B
RIEF
R
EPORTS
Touch Feel Illusion in Schizophrenic Patients
Avi Peled, Michael Ritsner, Shmuel Hirschmann, Amir B. Geva, and Ilan Modai
Background:The rubber hand illusion is a tactile sensa-tion referred to as an alien limb. The illusion has been explained by a spurious reconciliation of visual and tactile inputs reflecting functional connectivity in the brain and was used to explore alterations of functional connectivity in schizophrenia.
Methods: The rubber hand illusion was achieved when two paintbrushes simultaneously stroke the hand of the subject hidden from vision by a screen, as well as an artificial hand placed in view of the subject. The rubber hand illusion was assessed with a questionnaire affirming or denying the occurrence of the illusion.
Results:Schizophrenic subjects felt the illusion stronger and faster then did normal control subjects. Some rubber hand illusion effects correlated with positive symptoms of schizophrenia but not with negative symptoms.
Conclusions: Altered functional integration of environ-mental inputs could constitute the basis for erroneous interpretations of reality, such as delusions and halluci-nations. Biol Psychiatry 2000;48:1105–1108 © 2000 Society of Biological Psychiatry
Key Words:Functional connectivity, context, schizophre-nia, rubber hand
Introduction
S
chizophrenia has been related both to a “disconnec-tion” and an “overconnec“disconnec-tion” hypothesis. The discon-nection hypothesis for schizophrenia suggests that differ-ent neuronal systems in the brains of schizophrenic patients become disconnected from each other (Friston 1996, 1998). David (1993, 1994) hypothesizes that in-creased, not dein-creased, corticocortical connectivity causes schizophrenia. Recently Mesulam (1998) and Fuster (1995) described brain organization as a hierarchical integration of neural systems; both overconnection and disconnection could simultaneously effect different parts of the brain hierarchy, for example, “vertically” inbe-tween-levels, ascending– descending processes, as well as “horizontally” in within-levels processes.
The rubber hand illusion (RHI), described by Botvinick and Cohen (1998), an illusion in which tactile sensations are referred to an alien limb, suggests a three-way inter-action (i.e., connectivity) between vision, touch, and proprioception. In their work, each of ten normal subjects was seated with his left arm resting upon a small table. A standing screen was positioned beside the arm to hide it from view and a life-sized rubber model of a left hand was placed on the table directly in front of the subject (Figure 1). The subject was instructed to look at the artificial hand while two small paintbrushes were used to stroke the rubber hand and the subject’s hidden hand synchronously. After the occurrence of the illusion, subjects completed a two-part questionnaire providing a description of their experience, affirming or denying the occurrence of nine specific perceptual effects (Table 1).
Disconnection between visual and somatosensory pro-cessors should result in delay or extinction of the illusion altogether. Inversely, overconnectivity should induce a strong and immediate RHI. To explore the alterations of functional connectivity in the brains of schizophrenic patients, we examined 1) the RHI among schizophrenic inpatients and normal control subjects, and 2) the relation-ship between positive/negative schizophrenic symptoms and the RHI effects.
Methods and Materials
A total of 49 right-handed adult subjects participated in the study (26 schizophrenic inpatients and 23 control subjects). Subjects with past history of neurologic disorders or drug abuse were excluded. Subjects were matched for age and education (Table 2). Number of patient hospitalizations ranged from two to four (mean and SD, 3.360.78). Twelve patients received olanzapine and nine received risperidone. Five patients were treated with typical neuroleptic medication (two with haloperidol, two with perphenazine and one patient with thioredazine) at the time of the experiment.
All participants were diagnosed according to the Structured Clinical Interview for DSM-IV. Patients were rated for symp-toms using the Scale for Assessment of Positive Sympsymp-toms (SAPS) and Scale for Assessment of Negative Symptoms (SANS; Andreasen 1983, 1984). All subjects were enrolled for the study after signing a valid informed consent.
Procedures of the experiment were similar to that of Botvinick and Cohen (1998). The brushing was synchronized (Figure 1).
From the Institute for Psychiatric Studies, Sha’ar Menashe Mental Health Center, Hadera (AP, MR, SH, IM), the Department of Electrical and Computer Engineering, Ben-Gurion University of the Negev, Beer Sheva (ABG), and Bruce Rappaport Faculty of Medicine, Technion, Haifa (MR, IM), Israel. Address reprint requests to Avi Peled, M.D., Mental Health Medical Center, Sha’ar
Menashe, Mobile Post, 38814 Hefer, Israel.
Received September 8, 1999; revised March 15, 2000; revised May 22, 2000; accepted May 26, 2000.
Subjects were instructed to verbally indicate if any change in sensation occurred during the procedure. In order to exclude suggestibility, no suggestions or references to illusions were included in the instructions.
After 10 min, subjects completed a two-part questionnaire that included an open-ended description of their experiences and asked subjects to affirm or deny the occurrence of nine specific perceptual effects (Botvinick and Cohen 1998). A retrospective evaluation of the effects preceding the formation of the illusion was included for comparison of the illusion effect at 5 min after the beginning of the experiment. Evaluation was retrospective, because stopping the brushing during the experiment would disrupt the formation of the illusion. Scoring for each of the nine perceptual effects was high for affirmation of the illusion and
low for the denial of the illusion. Scoring was established as follows: 1,222; 2,22; 3,2; 4, 0; 5,1; 6,11; 7,111. In addition, an RHI index was established; this is the mean score for all perceptual effects (i.e., 1–9 questions).
Results
Time latency for the appearance of the RHI, the prominent finding, differed significantly between schizophrenic pa-tients and control subjects. Schizophrenic papa-tients had the illusion five times faster than normal control subjects (mean and SD, 1.462.9 and 7.162.2 min, respectively;
t 5 7.5, p , .001). Table 3 describes the perceptual effects of the RHI documented (based on the perceptual effect questionnaire) at a 5 min cutoff point in time. At that time point, schizophrenic patients felt the RHI much more then normal control subjects. This was most prominent in three perceptual effects: 1) feeling sensation on rubber-hand location; 2) feeling brush touch rubber-rubber-hand; and 3) rubber-hand shape and texture resembling real hand. These three perceptual effects at that point in time also exhibited significant differences between the groups.
From the recorded descriptions of the subjects it was evident that compared to control subjects the illusion had been formed not only faster, but was also experienced very intensely by schizophrenic patients. One patient even had the illusion from viewing the rubber-hand in the position
Figure 1. Setting of rubber hand experiment. The subject was seated with his left arm resting upon a small table. A standing screen was positioned beside the arm to hide it from the subject’s view, and a life-sized rubber model of a left hand and arm was placed on the table directly in front of the subject. The subject sat with eyes fixed on the artificial hand while two small paint-brushes were used to synchronously stroke the rubber hand and the subject’s hidden hand.
Table 1. Perceptual Effects Questionnaire and Scoring, Affirming (1) or Denying (2) Rubber Hand Illusion
Perceptual effects Denying (2) Affirming (1) 1. It seemed as if I were feeling the touch of the paintbrush in the
location where I saw the rubber hand touched.
222 22 2 0 1 11 111
2. It seemed as though the touch I felt was caused by the paintbrush touching the rubber hand.
222 22 2 0 1 11 111
3. I felt as if the rubber hand was my hand. 222 22 2 0 1 11 111
4. I felt as if my (real) hand were drifting toward the right (toward the rubber hand).
222 22 2 0 1 11 111
5. It seemed as if I had more then one left hand. 222 22 2 0 1 11 111
6. It seemed as if the touch I was feeling came from somewhere between my own hand and the rubber hand.
222 22 2 0 1 11 111
7. It felt as if my (real) hand was turning “rubbery.” 222 22 2 0 1 11 111
8. It appeared (visually) as if the rubber where drifting toward the left (towards my hand).
222 22 2 0 1 11 111
9. The rubber hand began to resemble my own (real) hand, in terms of shape, skin tone, freckles or some other visual feature.
222 22 2 0 1 11 111
Table 2. Demographic Data
Schizophrenic patients [mean (SD)]
Normal control subjects [mean (SD)]
n 26 (M 20/F 6) 23 (M 10/F 13) Age (years) 36 (7.2) 40 (10.7) Education (years) 10 (2.5) 11 (2.6)
M, male; F, female.
1106 BIOL PSYCHIATRY A. Peled et al
of the experimental setting, i.e., even before any tactile stimuli were applied.
Table 4 represents the correlation between the relevant perceptual events from above (i.e., of questions 1, 2, and 9) and the positive/negative symptomatic profiles of the patients. Questions 1 and 2 correlated significantly (p 5
.05) with hallucinations. Although the remaining correla-tions did not reach statistical significance, in general it is evident that there was greater correlation between RHI and positive symptoms of schizophrenia than with negative symptoms.
Discussion
According to the connectionist approach, a “disconnection syndrome” in schizophrenia warrants reduced RHI effect in patients compared to control subjects (Botvinick and Cohen 1998). A more complex view would suggest a reduced top-down hierarchical connectivity with reduction of control over “false” overconnections of lower-level neural systems. These false interpretations of stimuli could distort environmental incoming information, altering the coherent perception of reality as is often typical to psy-chotic symptoms. The possible association between posi-tive symptoms and the RHI effects of questions 1, 2, and 9 (Table 4) suggests that the underlying mechanisms responsible for positive symptoms in schizophrenia could have common features with the mechanisms causing the enhancement of the RHI. These findings are not a reflec-tion of schizophrenia per se. Other kinds of mental disorders need investigation with the RHI before any specificity could be discussed.
Medication effect on connectivity should be considered (Coull et al 1999) in future studies with the RHI; however, because patients had active symptoms at the time of the experiment, this suggests that medication does not effect the underlying mechanisms responsible for the symptoms. Additionally, medications typically slow reaction time, and the RHI is faster in patients, suggesting that medica-tions might have limited effect on this particular illusion. Explaining the RHI in terms of altered functional connec-tivity does not rule out other explanations, for example, a meta-cognitive vulnerability, such as difficulty in differ-entiating perceptual experiences that arise from self versus others (Baker and Morrison 1998).
Testable predictions from this model propose that cor-relations in the neuronal activity among relevant brain
Table 4. Intensity of Positive and Negative Symptoms and their Pearson’s Correlations with Relevant Perceptual Effects of the Rubber Hand Illusion
Symptoms
Hallucinations 1.9 (1.9) .38c .30c .28
Delusions 3.2 (1.6) .18 .18 .11 Bizarre Behavior 2.5 (1.4) .23 .23 .25 Formal thought
disorders
2.8 (1.4) .50 .50 .04
Negatived
Affective flattening 1 (1.3) .10 .10 .01 Alogia 2.5 (1.6) .03 .03 .09 Avolition–Apathy 3 (1.2) .12 .12 .02 Anhedonia
Asociality
2.6 (1.3) .06 .06 .04
Attention 2.1 (1) .02 .02 .2
aMean and SD are shown.
bScale for Assessment of Positive Symptoms. cp
,.05 (N526).
dScale for Assessment of Negative Symptoms.
Table 3. Affirmation (High Values) and Denial (Low Values) of Perceptual Effects for the Rubber Hand Illusion after 5 Minutes of Experimental Procedure
Perceptual effects
1. Sensation on rubber hand location 6.2 (1.9) 3.7 (2.8) 3.63a
2. Felt brush on rubber hand 6.2 (1.9) 3.6 (2.8) 3.81a
3. My hand is rubber hand 4.8 (2.7) 3.6 (2.7) 1.5 4. Real hand drift (toward rubber hand) 3.1 (2.3) 2.2 (2.1) 1.5 5. More then one left hand 2.3 (2.3) 1.7 (1.6) 0.95 6. Touch between two hands (rubber and real) 2.0 (1.9) 2.0 (1.8) 0.06 7. Real hand turns rubbery 2.3 (2.3) 1.8 (2.4) 0.73 8. Rubber hand drift (toward real) 2.3 (2.0) 1.7 (1.7) 1.11 9. Rubber hand shape and texture resemble real hand 5.8 (2.1) 3.5 (2.8) 3.27a
RHI index 4.0 (1.2) 2.6 (1.7) 2.9b
Mean and SD are shown. Scoring: 1,222; 2,22; 3,2; 4, 0; 5,1; 6,11; 7,111. RHI index, rubber hand illusion mean score through 1–9 items.
a
p,.01 (two-tailedttest).
b
p,.05 (two-tailedttest).
Touch Feel Illusion in Schizophrenic Patients BIOL PSYCHIATRY 1107
systems (visual, somatosensory, and their respective asso-ciative regions) sampled via magnetic resonant or electro-physiologic imaging devices would deviate significantly in schizophrenic patients compared to control subjects and have promising perspectives for defining the “connectivity abnormalities” involved in the symptom formation of mental disorders like schizophrenia.
Special acknowledgment goes to Rena Kurs, for her valuable input regarding presentation and editing. We also thank the clinical and nursing staff of Sha’ar-Menashe Mental Health Center and the research assistants Michal Tzada and Limor Shoshan for their participation in the study. For the rubber hand we thank David Schmitz at the Orthopedic Institute “Gapaim.”
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