Special issue: Research reportFeeling touch on the own hand restores the capacity to visually discriminate it from someone else' hand: Pathological embodiment receding in brain-damaged patients
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.
References (61)
- et al.
A sensational illusion: Vision-touch synaesthesia and the rubber hand paradigm
Cortex
(2013) - et al.
The free-energy self: A predictive coding account of self-recognition
Neuroscience and Biobehavioral Reviews
(2014) - et al.
Behavioral, neural, and computational principles of bodily self-consciousness
Neuron
(2015) Embodiment, ownership and disownership
Consciousness and Cognition
(2011)- et al.
Mirror-view reverses somatoparaphrenia: Dissociation between first- and third-person perspectives on body ownership
Neuropsychologia
(2011) Philosophical conceptions of the self: Implications for cognitive science
Trends in Cognitive Sciences
(2000)- et al.
Embodiment of others' hands elicits arousal responses similar to one's own hands
Current Biology
(2014) - et al.
When your arm becomes mine: Pathological embodiment of alien limbs using tools modulates own body representation
Neuropsychologia
(2015) - et al.
Embodiment of an alien hand interferes with intact-hand movements
Current Biology: CB
(2013) - et al.
Expanding the mirror: Vicarious activity for actions, emotions, and sensations
Current Opinion in Neurobiology
(2009)
Matching categorical object representations in inferior temporal cortex of man and monkey
Neuron
More than skin deep: Body representation beyond primary somatosensory cortex
Neuropsychologia
What is embodiment? A psychometric approach
Cognition
Self awareness and the body image
Acta Psychologica
Mirror-touch synaesthesia changes representations of self-identity
Neuropsychologia
Cortical dynamics during naturalistic sensory stimulations: Experiments and models
Journal of Physiology, Paris
From intention to perception: The case of anosognosia for hemiplegia
Neuropsychologia
Modular structure of awareness for sensorimotor disorders: Evidence from anosognosia for hemiplegia and anosognosia for hemianaesthesia
Neuropsychologia
My body in the brain: A neurocognitive model of body-ownership
Neuropsychologia
Dynamic causal modeling of touch-evoked potentials in the rubber hand illusion
NeuroImage
Mechanisms of self-other representations and vicarious experiences of touch in mirror-touch synesthesia
Frontiers in Human Neuroscience
Mechanisms of production control and belief fixation in human visuospatial processing: Clinical evidence from hemispatial neglect and misrepresentation
Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia
Brain: A Journal of Neurology
Multisensory brain mechanisms of bodily self-consciousness
Nature Reviews. Neuroscience
Crossmodal illusions in neurorehabilitation
Frontiers in Behavioral Neuroscience
The extended mirror neuron Network: Anatomy, origin, and functions
The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry
Italians do it worse. Montreal Cognitive Assessment (MoCA) optimal cut-off scores for people with probable Alzheimer's disease and with probable cognitive impairment
Aging Clinical and Experimental Research
Rubber hands “feel” touch that eyes see
Nature
The bodily self and its disorders
Current Opinion in Neurology
Empathy or Ownership? Evidence from corticospinal excitability modulation during pain observation
Journal of Cognitive Neuroscience
Cited by (30)
Reach planning with someone else's hand
2022, CortexCitation Excerpt :According to previous studies (e.g., Pia et al., 2014; Piedimonte et al., 2016; Ricci et al., 2016), motor and tactile functions, as well as general cognitive impairment, personal and extrapersonal neglect were assessed through standardized neurological protocols (see details in Table 1 and caption). As in previous studies (Fossataro et al., 2017, Fossataro, Bruno, Gindri, et al., 2018; Fossataro, Bruno, Giurgola, et al., 2018), proprioception was assessed by means of two evaluation protocols for testing the limb localization: the Contralateral Limb Matching Task [CLMT (Goble, 2010; Lincoln et al., 1991; Piriyaprasarth et al., 2009)] and the Finger Localizing Test [FLT (Head & Holmes, 1911; Hirayama et al., 1999; Lincoln et al., 1991)]. To evaluate the presence/absence of pathological embodiment we employed a previously devised protocol (Garbarini et al., 2020; Pia et al., 2020).
Differentiating self-touch from social touch
2022, Current Opinion in Behavioral SciencesWhat pathological embodiment/disembodiment tell US about body representations
2020, NeuropsychologiaCitation Excerpt :In other words, the fact that the alien hand belongs to a young experimenter (thus being completely different from the patients’ hand) does not prevent the patients from considering it their own. It is as if E+ patients are no longer able to use the visual characteristics (e.g., the fingers length, the nails shape, the skin colour …) of the alien and their own hand to make their choice ( 2018c, Pia et al., 2020). This will be further discussed in the last part of the paper.
The anatomo-clinical picture of the pathological embodiment over someone else's body part after stroke
2020, CortexCitation Excerpt :Here we report how we determined our sample size, all data exclusions (if any), all inclusion/exclusion criteria, whether inclusion/exclusion criteria were established prior to data analysis, all manipulations, and all measures in the study. Participants were selected from a series of stroke patients admitted to four different rehabilitation centers from 2010 to 2017 and were included in previous published papers on the delusion of ownership (Fossataro, Bruno, Gindri, et al., 2018a, b; Fossataro et al., 2016; Garbarini et al., 2014; Garbarini et al., 2015; Garbarini & Pia, 2013; Garbarini et al., 2013; Pia et al., 2013). The inclusion criteria were the presence of a documented unilateral brain damage and contralesional upper limb motor and/or sensory deficits demonstrated by a neurological exam (see description below and scores in Table 1).
The sense of body-ownership gates cross-modal improvement of tactile extinction in brain-damaged patients
2020, CortexCitation Excerpt :Interestingly, the improvement of tactile extinction was similar in both main and control experiments. When visual and tactile stimuli were generated by the robotic hands movements, the observed improvement in the Alien-Hand-Condition could be due to the “sensory embodiment” [i.e., the tactile sensation reported by E+ patients while observing the examiner's hand being touched (Fossataro, Bruno, Pia, et al., 2018; Fossataro et al., 2016; Garbarini et al., 2014)]. In this condition, E+ patients might have reported bilateral stimulations more frequently, not because of the contralesional tactile detection improvement, but because the observed touches on the alien hand could induce tactile sensations irrespective of whether the real hand was touched.