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Rubber Hand : Evidence for of

La Ilusión de la Mano de Goma: evidencias de Integración multisensorial de la propriocepción A Ilusão da Mão de Borracha: Evidências de Integração Multissensorial da Propriocepção

Thiago Gomes de Castro*, William Barbosa Gomes* Universidade Federal do Rio Grande do Sul

Doi: http://dx.doi.org/10.12804/revistas.urosario.edu.co/apl/a.3430

Abstract definition, limits, and scope ofrhi ; (2) the physiolog- ical and neurocognitive evidence backing rhi; and This review seeks to describe a multisensory integration (3) the use of action based rhi experimental settings. hypothesis for proprioception through the description The paper concludes that rhi is a salient example of of different Rubber Hand Illusion (rhi) experimental a neuroscientific trend towards an integrated account settings. rhi is a created in 1998 to explore of body, , and perceptual space. The discovery of the relation between visual and tactile sensory systems. the illusion has also provided an alternative context for The task involves a synchronous stroking, using a paint- the study of proprioception and related brain dynamics brush, of one of a subject’s hands occluded from his in normal subjects. vision, and a prosthetic rubber hand located in front of Keywords: proprioception; perceptual illusion; multi- the subject. Instructed to look at the rubber hand, the sensory integration. subject starts to feel as if the rubber hand is his own hand after approximately half a minute, which is to Resumen say that the illusion produces a of ownership of the rubber hand. Additional research over the last La presente revisión tiene como objetivo describir una 15 years has widely explored these results, illustrating hipótesis de integración multisensorial para la propio- the dynamic functions of the brain and body sensory cepción a través de la descripción de distintos config- systems, as well as shedding light on the bases of am- uraciones experimentales con la Ilusión de la Mano de putee rehabilitation and different types of . Goma (img). img es un paradigma creado en 1998 para The review is structured around three topics: (1) the explorar la relación entre los sistemas sensoriales visual

* Universidade Federal do Rio Grande do Sul. E-mail: [email protected]

Cómo citar este artículo: DeCastro, T. G., & Gomes, T. B.. (2017). Rubber Hand Illusion: Evidence for Multisensory In- tegration of Proprioception. Avances en Psicología Latinoamericana, 35(2), 219-231. doi: http://dx.doi.org/10.12804/revistas. urosario.edu.co/apl/a.3430

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y táctil. La tarea implica una estimulación síncrona de dinâmicas dos sistemas sensoriais do cérebro e do cor- una mano de los sujetos, oculto de su visión, y una mano po, assim como clarificando aspetos da reabilitação de de goma en frente del sujeto. Instruidos para mirar la sujeitos amputados e diferentes tipos de parestesia. A mano de goma, después de aproximadamente medio revisão estrutura-se em torno a três temas: (1) definição minuto, el sujeto comienza a sentir la mano de goma da img, os seus limites e alcances, (2) evidências fisi- como su propia mano. La ilusión produce un sentimien- ológicas e neurocognitivas que dão apoio à img e (3) a to de propiedad de la mano de goma. La literatura ha img em configurações experimentais implicando ação. investigado ampliamente el experimento en los últimos A revisão conclui que a img é um exemplo prático de 15 años, demostrando las funciones dinámicas de los uma tendência neurocientífica inovadora para o estudo sistemas sensoriales del cerebro y del cuerpo, así como integrado do corpo, o cérebro e o espaço percetual. A clarificando aspectos de la rehabilitación de sujetos ilusão também tem estabelecido uma alternativa para amputados y diferentes tipos de parestesia. La revisión o estudo da propriocepção e a dinâmica do cérebro em se estructura en torno de tres temas: (1) definición de la sujeitos normais. img, sus límites y alcances, (2) evidencias fisiológicas Palavras-chave: propriocepção, ilusão percetiva, inte- y neurocognitivas que dan apoyo a la img, y (3) la img gração multissensorial. en configuraciones experimentales implicando acción. La revisión concluye que la img es un ejemplo práctico de una tendencia neurocientífica innovadora para el Introduction estudio integrado del cuerpo, el cerebro y el espacio perceptual. La ilusión también ha establecido una for- Proprioception was first explained as the re- ma alternativa para el estudio de la propiocepción y la sult of specific sensorial receptors located in deep dinámica del cerebro en sujetos normales. body tissue. In the present study, proprioception Palabras clave: propiocepción; ilusión perceptiva; in- will be approached through an integrated account tegración multisensorial. that considers the conjoint operation of different neuroanatomical structures and complex exec- Resumo utive command. The use of perceptual has helped to shape the path for this integrated A presente revisão tem como objetivo descrever uma view (e.g. Ehrsson, 2007; Guterstam, Björnsdotter, hipótese de integração multissensorial para a proprio- Gentile, & Ehrsson, 2015). In the specific case of cepção através da descrição de diferentes configurações proprioception, the Rubber Hand Illusion (rhi) experimentais com a Ilusão da Mão de Borracha (img). experiment (Botvinick & Cohen, 1998) clearly img é um paradigma criado em 1998 para explorar a conveys the notion of multiple processes acting relação entre os sistemas sensoriais visual e táctil. A conjointly to produce proprioception. This paper tarefa implica uma estimulação síncrona de uma mão will be developed in three sections: (1) a gen- dos sujeitos, oculto de sua visão, e uma mão de borra- eral description of the experimental conditions cha em frente ao sujeito. Instruídos para olhar a mão required to produce the rhi; (2) a brief review of de borracha, depois de aproximadamente meio minuto, neurocognitive and physiological evidence sup- o sujeito começa a sentir a mão de borracha como a porting the integrated account of proprioception sua própria mão. A ilusão produz um sentimento de in the rhi; and (3) the use of actions within the propriedade da mão de borracha. A literatura tem in- rhi setting that help to elucidate the multisensory vestigado amplamente o experimento nos últimos 15 integrated account. anos, demostrando as funções demonstrando as funções

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The Rubber Hand Illusion - General & Coslett, 2004). The rhi model has been used experimental conditions of occurrence since 1998 as a tool to investigate the basis of proprioception and space overall, es- Botvinick and Cohen (1998) carried out an pecially in the conjunction of visual and tactile experiment called the Rubber Hand Illusion (rhi) systems. Alternative explanations for the extent to evaluate intermodal proprioceptive integration of proprioceptive recalibration observed in rhi by producing tactile sensations and synchronous have recently been invoked, however, including visualization of touch in the limbs (figure 1). They the role of socio-emotional processes (Van Stralen produced a perceptual illusion by simultaneous- et al., 2014) and previous interoceptive sensitivi- ly stroking subjects’ real hands and prosthetic ty regarding body ownership (Suzuki, Garfinkel, rubber hand in the view of subjects. Participants Critchley, & Seth, 2013). These investigations recognized the rubber hand as their own hand af- have demonstrated that the proprioceptive recali- ter approximately half a minute of synchronous bration process observed in rhi cannot be regarded stroking. Although Botvinick and Cohen’s results as the product of exteroceptive pairing of visual did not provide evidence regarding which brain and tactile inputs alone. Other sources of sensory areas were activated during intermodal correlation, such as cardiac feedback and affective they indicated that simple stimuli pairing may be processing may lead to a better of sufficient to create self-attribution of prosthetic proprioceptive recalibration. body parts. Ehrsson et al. (2008) investigated the rhi among subjects who had undergone hemilateral upper limb amputation. Their research sought to deter- mine if the illusion created among this population Visual partition would be similar to the effect produced among Real left hand non-amputees. Their research hypothesis was that the somatosensory cortex would be greatly acti- vated during rhi in the amputee group. Taking into account the syndrome usually observed in amputees, the researchers that having an amputated limb could result in an even more realistic representational replacement of the Real right hand Paint brushes Prosthetic hand arm through the rhi. Their results corroborated Figure 1. Rubber Hand Illusion Setting the stronger illusion hypothesis among amputees compared to the control group. When comparing the illusion effect between preserved arms and The Rubber Hand Illusion was first explained amputated arms among amputee subjects, how- as a recalibration of real hand proprioception to ever, the results did not support the existence of the false hand as a consequence of a distortion in significant differences. In fact, therhi was weaker the interaction of visual, tactile, and proprioceptual in amputated limbs. Interestingly, results have sensation (Botvinick & Cohen, 1998). Propriocep- shown that the more recent the amputation, the tion has long proved to play an important role in stronger the illusion. This specific finding suggests guiding body representation and is considered the a progressive adaptation of body to the dominant sensory input to the on-line sef-represen- new post-amputation body condition. tation of the body in space (Shenton, Schwoebel

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In another experiment with amputated subjects are stroked simultaneously. Holmes, Snijder and called “ illusion” (Ramachandram & Rog- Spence (2006) corroborated this result, demon- ers-Ramachandram, 1996), the effect of replacing strating that minimally incongruent positions of a phantom limb with a mirror reflex of the pre- the rubber hand compared to the real hand being served limb is explained as the main result of a stroked reduced the strength of the illusion (e.g. visual overlap rather than a tactile effect. Mirror by turning the false hand 15° or more to the left illusion findings suggest a outcome or right side of the body). In addition, the rhi is —a perception of sensorial mixing resulting from not produced if a rubber hand in front of the body conflict between different sensory channels— in crosses the body midline (an imaginary vertical which visual orientation can produce a specific division between the left and right sides of the sort of tactile sensation. In the context of the rhi body) toward the non-stimulated hand (Cadieux, experiment, the addition of rather than Whitworth, & Shore, 2011). This evidence indi- a prosthetic hand to produce a recalibration of cates that previous representations and expectations ownership did not by itself prove to be a reliable of body image can also have a significant effect variable in producing a typical rhi effect (Ber- on proprioceptive recalibration (Constantini & tamini, Berselli, Bode, Lawson, & Wong, 2011). Haggard, 2007). Mirrors induced recalibration, but not of Haans, Ijsselsteijn and Kort (2008) found that ownership towards false hands as in earlier rhi the resemblance between the artificial hand and experiments. This indicated that tactile input, not the real hand is equally important to the strength visual information alone, remained a crucial factor of the illusion. According to these researchers, for producing the illusion. the visually perceived skin texture of the rubber Ehrsson, Spence and Passinham (2004) found hand is the most important independent variable evidence that the occurrence of the rhi was con- in producing the rhi. They found that variables ditioned by synchronous stroking of the real hand such as skin color, perceived gender-specific fea- and the rubber hand. Overall, 80 % of participants tures of the hand, or hand size did not directly or reported the expected illusion within an interval significantly interfere with the production of the of 15 seconds of synchronous stroking (Ehrsson, illusion. On the other hand, prosthetic hands man- Holmes, & Passingham, 2005). Asynchronous ufactured from wooden or metallic materials did stroking diminishes the effect or even eliminates not efficiently reproduce the typical propriocep- the proprioceptive illusion as a consequence of the tive drift. Synthetic materials resembling delay between feeling and seeing the touch skin, especially those manufactured from rubber (Shimada, Suzuki, Yoda, & Hayashi, 2014). While derivatives, are the ideal prosthetic materials for visuotactile synchronicity in stimulation is a pre- this purpose. Tsakiris, Carpenter, James, and Fo- ponderant factor in the illusion, it cannot by itself topoulou (2010) reached the same conclusion by explain the proprioceptive recalibration. varying stroking conditions and controlling the Tsakiris and Haggard (2005) demonstrated that materials from which false hands were produced. the illusion effect is significantly diminished or These researchers used a plain block of wood; a even eliminated, despite synchronous stroking, wooden hand; and a prosthetic hand with visual when the position or laterality of the rubber hand features similar to . The prosthetic hand are incompatible with the orientation of the real was the only one of the three that produced the ex- hand being synchronously stimulated by stroking. pected illusion. In more recent research, Kalckert The illusion effect is extinguished, for example, and Ehrsson (2012) showed that placing surgical when the real right hand and a prosthetic left hand gloves on both rubber and real hands produces

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the same proprioceptive illusion as in traditional neutral object (e.g. a table surface), as suggested rhi experiments. by Armel and Ramachandram (2003). This hy- An innovation in recreating the illusion was the pothesis inferred that the illusion was the result use of an online video projection of the subject’s of Bayesian perceptual . In this , it own hand being stimulated. Tsakiris, Prabhu, and suggested that the rhi would result solely from Haggard (2006) used online projections of partic- bottom-up mechanisms that link visuotactile events ipants’ own real hands over a plain black surface exclusive to stimulation synchronicity. This alter- as the “rubber hand” variable. The embodiment native explanation excluded previous representa- of the subjects’ own real hands through video pro- tional knowledge of the body (top-down processes). jections opened up the possibility of testing the In the Bayesian hypothesis, psychological con- rhi in virtual contexts. The effectiveness of cepts such as embodiment or selfhood would be the paradigm has been attested through different misleading because Bayesian principles of statis- experiments (Ijsselsteijn, DeKort, & Haans, 2006; tical correlation alone should be sufficient to ex- Slater, Perez-Marcos, Ehrsson, & Sanchez-Vives, plain why objects extraneous to the body could be 2008) showing that the feeling of ownership embodied regardless of their aesthetics. If so, the is replicated in virtual reality since the body’s rhi would be resistant to top-down knowledge of spatial references are respected, as discussed the body such as self-conscious body representa- above. tions. This discussion was partially resolved when Blefari, Cipriani, and Carrozza (2011) have researchers observed the brain areas involved in reported that today’s challenge for neuroprosthet- manifestations of the rhi and refuted the Bayesian ics is to produce artificial limbs with “ownership hypothesis, as will be described in the following feeling,” that can be recognized and felt as nat- section. urally as preserved limbs. To meet this goal, it is necessary for prosthetic limbs to appear very Neurocognitive and Physiological similar to real limbs, a condition that favors sta- Evidence in the rhi ble sensorimotor feedback in synchrony with the brain’s dynamic patterns. Marasco, Kim, Colgate, Ehrsson et al. (2005) pioneered the investigation Peshkin, and Kuiken (2011) have shown that the of brain areas involved in the rhi. Their results rubber hand effect is produced even among ampu- first demonstrated that the illusion effect increases tees with robotic prostheses. Robotic prostheses ventral premotor cortex activity, which they inter- are connected to the innervated skin of the resid- preted as the feeling of ownership of the rubber ual limb, and when induced so do so through rhi hand. They also observed increased activity in the experiment procedures, subjects feel the rubber bilateral intraparietal cortex. This region is linked hand to be their own, perceiving the rubber hand to the proprioceptive recalibration processing of to be their robotic hand with the same vivacity as the real hand towards the rubber hand. Another observed in non-amputee samples. The researchers brain structure affected and identified was the also measured this effect with a variable tempera- cerebellum. Activity in the cerebellum increased ture of the residual innerved limb, finding that real proportionally to the intensity of the reported il- limb temperature significantly and proportionally lusion during rhi. These findings corroborated correlated with the intensity of the illusion effect the multisensory hypothesis on proprioception, (Moseley et al., 2008). though it was still not explained how the brain These findings controverted the hypothesis temporally integrates different lobe activations. that a feeling of ownership can be induced in any Nevertheless, the observation of activity in ­multiple

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brain regions associated with ownership and pro- the posterior cingulate cortex is involved in body prioception during rhi contradicts the thesis that ownership and self-location of objects external to the rhi effect is the simple result of visual pairing the real body (Guterstam et al., 2015). In addition, interference based on synchronic visual and tactile Ehrsson, Wiech, Weiskopf, Dolan, and Passing- input, independent of previous body-action rep- ham (2007) have shown that physical threats to resentations, i.e. the Armel and Ramachandram the rubber hand prosthesis, such as hammering (2003) hypothesis. Ehrsson et al. (2005) concluded the rubber hand or threatening it with a knife, that rhi encompasses the activity of three neu- significantly increase subcortical activity related ral networks: 1) the multisensory integration of to anxiety and interoceptive . Re- parieto-cerebellar areas; 2) the recalibration of sults obtained through functional magnetic reso- proprioceptive representations for upper limbs in nance imaging (fmri) indicated that threatening the same circuit as a reach-to-grasp action occur- situations increased de activity in the insula and ring in the premotor cortex; and 3) a mechanism anterior cingulate gyrus. In a similar vein, Novaes, of body ownership, also in the premotor cortex. Gama, Melo, Araújo, and Franco (2011) used the Tsakiris (2010) reviewed the literature on rhi experiment to compare the power of the illusion to formulate a neurocognitive model hypothesis in conditions involving painful stimuli and a con- based on cumulative neurological findings. The trol consisting of regular stimulation. They found review showed that first, there seems to be a previ- that the presence of painful stimuli increases the ous representational body model that distinguishes illusion effect in comparison to regular stroking objects that can and cannot be part of the body. with a paintbrush. This result are parallel to the Second, the literature indicates that instantaneous findings of Ehrsson et al. (2007) on increased in- anatomical and postural representations of the body sula and cingulate gyrus activity when the rubber modulate the integration of multisensory informa- hand is threatened. tion and consequently lead to the recalibration of Although fmri studies have shown different the visual and tactile coordination systems. Third, brain areas related to body ownership and body the referred result of tactile feeling of the rubber schema codification, temporal contiguity between hand will lead to the subjective experience that tactile and visual stimulation remained an import- the prosthesis is part of the body. Tsakiris (2010) ant factor in explaining the rhi effect. Shimada, posits that these processes imply a neural network Fukuda, and Hiraki (2009) demonstrated that the composed of (a) the right temporo-parietal junc- criteria for synchronous and asynchronous strok- tion, which tests the non-corporeity of external ing follow specific temporal discrepancies. Syn- objects; (b) the secondary somato-sensorial cor- chronicity of visual and tactile stimulation below tex, which sustains an online representation of the 300ms induces stronger feelings of ownership of body; (c) posterior parietal and ventral premotor the rubber hand, whereas a temporal discrepan- cortices that encode information to recalibrate cy beyond 300ms induces progressively weaker the coordination system of the hand position; and ownership towards the rubber hand. As a result, (d) the right posterior insula, which underlies the the definition of synchronous and asynchronous subjective experience of rubber hand ownership. stroking must respect specific temporal contin- The multiple cortical areas explanation is not gencies. Studies applying electroencephalography always clear as to whether the rhi can be under- (eeg) to rhi pioneered the investigation of tem- stood as completely independent from subcortical poral contiguity between visual and tactile inputs activation. Recent research applying variations (Press, Heyes, Haggard, & Eimer, 2008; Sambo of the rhi have demonstrated, for example, that & Forster, 2009). The main contribution of these

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studies beyond the comprehension of temporal decreased the tactile processing of the stimulated discrepancies was the elucidation that proprio- real hand, an event also observed among patients ceptive integration does not rely exclusively on who report disembodiment of specific body re- previous representations of body, as suggested by gions after a stroke. Rohde, Wold, Karnath, and fMRI studies based on the activation of cortical Ernst (2013) added evidence regarding the limb structures. Somatosensory event-related potentials cooling effect observed in rhi. They found that if are present in synchronous stimulation before the stimulation was applied by a robot arm, the cool- activation of cortical areas associated with body ing correlate of rhi effect was not observed. The representation, which means that rhi comprises cooling effect was observed only when stimulation early stages (somatosensory activation) and later was synchronously and manually administered stages (preexisting body representations) of tactile by a researcher, which opens the discussion to processing. other factors of rhi production such as theories of Using EEG, Blefari et al. (2011) sought to map and affective processing. the electrical channels activated by the illusion Similarly, Barnsley et al. (2011) demonstrat- that were not studied in previous research using ed increased histamine production in the real fMRI. The results demonstrated that the frequency hand being stimulated during rhi. Histamine is of brain electrical activity measured by potential an enzyme associated with the immunological spectral density (psd), was compatible and pro- system, the production of which is an innate im- portional to the occurrence of illusion as repor­ mune response and is involved in autoimmune ted by participants. Specifically, a multisensory disorders like multiple sclerosis. The researchers activation of electrodes in the frontal, parietal, observed that during rhi, the stimulated real hand and central areas of the premotor cortex was re­ produced vasodilatation reactions and reddish pa­ gistered, corroborating the areas described in some pules as a combined reaction to previous histamine fMRI studies (Ehrsson et al., 2005; Ehrsson et al., injections. In the experiment, histamine injections 2008). In the same study, no differential electrical were administered previously to both stimulated activity was found in the referred areas when and non-stimulated hands. The observed vaso- testing for the asynchronous stroking condition, dilatation and skin reddening exclusively in the corroborating subjective reports of no feelings stimulated hand are typical reactions of increased of illusion in this specific condition (Lewis & histamine production in the area. The authors Lloyd, 2010). concluded that these reactions resulted from in- In addition to stimulating increased activi­ creased histamine reactivity due to decreased ty in some brain areas, rhi also affects body natural histamine metabolism (rhi direct effect) temperature. Moseley et al. (2008) observed in the region, a compensation mechanism that ­decreased temperature of the real hand being stim- also occurs under conditions of immunological ulated as participants ‘embodied’ the rubber hand, defense reaction. Another possible interpretation indicating proprioceptive drift and a selective de- is the antagonist effect of increased histamine in crease of blood flow in the region. It is important response to decreased production of compounds to note that reduced temperature was specific to the responsible for vascular integrity, such as adrenalin. limb or hand that was being replaced by the rubber Either way, the findings are consistent with the hy- hand. The same did not occur in the non-stimu- pothesis of a preconscious representational matrix lated real hand, nor in the ipsolateral foot. The in the brain that modulates homeostatic perceptual authors concluded that rubber hand ownership and immunological mechanisms.

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rhi experimental settings evolved toward would extinguish, diminish, or increase the illusion the investigation of hand-action effect in the effect, or if the illusion effect would be maintained proprioceptive drift. In this scenario, the multi- as in conventional rhi. Participants were exposed sensory integration account is strengthened as to three conditions: (1) voluntary movement of outlined in the following section. the index finger during stroking; (2) involuntary movement of the index finger during stroking; and rhi in Action: Active and Passive (3) a passive, static finger (the control condition). Movements in Experimental Settings The results indicated that the illusion was restricted to the index finger when stimulation patterns two According to Jones and Lederman (2006), Da- and three were performed. In stimulation pattern vid Katz (1884-1953), Geza Révész (1878-1955), one, the feeling of ownership of the rubber hand and James Gibson (1904-1979) were the main spread to the whole hand (active action condition), researchers in the first half of the 20th century to indicating that motor agency may integrate differ- work on the critical role of hand movements in the ent parts of the hand in a coherent sense, including development of human global perception. Katz non-stimulated regions of the hand. offered important evidence on tactile perception Kammers et al. (2009) also tested rhi in an and its functional contiguity to visual and auditory action setting. Participants were instructed to pro- perception. Révész investigated shape perception vide verbal judgment of the position of their felt through the hands, studying blind subjects and index finger after stroking, and point with their their manipulation of objects. This field of research non-stimulated hand to the felt position of the came to be known as haptics in the 1990s. Haptics stimulated hand. In addition, participants were has been described as the study of touch and the asked to perform alternate movements with the human interaction with the external environment stimulated hand during stroking, to evaluate the through touch (Jütte, 2008). Guided by the work impact of action on their final positional judgment of Katz and Révész, Gibson reinforced the evi- either for pointing with the non-stimulated hand, dence that hands have simultaneous perceptive or their verbal judgment. The main idea of the and executive functions leading to instantaneous experiment was to create noise with intervening recalibration of action and perception. The evo- action on the usual main effect of rhi. Using kin- lution of this field opened up a broad range of esthetic equipment on both hands, researchers research, from action to the motility of found that the kinesthetic noise created by point- hand control and proprioceptive recalibration in ing movement eliminated the main illusion effect, reaction to sensory conflict. while only moving the stimulated hand and asking In relation to haptics, rhi represents a fertile for verbal judgments did not affected the usual experimental setting to test associations between rhi. This specific result demonstrates that body proprioception and action control. Tsakiris et al. movement can either work antagonistically or as (2006), for example, argue that the tactile sensa- an integrator of the illusion, depending on how tion caused by rhi is fragmented and localized, and where the action performance occurs. normally restricted to the passive index being In that sense, DeCastro (2013) illustrated that stimulated. The authors replicated the experiment producing synchronous stimulation when the in an action setting to evaluate if the distortion real hand and the rubber hand are continuously produced by rhi is modified when induced by squeezing a tennis ball is not sufficient to create active index finger movements. They wanted to rhi. This researcher had originally used the rhi ascertain if putting a stimulated finger into action to understand how proprioceptive recalibration

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affects numerical estimation in visually tracking studies (Dummer, Picot-Annand, Neal, & Moore, peri-personal distances. The research focused on 2009; Riemer, Kleinböhl, Hölzl, & Trojan, 2013) the relation between space perception, active rep- have found stronger proprioceptive drifts in ac- resentation of space, and body proprioception. tive movement, this could be due to experimental Results showed that synchronous stimulation was setting designs, such as individual differences in the sole independent variable predicting changes in between-group comparisons or manual pointing both numerical space estimates and body proprio- procedures. Kalckert and Ehrsson (2014) conclud- ception. Interestingly, numerical space estimates ed that considering the earlier literature and the followed the non-numerical space recalibration of present data, active and passive movements elicit after passive rhi. When participants equally vivid rhi, and this illusion is as vivid as reported stronger effects of the illusion, space es- the classical version induced by passive stroking. timation distances were closer to the body midline On the other hand, even though efferent signals (rubber hand position). and voluntary motor command do not play a dif- Kalckert and Ehrsson (2012), also working with ferential role in the ownership illusion, they do an action rhi, tested the distinction between own- play a significant role in the feeling of agency ership and agency of the rubber hand by putting over the rubber hand. the real index finger and the rubber hand index Active manual movements led to some differ- finger in motion. Their findings first indicated that ent conclusions compared to previous rhi experi- asynchronous finger movement on the rubber hand ments, when real hands were passively stimulated. and the real hand extinguished both the feeling of Features such as prosthesis size, which were in- ownership and the feeling of agency of the rubber significant for the main illusion effect, acquired hand, but this was not the case when the index relevance in action settings. Haggard and Jundi finger was put into active motion during the ex- (2009) showed that the bigger the rubber hand periment. Second, when the fingers were put into presented, the heavier the object being held by the motion mechanically (passive action), there was real hand seemed. The research demonstrated that proprioceptive illusion in addition to synchronous regardless of the real weight of objects being held moving of the rubber index finger and the real by rubber hands and real hands, the perception of index finger, but there was no feeling of agency weight is directly proportional to the size of the of the rubber hand. Finally, when finger move- rubber hand in action, if within the . ments were both synchronous and voluntary, the Heed et al. (2011) corroborated these findings with observed result was a robust feeling of ownership research showing that the bigger the prosthesis size, and a strong feeling of agency of the rubber hand. the greater the grasping effort to hold a neutral ob- They then retested the same setting (Kalck- ject. They explained that this correlation was the ert & Ehrsson, 2014) and found that the illusion result of enhanced confidence in proprioceptive occurred whether it was elicited by an active or information due to distorted visual information passive index finger movement. The strength of represented by wrong hand size. It seems that the illusion was not significantly different and the the brain tries to rely on proprioceptive informa- proprioceptive drift was equally strong across the tion, balancing distorted large hand image with conditions. The observation that the active move- stronger grasping. Interpreting this effect, Haggard ment did not improve the illusion does not support and Jundi (2009) affirmed that body self-repre- the hypothesis that efferent signals associated with sentation provides references for comparison to voluntary motor commands play a differential role compensate for illusory of objects in ownership feelings during rhi. Although other outside the body.

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In line with proprioceptive drift studies, Honma Repercussions of rhi applications in clinical et al. (2014) tested whether subjective feelings of are well described in a review by ownership and proprioceptive drift measured by Ramakonar, Franz, and Lind (2011). Their study active reaching movements were resistant to sleep. compares effects observed in rhi to similar con- They assessed learning indexes of participants ditions of paresthesia resulting from strokes, or after routine and repetitive daily exposure to rhi. temporary paresthesia resulting from drug and Their results indicated that subjective ownership alcohol abuse. The rehabilitation of amputees is remained stable and proprioceptive drift increased also a focus of the review, which discusses how with daily training, showing increased performance knowledge of rhi mechanisms can be useful in the in reaching movements. Proprioceptive drift —but adaptation to prosthetic limbs. Nicolelis (2011) not subjective ownership— was significantly atten- has mentioned rhi as a breakthrough experiment, uated after sleep. These researchers concluded that of great relevance to the machine-human rehabil- although repetitive rhi training facilitates multi­ itation field, especially because it has provided sensory integration and physiological habituation descriptions of brain networks associated with to an incongruent multisensory environment, sleep different sensory processes. corrects illusional integration and habituation of Christ and Reiner (2014) also shed light on proprioceptive drift. Subjective ownership of a possible applications of rhi in non-invasive reha- rubber hand seemed to be a stable and resistant bilitation, emphasizing the need for technological process, unlike the active use of non-stimulated evolution in order to exploit information derived effectors to incorporate incongruent multisensory from rhi experiments to meet the demands of environments. Still, current findings in sensory immersive virtual rehabilitation. In this sense it feedback demonstrate a promising line of research is important to note that rhi assessment offers in the active use of prosthetic hands by upper limb potential new avenues for developing effective amputees (Antfolk et al., 2013). The challenge in rehabilitation and stimulation programs. this field is to translate sensory feedback systems rhi experimentation may be applied to purposes between tactile sensation and action control into ranging from the teaching of basic psychological routine long term use. processes to neuropsychological and clinical re- habilitation contexts. Its richness resides in the Concluding Remarks unexpected implications that a simple experiment can bring to the mainstream discussion regard- Even though rhi is just a perceptual illusion, it ing the nature of mind and body relationships. illustrates that body and brain interact to create a In this case, the postulation of an integrated ac- consistent and coherent sense of body integrality. count for proprioception including brain, body, Our review has shown that rhi was first created and perceptual space recalls current debates over as a simple tool to demonstrate the relationship the definition and study of embodied between visual and tactile systems. It has devel- (Wilson & Golonka, 2013) in which rhi is directly oped over the last decade, however, into a useful involved (e.g. Longo, Schüür, Kammers, Tsakiris, experimental setting for investigating complex & Haggard, 2008). Recent technology and new brain networks and the interplay between action methods for the study of embodied cognition and and perception. It has evolved into a central site the action-perception axis may benefit from the for a broad theoretical discussion about underlying use of rhi experiments and should be addressed body representation, the empirical basis for pro- specifically in a future review. prioception, and the extension of brain plasticity.

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Received: october 26, 2014 Accepted: october 18, 2016

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