry.

[15]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[16]  B. Gelder,et al.  Audiovisual emotion recognition in schizophrenia: Reduced integration of facial and vocal affect , 2009, Schizophrenia Research.

[17]  G. Pearlson,et al.  Schizophrenia, the heteromodal association neocortex and development: potential for a neurogenetic approach , 1996, Trends in Neurosciences.

[18]  J. Ford,et al.  Out-of-Synch and Out-of-Sorts: Dysfunction of Motor-Sensory Communication in Schizophrenia , 2008, Biological Psychiatry.

[19]  S. Lederman,et al.  The Golf-Ball Illusion: Evidence for Top-down Processing in Weight Perception , 1998, Perception.

[20]  H E Ross,et al.  Weight Illusions and Weight Discrimination—a Revised Hypothesis , 1970, The Quarterly journal of experimental psychology.

[21]  K. Nuechterlein,et al.  Information processing and attentional functioning in the developmental course of schizophrenic disorders. , 1984, Schizophrenia bulletin.

[22]  B. Ritzler Proprioception and schizophrenia: a replication study with nonschizophrenic patient controls. , 1977, Journal of abnormal psychology.

[23]  S. Blakemore,et al.  The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences: evidence for a breakdown in self-monitoring , 2000, Psychological Medicine.

[24]  D. Wolpert,et al.  Is the cerebellum a smith predictor? , 1993, Journal of motor behavior.

[25]  P. Haggard,et al.  Altered awareness of voluntary action after damage to the parietal cortex , 2004, Nature Neuroscience.

[26]  E. Torrey,et al.  Schizophrenia and the inferior parietal lobule , 2007, Schizophrenia Research.

[27]  Robert Tibshirani,et al.  An Introduction to the Bootstrap , 1994 .

[28]  HELEN E. ROSS Sensory Information necessary for the Size–Weight Illusion , 1966, Nature.

[29]  I Feinberg,et al.  Efference copy and corollary discharge: implications for thinking and its disorders. , 1978, Schizophrenia bulletin.

[30]  D. Javitt,et al.  Panmodal processing imprecision as a basis for dysfunction of transient memory storage systems in schizophrenia. , 1999, Schizophrenia bulletin.

[31]  Daniel M. Wolpert,et al.  Forward Models for Physiological Motor Control , 1996, Neural Networks.

[32]  J. Vroomen,et al.  Audio-visual integration in schizophrenia , 2003, Schizophrenia Research.

[33]  Satoru Kawai,et al.  A reexamination of the size–weight illusion induced by visual size cues , 2007, Experimental Brain Research.

[34]  P. Maruff,et al.  Attention, motor control and motor imagery in schizophrenia: implications for the role of the parietal cortex , 2004, Schizophrenia Research.

[35]  Anthony C. Davison,et al.  Bootstrap Methods and Their Application , 1998 .

[36]  Judith M Ford,et al.  Corollary discharge dysfunction in schizophrenia: can it explain auditory hallucinations? , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[37]  J. Schuck,et al.  Proprioception in Schizophrenia , 1982, The Journal of nervous and mental disease.

[38]  John J. Foxe,et al.  Impaired multisensory processing in schizophrenia: Deficits in the visual enhancement of speech comprehension under noisy environmental conditions , 2007, Schizophrenia Research.

[39]  H. Holcomb,et al.  Parametric study of accuracy and response time in schizophrenic persons making visual or auditory discriminations , 2004, Psychiatry Research.

[40]  J. Fleiss,et al.  Biometric approach to psychopathology: abnormal and clinical psychology-statistical, epidemiological, and diagnostic approaches. , 1975, Annual review of psychology.

[41]  N. Andreasen The Scale for the Assessment of Negative Symptoms (SANS): Conceptual and Theoretical Foundations , 1989, British Journal of Psychiatry.

[42]  R. Johansson,et al.  Experience Can Change Distinct Size-Weight Priors Engaged in Lifting Objects and Judging their Weights , 2008, Current Biology.

[43]  Michael I. Jordan,et al.  Forward Models: Supervised Learning with a Distal Teacher , 1992, Cogn. Sci..

[44]  J. Vroomen,et al.  Multisensory integration of emotional faces and voices in schizophrenics , 2005, Schizophrenia Research.