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Sense of body and sense of action both contribute to self-recognition
E. van den Bos, M. Jeannerod / Cognition 85 (2002) 177–187
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COGNITION Cognition 85 (2002) 177–187 www.elsevier.com/locate/cognit
Sense of body and sense of action both contribute to self-recognition Esther van den Bos a, Marc Jeannerod b,* a
Leiden University, Section Cognitive Psychology, Wassenaarseweg 52, 2333 AK, Leiden, The Netherlands b Institut des Sciences Cognitives, 67 Boulevard Pinel, 69675, Bron, France Received 7 December 2001; accepted 14 May 2002
Abstract Recognizing oneself, easy as it appears to be, seems at least to require awareness of one’s body and one’s actions. To investigate the contribution of these factors to self-recognition, we presented normal subjects with an image of both their own and the experimenter’s hand. The hands could make the same, a different or no movement and could be displayed in various orientations. Subjects had to tell whether the indicated hand was theirs or not. The results showed that a congruence between visual signals and signals indicating the position of the body is one component on which selfrecognition is based. Recognition of one’s actions is another component. Subjects had most difficulty in recognizing their hand when movements were absent. When the two hands made different movements, subjects relied exclusively on the movement cue and recognition was almost perfect. Our findings are in line with pathological alterations in the sense of body and the sense of action. q 2002 Elsevier Science B.V. All rights reserved. Keywords: Sense of body; Sense of action; Self-recognition
1. Introduction How do we recognize ourselves? Although this seems a bizarre question, it needs to be considered seriously. There are circumstances in everyday life where self-recognition may not be straightforward. Consider, for example, a situation like seeing one’s face in a mirror at the far wall of a restaurant while looking for an empty table, or seeing one’s hand through a hole. Because there is discontinuity between the body part we see and the rest of the body, an active process must take place in order to refer the body part to a representation of the whole body, what Gallagher calls our body image. According to this author * Corresponding author. Tel.: 133-4-37-911-212; fax: 133-4-37-911-210. E-mail address: [email protected] (M. Jeannerod). 0010-0277/02/$ - see front matter q 2002 Elsevier Science B.V. All rights reserved. PII: S 0010-027 7(02)00100-2
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(Gallagher, 1995, 2000), the body image is a representation (sometimes conscious, sometimes not) of an owned body, one that belongs to the experiencing self. Developmental studies provide evidence that self-recognition appears early in life. At the preconceptual stage, infants at 5 months of age are able to discriminate their own leg movements displayed in a mirror from those of another infant, presumably by making use of a perceived contingency between their own behavior and its effects (Bahrick & Watson, 1985). As they grow older the infants’ behavior will increasingly testify to their development of a conscious self-representation. Infants of 15–20 months of age, for example, will typically resolve the task of wiping a red spot stuck on their face, when they see themselves in a mirror (see Bahrick, 1995 for review). In the present study, we were interested in identifying the constituents of self-recognition in normal adult subjects. We focused on several potential sources of information indicated by the available literature to contribute to self-recognition. First, the matching of visual, tactile and proprioceptive signals originating from the same body parts contributes to an intermodal sensory image of the body. Second, the matching of one’s intentions and the bodily effects of self-generated actions contributes to a sense of the self as an agent. Concerning the contribution of sensory cues, many experimental results stress a prevalent role of vision over other senses in self-recognition: we feel our hand where we see it, not the converse. Optical distortion of the visually perceived position of a limb with respect to its felt position (e.g. by displacing prisms) produces no alteration of the sense of ownership: the position sense is actually recalibrated to conform with the visual information (Harris, 1965). This prevalence of vision was confirmed in experiments using a rubber hand. Botvinick and Cohen (1998) positioned a realistic rubber arm in front of subjects, while their real arm, hidden by a screen, was placed aside: tactile stimulation was applied simultaneously to the real and the rubber arms. After some time, the subjects experienced an illusion in which they felt the touch at the locus of the rubber arm (that they could see), not of their real (hidden) arm. In other words, the tactile stimulus was felt where it was seen, at the expense of a distortion of the felt position of the real arm. In addition, subjects spontaneously reported experiencing a clear sense of ownership for the rubber arm. According to other authors who replicated this experiment, the displacement of tactile sensations and the illusion of ownership disappear if the rubber arm is not properly aligned with the subject’s body (Farne´ , Pavani, Meneghello, & Ladavas, 2000). Body ownership, however, is only part of the problem of self-recognition. The self is most of the time an acting self. Body parts are moving with respect to one another and with respect to external objects as the result of intentional actions. It is common experience that our actions are readily self-attributed as a consequence of a normally perfect correlation between their expected effects and the flow of resulting (visual and proprioceptive) stimulation. This matching process provides the agent of an action with the sense that he is causing that action (the sense of agency). Again, however, situations may arise where this attribution becomes less than obvious. In social interactions (like playing a ball game) several people might participate in the same action and interact rapidly on the same object. In this situation an active identification process is needed to disentangle one’s hand among other hands. Both the sense of ownership and the sense of agency concur to self-identification: it is as essential to recognize oneself as the owner of one’s body as it is to
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recognize oneself as the agent of one’s actions. Indeed, the role of movement is implicit in many descriptions of self-recognition (e.g. in the developmental context). This point was the subject of experiments where subjects had to identify their own hand from an alien hand appearing at the same locus (Nielsen, 1963). In the experiment of Daprati et al. (1997), subjects were instructed to perform simple finger movements on command: when the movement performed by the subjects with their (unseen) hand departed from the movements made by the alien hand, no attribution errors were found. By contrast, when the alien hand performed the same movement as the subject, the error rate amounted to 30%: subjects tended to over-attribute to themselves movements that were grossly compatible with their own movements. In other words, subjects used movement as a cue for selfrecognition when the movement they saw matched more or less closely the representation they had of their own movement. In the present paper, we used a situation which combined uncertainty about the ownership of the subject’s hand and uncertainty about the agency of the movements performed with that hand. This situation, designed by Farrer et al. (in press), involved simultaneous presentation of two hands, one of which was the subject’s hand, the other being an alien hand. This situation is more realistic than the one used in previous experiments, since it involves ‘social’ interaction between two people, in which problems of self-recognition are most likely to arise. In social interactions people will generally be able to see both their own hand and the other’s. The question in self-recognition in this situation was therefore not whether an observed action corresponded to the action one had performed, but rather which of several observed actions was the one corresponding to the action performed by the self. 2. Methods 2.1. Participants Sixteen normal subjects (six males and ten females, mean age 28.6 years) volunteered to participate in the experiment. All but two were right handed. One male subject was later excluded, because he did not comply with the instructions. 2.2. Apparatus The experiment took place in a dimly lit room. The subject and the experimenter sat at the opposite sides of a table. The subject was facing an LCD screen positioned at 20 cm above the table at an inclination of 458 from the horizontal plane. The experimenter sat in front of a computer monitor and keyboard on the left of the LCD screen (see Fig. 1). Both the subject and the experimenter placed their right hand under the screen and folded their fingers over a support to make a relaxed fist. The support for the subject’s hand was located at approximately 40 cm from the subject’s frontal plane. The support for the experimenter’s hand was located approximately 10 cm further than the subject’s support, about 11 cm to the right. A mirror attached to the backside of the screen reflected the image of the two hands to a video camera positioned at a distance of 2 m from the screen. The camera was connected
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to a computer and the image was sent to a numeric video acquisition map. A program processed the digitized video image in real time (within 20 ms) and sent a black and white image of the hands onto the LCD screen and the computer monitor. The program allowed rotating the image displayed on the screen by 2908, 908 and 1808. So, the subject could see his or her own hand at the bottom of the screen, where it would be in reality (08 Rotation), at the top of the screen (1808 Rotation), at the left of the screen (908 Rotation) or at the right of the screen (2908 Rotation), while the experimenter’s hand was always in the opposite direction. The rotations provided the possibility to study how the recognition of one’s hand was influenced by the location where it appeared visually. To prevent recognition based on morphological characteristics, both the subject’s hand and the experimenter’s hand were covered with identical gloves. The presentation of the image was limited to 2 s to minimize the time available to study remaining morphological differences.
Fig. 1. Schematic representation of the experimental apparatus.
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2.3. Procedure At the beginning of each trial, one of three possible instructions was displayed on the LCD screen: ‘index finger’, ‘thumb’ or ‘none’. ‘Index finger’ meant that the subject should extend the index finger, ‘thumb’ meant that the subject should extend the thumb and ‘none’ meant that the subject should not move at all. When the experimenter pressed a key, the instruction was replaced by the image of the two hands. After 500 ms the computer produced a beep indicating the moment at which the subject and the experimenter should start their movements. On the trials when the subject was instructed to make a movement, the experimenter would either make the same or the alternative movement. Once the movements were performed, the screen returned dark within about 1 s. Subjects were required to leave their hands in the end position during this time and to return to the starting position when the image had disappeared. Then an arrow appeared on the screen pointing to a position where one of the hands had been (either to the left or to the right for the trials with rotations of 2908 and 908; either up or down for the trials with rotations of 08 and 1808). Subjects had to say ‘yes’ if they thought that the hand indicated by the arrow was their hand and ‘no’ if they thought that the hand indicated by the arrow was not their hand. The experimenter registered the response by pressing one of two keys on the keyboard and the next instruction appeared on the screen. 2.4. Design There were five conditions of movement: (1) subject extended index finger, experimenter extended thumb; (2) subject extended thumb, experimenter extended index finger; (3) subject and experimenter extended index finger; (4) subject and experimenter extended thumb; (5) subject and experimenter did not move. The combination of these five conditions of movement with the four possible rotation angles (08, 2908, 908, 1808) and the two hands that could be indicated led to 40 different trials. For half of the trials ‘yes’ was the correct response; errors by saying no on these trials reflect miss-attribution to the other. For the other half the response should be ‘no’; errors by saying yes on these trials reflect miss-attribution to the self. Each trial was repeated ten times. The 400 resulting trials were randomized under the constraints that identical trials were not allowed to follow each other directly and that no more than three consecutive trials were allowed to be either in the same rotation angle or from the same movement condition. Then the 400 trials were split into eight blocks of 50 trials. The first four blocks formed session 1 and the remaining four blocks formed session 2. The order of presentation of the sessions was counterbalanced across subjects as was the order of presentation of the blocks within the sessions. The two sessions of the experiment – 45 min each – were run on separate days. Both sessions started with five practice trials. Each block began with one filler trial to verify the position of the hands. After two blocks there was a short break. 2.5. Data analysis For all subjects the proportion of errors in each combination of conditions was computed and submitted to a repeated measures analysis of variance (ANOVA). Move-
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ment (Index–Thumb, Thumb–Index, Index–Index, Thumb–Thumb, None), Rotation (08, 2908, 908, 1808) and Type of Miss-attribution (to Other, to Self) were treated as withinsubject factors. Sex was a between-subjects variable. Tukey’s post-hoc tests were used to analyze the differences between the levels of the factors.
3. Results A total of 1.4% of trials were considered invalid, because the subject executed a movement different from the required one, performed additional movements during or immediately after the required one, missed the beep or started the movement before the beep. Invalid trials were rejected and repeated. The mean proportion of erroneous responses over all conditions was 0.17 (SD ¼ 0.06). There was no significant correlation of Age and proportion of errors (Pearson’s r ¼ 0.33, P . 0.05). The ANOVA revealed a highly significant effect of Movement (univariate approach with Greenhouse–Geisser correction: F(2.07,26.90) ¼ 77.26, P , 0.00001; multivariate approach: V(4,10) ¼ 39.19, P , 0.00001). The effect of Rotation was also significant (univariate approach with Greenhouse–Geisser correction: F(2.10,27.32) ¼ 10.24, P ¼ 0.00041; multivariate approach: V(3,11) ¼ 5.23, P ¼ 0.017). Moreover, there was a significant interaction between Movement and Rotation (F(12,156) ¼ 4.77, P , 0.00001). The effect of Type of Miss-attribution reached significance (F(1,13) ¼ 6.27, P ¼ 0.026) and interacted with Movement (F(4,52) ¼ 3.58, P ¼ 0.012). Sex had no influence on the proportion of errors (F(1,13) ¼ 0.37, P ¼ 0.551). 3.1. Effect of Movement Tukey’s post-hoc tests showed that the proportion of errors for the Index–Thumb condition (M ¼ 0.014, SD ¼ 0.025) was not different from the Thumb–Index condition (M ¼ 0.015, SD ¼ 0.021, P , 1). Neither was there any difference between the Index– Index condition (M ¼ 0.23, SD ¼ 0.11) and the Thumb–Thumb condition (M ¼ 0.25, SD ¼ 0.11, P , 1). When the subject and the experimenter made the same movement (Index–Index or Thumb–Thumb), there were significantly more errors than when they made a different movement (Index–Thumb or Thumb–Index, P ¼ 0.001 for all comparisons). In the No Movement condition subjects made even more errors (M ¼ 0.34, SD ¼ 0.10). This condition differed significantly from all others (P , 0.001 for all comparisons). So, when the two hands made different movements, subjects could easily recognize their own hand. When the hands made the same movement, this was more difficult. Subjects had most difficulty in recognizing their own hand when there was no movement. 3.2. Effect of Rotation The proportion of errors was smallest for the trials with a 08 Rotation (M ¼ 0.11, SD ¼ 0.09). There were more errors for the 2908 Rotation (M ¼ 0.14, SD ¼ 0.08) and still more for the 908 Rotation (M ¼ 0.17, SD ¼ 0.08). Most errors were made in the 1808
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Rotation (M ¼ 0.25, SD ¼ 0.09). Tukey’s post-hoc tests showed that the 1808 Rotation differed significantly from all other rotations (P , 0.02 for all comparisons).
3.3. Interaction effect of Movement and Rotation Tukey’s post-hoc tests indicated that the Different Movement conditions (Index–Thumb and Thumb–Index) did not differ significantly from Different Movement conditions in other rotations (P , 1 for all comparisons). For the Same Movement conditions (Index– Index and Thumb–Thumb), however, the 1808 Rotation differed significantly from the 08 and 2908 Rotations (P , 0.012 for all comparisons). For the No Movement condition the 1808 Rotation differed significantly from all other Rotations (P , 0.0001). So, when the movements were similar or absent, the percentage of errors was influenced by the Rotation factor, but when there were different movements, Rotation had no influence. This is illustrated by Fig. 2.
3.4. Type of Miss-attribution Subjects made more errors by miss-attributing the experimenter’s hand to themselves (M ¼ 0.21, SD ¼ 0.13) than by attributing their own hand to the experimenter (M ¼ 0.13, SD ¼ 0.06). Fig. 3 shows that this type of miss-attribution was predominant in all rotations when movements were the same or absent.
Fig. 2. Mean proportion of errors for the different conditions of Movement per Rotation.
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Fig. 3. Mean proportion of errors as a function of Type of Miss-attribution per Rotation per Movement.
4. Discussion The present experiment reveals that self-recognition is a highly consistent process which depends on available cues. Our main finding was that, in the absence of morphological characteristics which were controlled by the presence of gloves, two main cues influenced self-recognition. First, the visual position of the hand with respect to the body. Second, the presence of movements, which was found to override other cues.
4.1. The role of spatial orientation of the hands When the two hands visually appeared at the loci corresponding to their real positions, subjects showed relatively little difficulty in recognizing their own hand. However, when the apparent locations of the hands were interchanged with respect to reality, as in the 1808 Rotations, they made attribution errors. Intermediate rotations resulted in an intermediate error rate. So, when subjects see a hand at the place where they feel their own hand, they tend to attribute that hand to themselves. Botvinick and Cohen (1998) concluded from their experiment in which synchronous tactile stimulation led subjects to feel their hidden hand to be at the locus of a visible dummy hand that a strong correlation of tactile and visual signals can be sufficient to cause self-attribution. The present experiment indicates that, in the absence of tactile stimulation, the contingency between visual and proprioceptive signals plays a similar role in self-recognition. The fact that spatial orientation influenced subjects’ recognition of their own hand, even though they could infer from the
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Different Movement conditions that this was not a reliable cue, suggests that this contingency is automatically taken into account in the process of self-recognition. 4.2. The role of finger movements When finger movements were present and these movements were clearly attributable to the self (i.e. they differed from those of the experimenter), no attribution errors were found. This result replicates those obtained in an earlier experiment (Daprati et al., 1997) where only one hand was shown to the subject: subjects correctly attributed the hand when the finger movements they saw were theirs or when the hand was that of the experimenter performing different movements. The surprising finding in the present experiment is that accurate self-recognition was possible for all orientations of the display, including the 1808 Rotation. In other words, when distinctive movements are available, subjects tend to recognize actions, not just hands. This fact that movement is the primary cue has implications for the general problem of self-recognition. In the present experiment, errors appeared when the two hands performed the same movements. The error rate amounted to 15–35% according to the degree of rotation of the display. When no movements were made, the error percentage increased to 25–50%. If movements were exactly the same for both hands, or if they were absent, the only cue for distinguishing the two hands would be orientation. From this assumption one would predict performance to be at chance level for the 2908 and 908 conditions, a little better for the 08 Rotations and a little worse for the 1808 Rotations. The fact that the error percentages were somewhat lower in the No Movement condition probably reflects remaining morphological differences (e.g. differences in hand size) which could not be eliminated. A recent experiment by Franck et al. (2001) may account for the residual selfidentification in the Same Movement conditions compared to the No Movement conditions. Subjects moved a joystick with their hand and watched the movement of a virtual hand, which either corresponded to their own movement or deviated from it by certain angles or temporal delays. They began to notice the discrepancy between their own and the distorted movements for delays of 150 ms or angular deviations of 158. In the present experiment movements made by the subject and the experimenter, although both in accordance with the instruction, might have presented larger temporal or angular differences and might thus have been recognized as different by the subject. 4.3. Pattern of attribution errors Finally, the present experiment revealed that subjects miss-attribute the indicated hand more often to themselves than to the other when movements are the same or absent. For normal subjects self-attribution might be a default attribution in circumstances where no clear cues for self-recognition are available. Pathological conditions where self-recognition appears to be altered may shed some light on the mechanisms involved in correctly attributing body parts to their owner and actions to their agent. Two main sets of data obtained from different pathological groups are available. First, patients suffering from lesions involving the parieto-occipito-temporal junction (usually in the right hemisphere) frequently deny ownership of the left side of their body. They may even report delusions about their left body half by contending that it
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belongs to another person in spite of contradictory evidence from touch or sight (Bisiach & Berti, 1987). Daprati, Sirigu, Pradat-Diehl, Franck, and Jeannerod (2000) studied a patient who had recovered from left hemiparesis and delusions about ownership of his left body half, but still suffered form tactile and proprioceptive deficits on that side. When this patient was shown an image of either his own moving hand or the hand of the experimenter, he denied seeing his own hand even when it was presented. The experimental situation seemed to reinstate the previous delusions of body ownership: the combination of deficient proprioceptive signals from the left hand and its unusual presentation on a TV screen made the subject unable to include it in his body representation. This observation stresses the importance of a coherence between visual and proprioceptive signals in selfrecognition and suggests that a stable body representation is required before one can profit from movement cues, as normal subjects do. Furthermore, it stresses the role of the parietal lobe in integrating these signals for building the body representation. The second set of data comes from experiments with schizophrenic patients. A particular group of schizophrenic patients (those of the ‘influenced’ type) presents alterations in their sense of agency. They may report experiencing that they are not the cause of their actions or thoughts, but that they are controlled by an external agent. However, although they fail to recognize themselves as agents of their actions, they still recognize themselves as the owners of the movements and the body parts through which these actions are executed. In experimental situations in which such patients are asked to recognize their moving hands, they are reliably more impaired than control subjects (Daprati et al., 1997; Farrer et al., in press; Franck et al., 2001). Although they made no errors when they saw their own hand or the hand of the experimenter making a different movement, the error percentage dramatically rose to 80% when they saw the experimenter’s hand making the same movement as their own (Daprati et al., 1997). These data indicate that schizophrenic patients with delusions are able to use movement cues in self-recognition when their own movements are clearly different from someone else’s movements. When the movements are similar, however, they have great difficulties recognizing their own hand. The results obtained by Franck et al. (2001) suggest why this is the case. These authors showed that schizophrenic patients with delusions attributed to themselves movements distorted by an angle of up to 308, as opposed to patients without delusions and normal subjects who recognized the discrepancy already at 158. Schizophrenic patients with delusions would be impaired in using movement cues, like deviations in the angle of a movement, in determining agency. In the above experiments where only one hand was presented at a time (the subject’s hand or an alien hand), influenced patients invariably miss-attributed the alien hand to themselves. However, in a recent experiment with two simultaneously visible hands, these patients used different decision criteria for both kinds of attribution and tended to miss-attribute their own actions more often to the experimenter than the converse (Farrer et al., in press). The present experiment shows that normal subjects, in contrast, made more errors by miss-attributing the experimenter’s hand to themselves than by miss-attributing their own hand to the experimenter. A possible link between impairments in self-recognition observed in patients with parietal lesions and schizophrenic patients seems to be provided by a PET study made by Spence et al. (1997). These authors found an increased activation in the right parietal cortex of influenced schizophrenic patients when they spontaneously executed actions and
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felt these actions to be imposed on themselves by external forces. Increased activity in right parietal cortex, as well as pathological exclusion of the same area, both lead to misrepresentation of the self. Acknowledgements We thank Marc Thevenet for his technical support and Chlo¨ e´ Farrer for her comments on the experiment. References Bahrick, L. E. (1995). Intermodal origins of self-perception. In P. Rochat (Ed.), The self in infancy. Theory and research (pp. 349–373). Amsterdam: Elsevier. Bahrick, L. E., & Watson, J. S. (1985). Detection of intermodal proprioceptive-visual contingency as a potential basis of self-perception in infancy. Developmental Psychology, 21, 963–973. Bisiach, E., & Berti, A. (1987). Dyschiria. An attempt at its systemic explanation. In M. Jeannerod (Ed.), Neurophysiological and neuropsychological aspects of spatial neglect (pp. 183–201). Amsterdam: Elsevier. Botvinick, M., & Cohen, J. (1998). Rubber hands ‘feel’ touch that eyes see. Nature, 391, 756. Daprati, E., Franck, N., Georgieff, N., Proust, J., Pacherie, E., Dalery, J., & Jeannerod, M. (1997). Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients. Cognition, 65, 71–86. Daprati, E., Sirigu, A., Pradat-Diehl, P., Franck, N., & Jeannerod, M. (2000). Recognition of self-produced movement in a case of severe neglect. Neurocase, 6, 477–486. Farne´ , A., Pavani, F., Meneghello, F., & Ladavas, E. (2000). Left tactile extinction following visual stimulation of a rubber hand. Brain, 123, 2350–2360. Farrer, C., Franck, N., Georgieff, N., Tiberghien, G., Marie-Cardine, M., Dalery, J., d’Amato, T., & Jeannerod, M. (in press). Confusing the self and other. Impaired attribution of actions in patients with schizophrenia. Schizophrenia Bulletin. Franck, N., Farrer, C., Georgieff, N., Marie-Cardine, M., Dalery, J., d’Amato, T., & Jeannerod, M. (2001). Defective recognition of one’s own actions in patients with schizophrenia. American Journal of Psychiatry, 158, 454–459. Gallagher, S. (1995). Body schema and intentionality. In J. L. Bermudez, A. Marcel & N. Eilan (Eds.), The body and the self (pp. 225–244). Cambridge, MA: MIT Press. Gallagher, S. (2000). Philosophical conceptions of the self: implications for cognitive science. Trends in Cognitive Science, 4, 14–21. Harris, C. S. (1965). Perceptual adaptation to inverted, reversed and displaced vision. Psychological Review, 72, 419–444. Nielsen, T. I. (1963). Volition: a new experimental approach. Scandinavian Journal of Psychology, 4, 225–230. Spence, S. A., Brooks, D. J., Hirsch, S. R., Liddle, P. F., Meehan, J., & Grasby, P. M. (1997). A PET study of voluntary movement in schizophrenic patients experiencing passivity phenomena (delusions of alien control). Brain, 120, 1997–2011.
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COGNITION Cognition 85 (2002) 177–187 www.elsevier.com/locate/cognit
Sense of body and sense of action both contribute to self-recognition Esther van den Bos a, Marc Jeannerod b,* a
Leiden University, Section Cognitive Psychology, Wassenaarseweg 52, 2333 AK, Leiden, The Netherlands b Institut des Sciences Cognitives, 67 Boulevard Pinel, 69675, Bron, France Received 7 December 2001; accepted 14 May 2002
Abstract Recognizing oneself, easy as it appears to be, seems at least to require awareness of one’s body and one’s actions. To investigate the contribution of these factors to self-recognition, we presented normal subjects with an image of both their own and the experimenter’s hand. The hands could make the same, a different or no movement and could be displayed in various orientations. Subjects had to tell whether the indicated hand was theirs or not. The results showed that a congruence between visual signals and signals indicating the position of the body is one component on which selfrecognition is based. Recognition of one’s actions is another component. Subjects had most difficulty in recognizing their hand when movements were absent. When the two hands made different movements, subjects relied exclusively on the movement cue and recognition was almost perfect. Our findings are in line with pathological alterations in the sense of body and the sense of action. q 2002 Elsevier Science B.V. All rights reserved. Keywords: Sense of body; Sense of action; Self-recognition
1. Introduction How do we recognize ourselves? Although this seems a bizarre question, it needs to be considered seriously. There are circumstances in everyday life where self-recognition may not be straightforward. Consider, for example, a situation like seeing one’s face in a mirror at the far wall of a restaurant while looking for an empty table, or seeing one’s hand through a hole. Because there is discontinuity between the body part we see and the rest of the body, an active process must take place in order to refer the body part to a representation of the whole body, what Gallagher calls our body image. According to this author * Corresponding author. Tel.: 133-4-37-911-212; fax: 133-4-37-911-210. E-mail address: [email protected] (M. Jeannerod). 0010-0277/02/$ - see front matter q 2002 Elsevier Science B.V. All rights reserved. PII: S 0010-027 7(02)00100-2
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(Gallagher, 1995, 2000), the body image is a representation (sometimes conscious, sometimes not) of an owned body, one that belongs to the experiencing self. Developmental studies provide evidence that self-recognition appears early in life. At the preconceptual stage, infants at 5 months of age are able to discriminate their own leg movements displayed in a mirror from those of another infant, presumably by making use of a perceived contingency between their own behavior and its effects (Bahrick & Watson, 1985). As they grow older the infants’ behavior will increasingly testify to their development of a conscious self-representation. Infants of 15–20 months of age, for example, will typically resolve the task of wiping a red spot stuck on their face, when they see themselves in a mirror (see Bahrick, 1995 for review). In the present study, we were interested in identifying the constituents of self-recognition in normal adult subjects. We focused on several potential sources of information indicated by the available literature to contribute to self-recognition. First, the matching of visual, tactile and proprioceptive signals originating from the same body parts contributes to an intermodal sensory image of the body. Second, the matching of one’s intentions and the bodily effects of self-generated actions contributes to a sense of the self as an agent. Concerning the contribution of sensory cues, many experimental results stress a prevalent role of vision over other senses in self-recognition: we feel our hand where we see it, not the converse. Optical distortion of the visually perceived position of a limb with respect to its felt position (e.g. by displacing prisms) produces no alteration of the sense of ownership: the position sense is actually recalibrated to conform with the visual information (Harris, 1965). This prevalence of vision was confirmed in experiments using a rubber hand. Botvinick and Cohen (1998) positioned a realistic rubber arm in front of subjects, while their real arm, hidden by a screen, was placed aside: tactile stimulation was applied simultaneously to the real and the rubber arms. After some time, the subjects experienced an illusion in which they felt the touch at the locus of the rubber arm (that they could see), not of their real (hidden) arm. In other words, the tactile stimulus was felt where it was seen, at the expense of a distortion of the felt position of the real arm. In addition, subjects spontaneously reported experiencing a clear sense of ownership for the rubber arm. According to other authors who replicated this experiment, the displacement of tactile sensations and the illusion of ownership disappear if the rubber arm is not properly aligned with the subject’s body (Farne´ , Pavani, Meneghello, & Ladavas, 2000). Body ownership, however, is only part of the problem of self-recognition. The self is most of the time an acting self. Body parts are moving with respect to one another and with respect to external objects as the result of intentional actions. It is common experience that our actions are readily self-attributed as a consequence of a normally perfect correlation between their expected effects and the flow of resulting (visual and proprioceptive) stimulation. This matching process provides the agent of an action with the sense that he is causing that action (the sense of agency). Again, however, situations may arise where this attribution becomes less than obvious. In social interactions (like playing a ball game) several people might participate in the same action and interact rapidly on the same object. In this situation an active identification process is needed to disentangle one’s hand among other hands. Both the sense of ownership and the sense of agency concur to self-identification: it is as essential to recognize oneself as the owner of one’s body as it is to
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recognize oneself as the agent of one’s actions. Indeed, the role of movement is implicit in many descriptions of self-recognition (e.g. in the developmental context). This point was the subject of experiments where subjects had to identify their own hand from an alien hand appearing at the same locus (Nielsen, 1963). In the experiment of Daprati et al. (1997), subjects were instructed to perform simple finger movements on command: when the movement performed by the subjects with their (unseen) hand departed from the movements made by the alien hand, no attribution errors were found. By contrast, when the alien hand performed the same movement as the subject, the error rate amounted to 30%: subjects tended to over-attribute to themselves movements that were grossly compatible with their own movements. In other words, subjects used movement as a cue for selfrecognition when the movement they saw matched more or less closely the representation they had of their own movement. In the present paper, we used a situation which combined uncertainty about the ownership of the subject’s hand and uncertainty about the agency of the movements performed with that hand. This situation, designed by Farrer et al. (in press), involved simultaneous presentation of two hands, one of which was the subject’s hand, the other being an alien hand. This situation is more realistic than the one used in previous experiments, since it involves ‘social’ interaction between two people, in which problems of self-recognition are most likely to arise. In social interactions people will generally be able to see both their own hand and the other’s. The question in self-recognition in this situation was therefore not whether an observed action corresponded to the action one had performed, but rather which of several observed actions was the one corresponding to the action performed by the self. 2. Methods 2.1. Participants Sixteen normal subjects (six males and ten females, mean age 28.6 years) volunteered to participate in the experiment. All but two were right handed. One male subject was later excluded, because he did not comply with the instructions. 2.2. Apparatus The experiment took place in a dimly lit room. The subject and the experimenter sat at the opposite sides of a table. The subject was facing an LCD screen positioned at 20 cm above the table at an inclination of 458 from the horizontal plane. The experimenter sat in front of a computer monitor and keyboard on the left of the LCD screen (see Fig. 1). Both the subject and the experimenter placed their right hand under the screen and folded their fingers over a support to make a relaxed fist. The support for the subject’s hand was located at approximately 40 cm from the subject’s frontal plane. The support for the experimenter’s hand was located approximately 10 cm further than the subject’s support, about 11 cm to the right. A mirror attached to the backside of the screen reflected the image of the two hands to a video camera positioned at a distance of 2 m from the screen. The camera was connected
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to a computer and the image was sent to a numeric video acquisition map. A program processed the digitized video image in real time (within 20 ms) and sent a black and white image of the hands onto the LCD screen and the computer monitor. The program allowed rotating the image displayed on the screen by 2908, 908 and 1808. So, the subject could see his or her own hand at the bottom of the screen, where it would be in reality (08 Rotation), at the top of the screen (1808 Rotation), at the left of the screen (908 Rotation) or at the right of the screen (2908 Rotation), while the experimenter’s hand was always in the opposite direction. The rotations provided the possibility to study how the recognition of one’s hand was influenced by the location where it appeared visually. To prevent recognition based on morphological characteristics, both the subject’s hand and the experimenter’s hand were covered with identical gloves. The presentation of the image was limited to 2 s to minimize the time available to study remaining morphological differences.
Fig. 1. Schematic representation of the experimental apparatus.
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2.3. Procedure At the beginning of each trial, one of three possible instructions was displayed on the LCD screen: ‘index finger’, ‘thumb’ or ‘none’. ‘Index finger’ meant that the subject should extend the index finger, ‘thumb’ meant that the subject should extend the thumb and ‘none’ meant that the subject should not move at all. When the experimenter pressed a key, the instruction was replaced by the image of the two hands. After 500 ms the computer produced a beep indicating the moment at which the subject and the experimenter should start their movements. On the trials when the subject was instructed to make a movement, the experimenter would either make the same or the alternative movement. Once the movements were performed, the screen returned dark within about 1 s. Subjects were required to leave their hands in the end position during this time and to return to the starting position when the image had disappeared. Then an arrow appeared on the screen pointing to a position where one of the hands had been (either to the left or to the right for the trials with rotations of 2908 and 908; either up or down for the trials with rotations of 08 and 1808). Subjects had to say ‘yes’ if they thought that the hand indicated by the arrow was their hand and ‘no’ if they thought that the hand indicated by the arrow was not their hand. The experimenter registered the response by pressing one of two keys on the keyboard and the next instruction appeared on the screen. 2.4. Design There were five conditions of movement: (1) subject extended index finger, experimenter extended thumb; (2) subject extended thumb, experimenter extended index finger; (3) subject and experimenter extended index finger; (4) subject and experimenter extended thumb; (5) subject and experimenter did not move. The combination of these five conditions of movement with the four possible rotation angles (08, 2908, 908, 1808) and the two hands that could be indicated led to 40 different trials. For half of the trials ‘yes’ was the correct response; errors by saying no on these trials reflect miss-attribution to the other. For the other half the response should be ‘no’; errors by saying yes on these trials reflect miss-attribution to the self. Each trial was repeated ten times. The 400 resulting trials were randomized under the constraints that identical trials were not allowed to follow each other directly and that no more than three consecutive trials were allowed to be either in the same rotation angle or from the same movement condition. Then the 400 trials were split into eight blocks of 50 trials. The first four blocks formed session 1 and the remaining four blocks formed session 2. The order of presentation of the sessions was counterbalanced across subjects as was the order of presentation of the blocks within the sessions. The two sessions of the experiment – 45 min each – were run on separate days. Both sessions started with five practice trials. Each block began with one filler trial to verify the position of the hands. After two blocks there was a short break. 2.5. Data analysis For all subjects the proportion of errors in each combination of conditions was computed and submitted to a repeated measures analysis of variance (ANOVA). Move-
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ment (Index–Thumb, Thumb–Index, Index–Index, Thumb–Thumb, None), Rotation (08, 2908, 908, 1808) and Type of Miss-attribution (to Other, to Self) were treated as withinsubject factors. Sex was a between-subjects variable. Tukey’s post-hoc tests were used to analyze the differences between the levels of the factors.
3. Results A total of 1.4% of trials were considered invalid, because the subject executed a movement different from the required one, performed additional movements during or immediately after the required one, missed the beep or started the movement before the beep. Invalid trials were rejected and repeated. The mean proportion of erroneous responses over all conditions was 0.17 (SD ¼ 0.06). There was no significant correlation of Age and proportion of errors (Pearson’s r ¼ 0.33, P . 0.05). The ANOVA revealed a highly significant effect of Movement (univariate approach with Greenhouse–Geisser correction: F(2.07,26.90) ¼ 77.26, P , 0.00001; multivariate approach: V(4,10) ¼ 39.19, P , 0.00001). The effect of Rotation was also significant (univariate approach with Greenhouse–Geisser correction: F(2.10,27.32) ¼ 10.24, P ¼ 0.00041; multivariate approach: V(3,11) ¼ 5.23, P ¼ 0.017). Moreover, there was a significant interaction between Movement and Rotation (F(12,156) ¼ 4.77, P , 0.00001). The effect of Type of Miss-attribution reached significance (F(1,13) ¼ 6.27, P ¼ 0.026) and interacted with Movement (F(4,52) ¼ 3.58, P ¼ 0.012). Sex had no influence on the proportion of errors (F(1,13) ¼ 0.37, P ¼ 0.551). 3.1. Effect of Movement Tukey’s post-hoc tests showed that the proportion of errors for the Index–Thumb condition (M ¼ 0.014, SD ¼ 0.025) was not different from the Thumb–Index condition (M ¼ 0.015, SD ¼ 0.021, P , 1). Neither was there any difference between the Index– Index condition (M ¼ 0.23, SD ¼ 0.11) and the Thumb–Thumb condition (M ¼ 0.25, SD ¼ 0.11, P , 1). When the subject and the experimenter made the same movement (Index–Index or Thumb–Thumb), there were significantly more errors than when they made a different movement (Index–Thumb or Thumb–Index, P ¼ 0.001 for all comparisons). In the No Movement condition subjects made even more errors (M ¼ 0.34, SD ¼ 0.10). This condition differed significantly from all others (P , 0.001 for all comparisons). So, when the two hands made different movements, subjects could easily recognize their own hand. When the hands made the same movement, this was more difficult. Subjects had most difficulty in recognizing their own hand when there was no movement. 3.2. Effect of Rotation The proportion of errors was smallest for the trials with a 08 Rotation (M ¼ 0.11, SD ¼ 0.09). There were more errors for the 2908 Rotation (M ¼ 0.14, SD ¼ 0.08) and still more for the 908 Rotation (M ¼ 0.17, SD ¼ 0.08). Most errors were made in the 1808
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Rotation (M ¼ 0.25, SD ¼ 0.09). Tukey’s post-hoc tests showed that the 1808 Rotation differed significantly from all other rotations (P , 0.02 for all comparisons).
3.3. Interaction effect of Movement and Rotation Tukey’s post-hoc tests indicated that the Different Movement conditions (Index–Thumb and Thumb–Index) did not differ significantly from Different Movement conditions in other rotations (P , 1 for all comparisons). For the Same Movement conditions (Index– Index and Thumb–Thumb), however, the 1808 Rotation differed significantly from the 08 and 2908 Rotations (P , 0.012 for all comparisons). For the No Movement condition the 1808 Rotation differed significantly from all other Rotations (P , 0.0001). So, when the movements were similar or absent, the percentage of errors was influenced by the Rotation factor, but when there were different movements, Rotation had no influence. This is illustrated by Fig. 2.
3.4. Type of Miss-attribution Subjects made more errors by miss-attributing the experimenter’s hand to themselves (M ¼ 0.21, SD ¼ 0.13) than by attributing their own hand to the experimenter (M ¼ 0.13, SD ¼ 0.06). Fig. 3 shows that this type of miss-attribution was predominant in all rotations when movements were the same or absent.
Fig. 2. Mean proportion of errors for the different conditions of Movement per Rotation.
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Fig. 3. Mean proportion of errors as a function of Type of Miss-attribution per Rotation per Movement.
4. Discussion The present experiment reveals that self-recognition is a highly consistent process which depends on available cues. Our main finding was that, in the absence of morphological characteristics which were controlled by the presence of gloves, two main cues influenced self-recognition. First, the visual position of the hand with respect to the body. Second, the presence of movements, which was found to override other cues.
4.1. The role of spatial orientation of the hands When the two hands visually appeared at the loci corresponding to their real positions, subjects showed relatively little difficulty in recognizing their own hand. However, when the apparent locations of the hands were interchanged with respect to reality, as in the 1808 Rotations, they made attribution errors. Intermediate rotations resulted in an intermediate error rate. So, when subjects see a hand at the place where they feel their own hand, they tend to attribute that hand to themselves. Botvinick and Cohen (1998) concluded from their experiment in which synchronous tactile stimulation led subjects to feel their hidden hand to be at the locus of a visible dummy hand that a strong correlation of tactile and visual signals can be sufficient to cause self-attribution. The present experiment indicates that, in the absence of tactile stimulation, the contingency between visual and proprioceptive signals plays a similar role in self-recognition. The fact that spatial orientation influenced subjects’ recognition of their own hand, even though they could infer from the
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Different Movement conditions that this was not a reliable cue, suggests that this contingency is automatically taken into account in the process of self-recognition. 4.2. The role of finger movements When finger movements were present and these movements were clearly attributable to the self (i.e. they differed from those of the experimenter), no attribution errors were found. This result replicates those obtained in an earlier experiment (Daprati et al., 1997) where only one hand was shown to the subject: subjects correctly attributed the hand when the finger movements they saw were theirs or when the hand was that of the experimenter performing different movements. The surprising finding in the present experiment is that accurate self-recognition was possible for all orientations of the display, including the 1808 Rotation. In other words, when distinctive movements are available, subjects tend to recognize actions, not just hands. This fact that movement is the primary cue has implications for the general problem of self-recognition. In the present experiment, errors appeared when the two hands performed the same movements. The error rate amounted to 15–35% according to the degree of rotation of the display. When no movements were made, the error percentage increased to 25–50%. If movements were exactly the same for both hands, or if they were absent, the only cue for distinguishing the two hands would be orientation. From this assumption one would predict performance to be at chance level for the 2908 and 908 conditions, a little better for the 08 Rotations and a little worse for the 1808 Rotations. The fact that the error percentages were somewhat lower in the No Movement condition probably reflects remaining morphological differences (e.g. differences in hand size) which could not be eliminated. A recent experiment by Franck et al. (2001) may account for the residual selfidentification in the Same Movement conditions compared to the No Movement conditions. Subjects moved a joystick with their hand and watched the movement of a virtual hand, which either corresponded to their own movement or deviated from it by certain angles or temporal delays. They began to notice the discrepancy between their own and the distorted movements for delays of 150 ms or angular deviations of 158. In the present experiment movements made by the subject and the experimenter, although both in accordance with the instruction, might have presented larger temporal or angular differences and might thus have been recognized as different by the subject. 4.3. Pattern of attribution errors Finally, the present experiment revealed that subjects miss-attribute the indicated hand more often to themselves than to the other when movements are the same or absent. For normal subjects self-attribution might be a default attribution in circumstances where no clear cues for self-recognition are available. Pathological conditions where self-recognition appears to be altered may shed some light on the mechanisms involved in correctly attributing body parts to their owner and actions to their agent. Two main sets of data obtained from different pathological groups are available. First, patients suffering from lesions involving the parieto-occipito-temporal junction (usually in the right hemisphere) frequently deny ownership of the left side of their body. They may even report delusions about their left body half by contending that it
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belongs to another person in spite of contradictory evidence from touch or sight (Bisiach & Berti, 1987). Daprati, Sirigu, Pradat-Diehl, Franck, and Jeannerod (2000) studied a patient who had recovered from left hemiparesis and delusions about ownership of his left body half, but still suffered form tactile and proprioceptive deficits on that side. When this patient was shown an image of either his own moving hand or the hand of the experimenter, he denied seeing his own hand even when it was presented. The experimental situation seemed to reinstate the previous delusions of body ownership: the combination of deficient proprioceptive signals from the left hand and its unusual presentation on a TV screen made the subject unable to include it in his body representation. This observation stresses the importance of a coherence between visual and proprioceptive signals in selfrecognition and suggests that a stable body representation is required before one can profit from movement cues, as normal subjects do. Furthermore, it stresses the role of the parietal lobe in integrating these signals for building the body representation. The second set of data comes from experiments with schizophrenic patients. A particular group of schizophrenic patients (those of the ‘influenced’ type) presents alterations in their sense of agency. They may report experiencing that they are not the cause of their actions or thoughts, but that they are controlled by an external agent. However, although they fail to recognize themselves as agents of their actions, they still recognize themselves as the owners of the movements and the body parts through which these actions are executed. In experimental situations in which such patients are asked to recognize their moving hands, they are reliably more impaired than control subjects (Daprati et al., 1997; Farrer et al., in press; Franck et al., 2001). Although they made no errors when they saw their own hand or the hand of the experimenter making a different movement, the error percentage dramatically rose to 80% when they saw the experimenter’s hand making the same movement as their own (Daprati et al., 1997). These data indicate that schizophrenic patients with delusions are able to use movement cues in self-recognition when their own movements are clearly different from someone else’s movements. When the movements are similar, however, they have great difficulties recognizing their own hand. The results obtained by Franck et al. (2001) suggest why this is the case. These authors showed that schizophrenic patients with delusions attributed to themselves movements distorted by an angle of up to 308, as opposed to patients without delusions and normal subjects who recognized the discrepancy already at 158. Schizophrenic patients with delusions would be impaired in using movement cues, like deviations in the angle of a movement, in determining agency. In the above experiments where only one hand was presented at a time (the subject’s hand or an alien hand), influenced patients invariably miss-attributed the alien hand to themselves. However, in a recent experiment with two simultaneously visible hands, these patients used different decision criteria for both kinds of attribution and tended to miss-attribute their own actions more often to the experimenter than the converse (Farrer et al., in press). The present experiment shows that normal subjects, in contrast, made more errors by miss-attributing the experimenter’s hand to themselves than by miss-attributing their own hand to the experimenter. A possible link between impairments in self-recognition observed in patients with parietal lesions and schizophrenic patients seems to be provided by a PET study made by Spence et al. (1997). These authors found an increased activation in the right parietal cortex of influenced schizophrenic patients when they spontaneously executed actions and
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felt these actions to be imposed on themselves by external forces. Increased activity in right parietal cortex, as well as pathological exclusion of the same area, both lead to misrepresentation of the self. Acknowledgements We thank Marc Thevenet for his technical support and Chlo¨ e´ Farrer for her comments on the experiment. References Bahrick, L. E. (1995). Intermodal origins of self-perception. In P. Rochat (Ed.), The self in infancy. Theory and research (pp. 349–373). Amsterdam: Elsevier. Bahrick, L. E., & Watson, J. S. (1985). Detection of intermodal proprioceptive-visual contingency as a potential basis of self-perception in infancy. Developmental Psychology, 21, 963–973. Bisiach, E., & Berti, A. (1987). Dyschiria. An attempt at its systemic explanation. In M. Jeannerod (Ed.), Neurophysiological and neuropsychological aspects of spatial neglect (pp. 183–201). Amsterdam: Elsevier. Botvinick, M., & Cohen, J. (1998). Rubber hands ‘feel’ touch that eyes see. Nature, 391, 756. Daprati, E., Franck, N., Georgieff, N., Proust, J., Pacherie, E., Dalery, J., & Jeannerod, M. (1997). Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients. Cognition, 65, 71–86. Daprati, E., Sirigu, A., Pradat-Diehl, P., Franck, N., & Jeannerod, M. (2000). Recognition of self-produced movement in a case of severe neglect. Neurocase, 6, 477–486. Farne´ , A., Pavani, F., Meneghello, F., & Ladavas, E. (2000). Left tactile extinction following visual stimulation of a rubber hand. Brain, 123, 2350–2360. Farrer, C., Franck, N., Georgieff, N., Tiberghien, G., Marie-Cardine, M., Dalery, J., d’Amato, T., & Jeannerod, M. (in press). Confusing the self and other. Impaired attribution of actions in patients with schizophrenia. Schizophrenia Bulletin. Franck, N., Farrer, C., Georgieff, N., Marie-Cardine, M., Dalery, J., d’Amato, T., & Jeannerod, M. (2001). Defective recognition of one’s own actions in patients with schizophrenia. American Journal of Psychiatry, 158, 454–459. Gallagher, S. (1995). Body schema and intentionality. In J. L. Bermudez, A. Marcel & N. Eilan (Eds.), The body and the self (pp. 225–244). Cambridge, MA: MIT Press. Gallagher, S. (2000). Philosophical conceptions of the self: implications for cognitive science. Trends in Cognitive Science, 4, 14–21. Harris, C. S. (1965). Perceptual adaptation to inverted, reversed and displaced vision. Psychological Review, 72, 419–444. Nielsen, T. I. (1963). Volition: a new experimental approach. Scandinavian Journal of Psychology, 4, 225–230. Spence, S. A., Brooks, D. J., Hirsch, S. R., Liddle, P. F., Meehan, J., & Grasby, P. M. (1997). A PET study of voluntary movement in schizophrenic patients experiencing passivity phenomena (delusions of alien control). Brain, 120, 1997–2011.