Elsevier

Cortex

Volume 104, July 2018, Pages 207-219
Cortex

Special issue: Research report
Feeling touch on the own hand restores the capacity to visually discriminate it from someone else' hand: Pathological embodiment receding in brain-damaged patients

https://doi.org/10.1016/j.cortex.2017.06.004Get rights and content

Abstract

The sense of body ownership, i.e., the belief that a specific body part belongs to us, can be selectively impaired in brain-damaged patients. Recently, a pathological form of embodiment has been described in patients who, when the examiner's hand is located in a body-congruent position, systematically claim that it is their own hand (E+ patients). This paradoxical behavior suggests that, in these patients, the altered sense of body ownership also affects their capacity of visually discriminating the body-identity details of the own and the alien hand, even when both hands are clearly visible on the table. Here, we investigated whether, in E+ patients with spared tactile sensibility, a coherent body ownership could be restored by introducing a multisensory conflict between what the patients feel on the own hand and what they see on the alien hand. To this aim, we asked the patients to rate their sense of body ownership over the alien hand, either after segregated tactile stimulations of the own hand (out of view) and of the alien hand (visible) or after synchronous and asynchronous tactile stimulations of both hands, as in the rubber hand illusion set-up. Our results show that, when the tactile sensation perceived on the patient's own hand was in conflict with visual stimuli observed on the examiner's hand, E+ patients noticed the conflict and spontaneously described visual details of the (visible) examiner's hand (e.g., the fingers length, the nails shape, the skin color…), to conclude that it was not their own hand. These data represent the first evidence that, in E+ patients, an incongruent visual-tactile stimulation of the own and of the alien hand reduces, at least transitorily, the delusional body ownership over the alien hand, by restoring the access to the perceptual self-identity system, where visual body identity details are stored.

Introduction

The sense of body ownership (i.e., the feeling that our different body parts belong to us; Blanke et al., 2015, Gallagher, 2000) is something that we typically take for granted. However, experimental manipulations in healthy people, such as the rubber hand illusion (RHI) (Botvinick & Cohen, 1998), can temporarily alter the sense of body ownership. During the RHI, the subjects watch a lifelike rubber hand being touched while their own hand, hidden from view, is touched at the same time. This manipulation creates the disturbing feeling that the artificial hand is part of the own body, and the real hand can be somehow ‘disembodied’ (Della Gatta et al., 2016, Longo et al., 2008, Moseley et al., 2008), although subjects always know that the rubber hand is not part of their body. More dramatic body ownership alterations can be observed in pathological conditions (Brugger & Lenggenhager, 2014). Brain damage can disrupt the sense of body ownership and make patients convinced that one of their upper or lower limbs does not belong to them but to another person, as in the somatoparaphrenic syndrome (Bisiach et al., 1990, Vallar and Ronchi, 2009). Recently, a complementary body awareness disorder has been described where brain-damaged patients claim that the examiner's hand is their own hand, whenever it is located in a body-congruent position. Because of this pathological embodiment, we named them E+ patients (Fossataro et al., 2016, Garbarini et al., 2014, Garbarini et al., 2015, Garbarini et al., 2013, Garbarini and Pia, 2013, Pia et al., 2016, Pia et al., 2013). In order to observe this phenomenon, the co-examiner's hand must be placed on the table next to the patient's contralesional affected hand, aligned with the patient's shoulder and, therefore, perceived in egocentric perspective. In this set-up, when the examiner asks the patient to identify his/her own affected hand, either by reaching with his/her intact hand or by naming a colored object in front of it, the patient systematically identifies the examiner's hand as his/her own. By contrast, pathological embodiment does not occur when the alien hand is misaligned with the patient's shoulder, when it is perceived in allocentric perspective or positioned in the intact ipsilesional body-side and when, instead of a human hand, a rubber hand is used. Considering the E+ patients' neurological characteristics, pathological embodiment seems to be strongly associated to severe primary sensory-motor deficits as well as to other cognitive deficits, such as neglect and personal neglect. However, none of these deficits alone can explain pathological embodiment because double dissociations between embodiment, neglect and primary sensory-motor deficits have been described (Garbarini, Pia, Fossataro, & Berti, in press). It is interesting to note that, the incidence of somatoparaphrenia in E+ patients is quite low. This, in turn, is consistent with the fact that this disease is rarely observed after the first week post-stroke (Vallar & Ronchi, 2009), whereas the pathological embodiment is reported in the sub-acute or chronic phase of the illness (Fossataro et al., 2016, Garbarini et al., 2013, Garbarini et al., 2014, Garbarini et al., 2015, Garbarini and Pia, 2013, Pia et al., 2016, Pia et al., 2013). However, when both the own and the alien hands are present and the examiner explicitly asks about their ownership, E+ patients not only misidentify the alien hand as their own, but also misattribute their own hand to the other person. In other words, E+ patients show, only in this condition, an explicit sense of disownership. The coexistence of the two delusional beliefs (i.e., disownership of the own hand and ownership of an alien hand) in the same patient, suggests that these two forms of body delusion might share at least some features. Accordingly, a previous study investigating the relationship between asomatognosia and RHI in stroke patients suggested that a number of asomatognosic patients, with impairment of the ability to perceive their real hand as belonging to them, easily integrated the fake hand as their own (Zeller, Gross, Bartsch, Johansen-Berg, & Classen, 2011).

One of the most counterintuitive observations related to E+ patients' behavior is that pathological embodiment occurs not only with a static alien hand, but also when the alien hand moves or when it is touched. Indeed, when E+ patients observe the examiner's hand reaching for an object or being stimulated, they experience to move their own hand (Fossataro et al., 2016, Garbarini et al., 2013, Garbarini et al., 2015) or to feel tactile sensations on it (Fossataro et al., 2016, Garbarini et al., 2014, Pia et al., 2013). With respect to the motor domain, it is interesting to note that E+ patients with contralesional hemiplegia are usually aware of their motor deficits and, when they are asked to move their affected hand, they perfectly know that they cannot perform any movement (i.e., they are not anosognosic). Thus, we could expect that, when the alien hand moves, the pathological embodiment would recede and patients would correctly recognize that the moving hand is the examiner's hand and not their own. On the contrary, what we found is that, when the alien hand moves, E+ patients claim they are moving their own (paralyzed) hand (Fossataro et al., 2016, Garbarini et al., 2013, Garbarini et al., 2015). This suggests the presence of a top-down control of the sense of body ownership on motor awareness. When E+ patients are not in the embodiment condition, they are aware of their motor impairment, whereas when body awareness is affected by the experimental manipulation, then they seem to feel that their left (paralyzed) hand moves. Interestingly, other aspects of motor cognition are affected by the sense of body ownership such as the sense of agency because E+ patients ascribed the alien hand's movements to themselves (Fossataro et al., 2016, Garbarini et al., 2013, Garbarini et al., 2015).

With respect to the sensory domain, it is important to note that E+ cases with spared tactile sensibility on both hands have been described (Fossataro et al., 2016, Garbarini et al., 2014, Pia et al., 2013). In these cases, we could expect that, when the patients observe the alien hand being stimulated without receiving tactile stimuli on their own hand, the pathological embodiment would recede and the patients would correctly recognize that the stimulated hand was the examiner's hand and not their own. On the contrary, what we found is that, when E+ patients observe the alien hand being touched, they report to feel tactile sensation on their own hand (Garbarini et al., 2014, Pia et al., 2013). It is important to note that the tactile sensation on the alien hand is reported either when they had intact tactile sensibility on the own hand [a few cases with spared tactile sensibility have been described (Fossataro et al., 2016, Garbarini et al., 2014, Pia et al., 2013)] or when the own hand is affected by tactile anesthesia but they do not acknowledge the sensory deficit (anosognosia for hemianaesthesia; see Pia et al., 2014b, Pia et al., 2014a, Pia et al., 2014b). On the other hand, when patients are aware that they cannot feel any tactile stimulation on the own hand (hemianaesthesia without anosognosia), they did not report to experience any tactile stimuli on the alien hand. These observations suggest that the belief the patients have, not only about their body, but also about their sensory abilities (whether true or false) is transferred to the alien hand, once it is embodied (Pia et al., 2013). This means that this delusion of body ownership meets the criteria of a recently proposed definition of the embodiment concept, claiming that others' body parts can be considered as fully embodied, “if and only if”, as in these patients, “some properties of them are processed in the same way as the properties of one's own body” (De Vignemont, 2011).

In the present paper, we asked whether, and to what extent, this altered sense of body ownership, exerting top-down modulation on sensory perception, can be contrasted by a bottom-up multisensory conflict between what the patients feel on the own hand and what the patients see on the alien hand, restoring a coherent sense of self (Gentile, Guterstam, Brozzoli, & Ehrsson, 2013). To this aim, three rare cases of E+ patients with spared tactile sensibility on the contralesional body parts were selected. Together with two control groups (E-patients with similar neurological/neuropsychological characteristics and age-matched healthy subjects), they took part in two experiments. In both experiments, the examiner's hand (i.e., alien hand) was always visible on the table while the patient's hand was hidden from view (as in the RHI set-up). Patients were asked to rate their sense of body ownership over the alien hand, either after segregated tactile stimulations of the own hand (out of view) and of the alien hand (visible on the table) (Experiment 1) or after synchronous and asynchronous tactile stimulations of both hands, as in the RHI set-up (Experiment 2). See details in section 2.2 and in Fig. 1A and B. In Experiment 1, we hypostasized that to feel a touch on the (hidden) own hand, while the alien (visible) hand is not touched, should create a multisensory conflict that may reduce (or even cancel) the pathological embodiment over the alien hand. In Experiment 2, we hypostasized that, in the asynchronous condition, where both hands are stimulated but with a temporal difference, the strength of the pathological embodiment might be reduced.

Section snippets

Patients' recruitment and participants

Six brain-damaged patients of cerebrovascular origin, with contralesional upper limb sensory-motor deficits, were recruited at the “San Camillo” Hospital (Turin, Italy). Exclusion criteria were: 1) previous neurological or psychiatric history; 2) severe general cognitive impairment [i.e., patients under the MOCA cut off were excluded (Bosco et al., 2017)]; 3) visual field deficits (i.e., patients with hemianopia were excluded); 4) tactile deficits [i.e., we included patients without

Experiment 1

In healthy controls group, Wilcoxon test, at both Ownership and Sensation statement, does not showed a significant difference between Own and Alien condition [mean ± standard deviation; Ownership statement: Alien = .6 ± 1.57; Own = 2.3 ± 3.88; Z = 1.278019; p = .20; r = .40; Sensation statement: Alien = .8 ± 1.3; Own = 1.3 ± 3.19; Z = .13484; p = .89; r = .04). This means that healthy subjects gave similarly low ratings in both conditions, suggesting that segregated stimulations of the own and

Discussion

When patients with pathological embodiment (E+ patients) look at the examiner's hand, located in a body-congruent position, systematically claim that that hand is their own. In the present study, we asked whether, in E+ patients with spared tactile sensibility, a coherent body awareness can be restored, when a multisensory conflict between what the patients feel on the own hand and what they see on the alien hand is introduced (Gentile et al., 2013). Indeed, we found that, when tactile

Conclusion

Previous studies demonstrated that experimental procedures inducing a multisensory conflict between touch and vision have been satisfactorily applied in clinical rehabilitation contexts. Indeed, cross modal illusions, such as the mirror box illusion and the RHI, seem to be useful in restoring, at least in part, disorders of body representation related to pain, sensory, and motor impairments in neuropsychological and neurological diseases (Bolognini, Russo, & Vallar, 2015). The present findings

Acknowledgements

The authors are grateful to all of the patients and volunteers involved in the study. This work has been funded by MIUR-SIR 2014 grant (RBSI146V1D) and by the San Paolo Foundation 2016 grant (CSTO165140) to F.G.

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