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Phantomology: The Science of the Body in the Brain


Notes: A Neurobiological diagnosis with aesthetic, cultural and philosophical implications.
Part 1: The Body Fantastic: Neuroscientific Explanations

Acknowledgment:
Part of the work described here was funded by the Swiss National Science Foundation (grant no. 3100-67168.01). This essay is a condensation of several recent publications by the author, focusing on phantoms of congenitally absent limbs (Brugger and Funk, 2005), supernumerary phantoms (Brugger, 2003), hemiphantoms and phantoms of one’s entire body (Brugger, in press), respectively.

Abstract

Three stereotypes are apparent in popular conceptions of and current research in phantom limbs. First, there is a relative overemphasis of painful post-amputation phantoms. Second, phantom sensations are too unilaterally conceived as sensorimotor memories of a once functional limb. Third, there is a bias toward the investigation of phantoms of single body parts. My presentation will focus on non-painful, non-amputation phantom phenomena. Observed in people with a limb missing since birth, they defy an explanation in terms of perceptuo-motor memories. Targeting one half of the body (“hemiphantoms”) or the entire body (as for instance in out-of-body experiences) they point to phantomization processes in their most general form. I try to delineate the scope of a proper “phantomology” (Stanislaw Lem) whose aim is to study the virtual reality of bodily awareness – from phantom limb to phantom body.

The present paper provides a phenomenological account of phantom experiences, i.e., experiences of a discrepancy between the spatial extents of physical and phenomenal body. As the current literatur is heavily biased toward the experience of phantom limbs after amputation (see Ramachandran and Hirstein, 1998, for overview), and the prime association to the term “phantom limb” is “pain”, I will concentrate on a discussion of non-painful non-amputation phantoms. To counter a further stereotype, i.e. the conception that any phantom limb experience would reflect the evocation of sensorimotor memories of a once functional limb, special emphasis will be given, in the opening section, to “congenital phantoms”, a term we use to designate the phantom limb experience reported by people born without the respective limb. The notion that the brain’s “re-membering” would be the sole source of phantom experiences is misleading in another respect: “re-member” suggests that only single limbs as members of a body would be resurrected after their loss. Yet, a discussion of hemiphantoms and the phantom of one’s entire body (the “phantom double”) will show that this is not the case. These latter types of phantoms clearly show that a proper phantomology as envisaged by Stanislaw Lem (Lem, 1964/1981) will have to consider representations of the self as much as representations of the body.

1. Congenital phantoms

In Berne, Switzerland, physiologist Gabriel Gustav Valentin (1810-1883) published his observations on the „Subjective sensations of persons born with incomplete extremities“ (Valentin, 1836). Theories that explain phantom limb sensations by a process of re-membering were already popular at these times (for a historical overview see Finger and Hustwit, 2003), but did not convince Valentin. Thus, in a deliberate attempt to falsify these theories, he systematically questioned persons with congenital limb deficiencies about phantom sensations of their missing limbs. A girl born without a left hand reported the phantom presence of a regular palm including all 5 fingers. Valentin was not satisfied by this purely subjective report, and “objectified” it by a simple manipulation. Specifically, he provoked paresthesias in some of the phantom fingers by prolonged pressure on certain nerves in the stump. As the pattern of innervation in the fingers could not be known by his subjects (three more persons with congenitally absent limbs reported phantoms as well), the fact that tingling sensations were elicited in the “correct” phantom fingers was taken as evidence for the genuineness of the reported phantoms.
On the basis of these observations, Valentin concluded that „[the sensation of a phantom] by persons born with limb dysplasias teaches us that it is out of the question that they could be accounted for by memory or recollective imagery” (p. 334). He vaguely proposed that peripheral and central nervous system factors were probably involved in the genesis of a congenital phantom limb. Later proposals may have been more specific, yet they were also less convincing, as the suggested mechanisms could easily been shown to be of limited value: they could only hold for a very specific subset of patients born with an incomplete body. We provide three examples.

Example 1: a theory based on functional finger rudiments

In many persons reporting congenital phantoms, absence of proximal limb structures is accompanied by an at least rudimentary preservation of distal body parts. For instance, small finger rudiments would be attached to an arm stump or to the shoulder. Interestingly, such rudiments have often a functional value to the person, i.e. they can be most skillfully used for certain manipulations and even show an abnormally enhanced motility. Phantom sensations of congenitally absent hands or arms have thus been conceived of as kinesthetic illusions of these distal body parts (Simmel, 1961). This idea may make make sense in the context of a very particular subset of limb dysplasia. Obviously, however, it cannot explain the occurrence of phantoms for limbs missing in their entirity or for highly specific features of distal phantom parts, such as entire sets of properly arranged fingers.

Example 2: a theory based on spared representations of an intact limb

Many case reports of congenital phantoms are about persons who lack only one single limb since birth. Accordingly, the patient’s phantom sensations were interpreted as transpositions of sensorimotor maps of the intact limb from one hemisphere to the other (e.g., Burchard, 1965; Grouios, 1996). It is most evident that, as convincing such a theory may appear for the cases of unilateral absence of one limb, it fails to account for the situation where both upper and/or lower limbs are missing. Such cases are not unique (e.g., Weinstein and Sersen, 1961; Poeck, 1964; Saadah and Melzack, 1994; Brugger et al., 2000), and already Valentin (1836, p. 643) recognized their theoretical importance. The phantom sensations reported by persons with bilateral limb aplasia are not qualitatively different from those described after unilateral defect.

Example 3: a theory of congenital arm phantoms based on fetal hand-mouth coordination

Based on behavioral and ultrasonic data on thumb suckling behavior of human fetuses that show a functional link between hand movements and anticipatory mouth opening, Gallagher et al. (1998) proposed an innate motor schema of hand-mouth coordination as responsible for phantoms of congenitally absent limbs. In the absence of a hand, an invasion of the cortical area of face representation into that for the hand may occur, and “activation of the expanded face-representing neural map may also reactivate the indigenous limb-representing neurons and thus cause the phantom experience” (Gallagher et al., 1998, p. 59). As thoughtful these reflections are in the struggle to explain the genesis of upper-limb congenital phantoms, as unsatisfactory they must appear in connection with the formation of phantoms of feet and leg that have never ben physically developed. For a tabular list of such cases see Price (in press).

These obviously unsatisfactory attempts to explain congenital phantoms by one general theory may be responsible for the current scientific status of phantoms of congenitally absent limbs: clearly, the phenomenon is not generally accepted as a “scientific fact” (sensu Fleck, 1935/1979). Even the more than 50 cases of congenital phantoms communicated since Valentin (see Price, in press, for an overview) have not convinced the medical community, whose members are “least prone to ask about something that they cannot see, feel, hear, or smell“ (Abramson and Feibel, 1981, p.100). Clearly, a proper phantomology has to go beyond mere clinical observation and base theoretical reflections on experimentation.
Two individuals born without arms: AZ and CL.

AZ is a woman born without forearms and legs (Fig. 1). At the time of the experiments reported below, she was 44 years old. For as long as AZ can remember, she has experienced phantom forearms including hands and fingers. She provided vividness ratings of parts that indicated greater awareness for hands and feet compared to lower arms and lower legs, and also seemed to reflect a tendency toward “right-handedness”. (This lateral bias was also reflected in AZ’s writing behavior, i.e., the consistent holding of a pen with the right side of her mouth). The symmetric bilateral absence of the upper extremities ruled out any genesis of her phantom hands by the representation of a normally developed limb on the contralateral side (Burchard, 1965; Grouios, 1996). Since her conically shaped upper stumps were free of any appendages in the form of rudimentary body parts, we could also reject Simmel’s (1961) proposal different body in terms of a distally displaced kinesthesis. Finally, the fact that AZ reported a distinct awareness of legs and feet, including first and fifth toes remained unexplained by referring to an innate schema for hand-mouth motor interactions (Gallagher et al., 1998). AZ skillfully uses her upper arms to steer her electric wheelchair, grasp objects, typewrite and eat (with the aid of a fork or spoon attached to a ring placed on her right upper stump). AZ’s thighs measure about 10 cm, are free from any rudimental appendages, and X-rays showed dysplasic hip articulations and very short proximal femurs. AZ holds a PhD and is a consultant for sexual problems in handicapped women.

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What is the evidence that AZ’s phantom sensations are not the product of wish-fulfilling fantasies (Sohn, 1914; Skoyles, 1990)? Several habits suggest that this is not the case. For instance, if AZ was asked to fold her arms (a posture she indicated she would take on occasionally), she took on the posture within seconds and answered the question as to which phantom arm was on top of the other without hesitation: it was her left resting on her right. When then asked to fold the arms “the other way around” such as the right would rest on the left, she did so but spontaneously noted “My gosh, I would never do it this way – this feels extremely awkward!” (Brugger and Funk, 2005). Almost everybody has a clear preference for one of these two possible ways of arm folding, one way dominating the other to almost 100%. It appears that AZ has a comparably strong preference, despite any physical experience with folding her arms, but consistent with evidence for a genetic basis of an individual’s preferred pattern of arm folding (McManus and Mascie-Taylor, 1979). More “objective” behavioral evidence for the reality of AZ’s phantoms comes from her performance in several tachistoscopic tasks. In one such task, we showed her line drawings of hands and feet, with fingers and toes pointing either up or down. The drawings were presented for a very short duration on a computer screen, and AZ was required to press a left-sided response key with her left upper stump for pictures of left body parts and a right-sided key for right body parts. She solved this task as accurately as control persons and, importantly, her reaction times were much faster for hands and feet whose fingers and toes, respectively, pointed up than for those presented “upside-down”. This differential reaction time effect was also observed in the control persons and had previously been documented in a large literature on laterality decisions to visually presented body parts (e.g., Sekiyama, 1982). It is interpreted as reflecting an implicit “reaching” movement of the observer, i.e. the matching between the visually presented hand and a representation of one’s own hand. This process is fast as long as the fingers are pointing upwards and one’s own hand can easily match the pictured hand, as if slipping into a glove. However, an imagery rotation of one’s hand is required when the drawing is rotated 180°, a time-consuming mental manipulation associated with longer decision times.

The fact that AZ showed this rotation effect speaks for an intact representation of hands and feet in her parietal cortex, reportedly activated during similar hand laterality decision tasks in subjects born with intact bodies (Bonda et al., 1995). These findings were later replicated and significantly extended by Funk (2001), who showed that AZ’s hand laterality decisions were constrained by the biomechanical limitations of wrist joints, much as is that of normal subjects, and qualitatively different from that of persons born with only one upper extremity but no phantom sensations of the missing limb (Funk and Brugger, 2002). When AZ performed self-paced movements with her phantom fingers while laying in a scanner for functional magnetic resonance imaging, phantom finger movements consistently activated cortical areas similar to those described in comparable studies with amputees (e.g., Ersland et al., 1996), without however, comprising primary sensorimotor cortex (Brugger et al., 2000; Fig. 2).

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So far there is plently of converging evidence for the genuineness of congenital phantoms in the case of AZ. However, even if this evidence could be used to make a case for other peoples’ congenital phantoms, there still remains the pressing question as to why only about 20% of people with limb aplasia experience phantom sensations (Melzack et al., 1997). An important task of phantomology is to try to find out why certain individuals born without a limb phantomize, while others do not. In an attempt to address this questions we have worked with CL, a 41-year-old man born without arms (no shoulder articulation). In daily life, he uses his right foot for writing, eating, pointing, and gesturing. CL has not suffered any visual or cognitive impairments in the course of his thalidomide-related embryopathy. The skillful use of his right foot enabled him to have a successful career as a journalist. Importantly, CL has never experienced any phantom sensations of his missing limbs.

The comparison of CL’s and AZ’s performances in a paradigm known as “apparent motion of body parts (Shiffrar and Freyd, 1990)” revealed intriguing findings. In this paradigm, subjects observe pairs of photographs depicting a human model. The two pictures of a pair differ from one another only in the posture of a single limb, for instance a hand or a lower arm. If the two pictures are repeatedly flashed on the screen in rapid succession (with an interstimulus interval of less than half a second), observers will invariably perceive the limb move along the shortest trajectory of apparent motion, a trajectory which, however, is impossible to execute due to anatomical limitations. With longer interstimulus intervals, observers begin to perceive the trajectories that are biologically possible for a given limb. In other words, what is seen during high flash rates is entirely determined by the visual system; there is no dialog with those regions of the brain that “know” about the specific laws that constrain human limb movements. These laws determine one’s apparent motion percept only when the brain is given enough time to integrate the purely visual with body schema information. In line with this interpretation, neuroimaging data have revealed motor and parietal cortex involvement at slow flash rates, but only visual cortex activation at brief interstimulus intervals (Stevens et al., 2000). It turned out that, while AZ showed the same rate-depending visual perception as did able-bodied observers, CL perceived the short, anatomically impossible limb trajectories irrespective of interstimulus interval. This means that phantom status in people with congenital limb aplasia may interfere with the visual perception of moving human bodies. Specifically, in CL, who has never experienced phantoms, analysis of biological motion seems to be visual-cortex driven, while in AZ there is a dialog between visual and parietal cortex in the interpretation of visually observed upper limb movements (Funk et al., 2005). The results of this experiment are compatible with the notion that some people with limb aplasia could build up a somatic (postural and kinesthetic) limb representation by the habitual visual observation of other people moving their limbs.

The importance of limb movement observation by people with limb aplasia is intriguingly demonstrated in the case report of a woman with a body similar to the one of AZ, i.e. without legs and lower arms (Frank, 1981; 1986). Despite the fact that this woman, Diane, has never experienced phantom sensations, she explicitly equalizes seeing another person’s body move with feeling the movements in her own body (“postural empathy”):

“It’s true that there is a Diane within this Diane who can dance which enabled me to teach my younger sister Debbie, but there’s another reason I could coach her so well. It’s hard to explain. Ever since Deb could walk she was taking care of me. I saw her body move from childhood’s awkwardness to adult gracefulness and strength. But not only did I see this, I felt her movements. In a sense, part of her body (the part I lacked on the exterior) was mine too. So, since I knew how her body moved, I could coach her in dancing.” Frank, 1986, p. 191; Italics in the original)

We are currently exploring the functionality of AZ’s and CL’s “mirror system” (Buccino et al., 2001; Rizzolatti et al., 2001) that is responsible for the matching of visually observed and physically executed limb movements. Should our suspiction that the mirror system contributes fundamentally to the genesis of congenital phantoms be justified, we would expect AZ and CL to differentially activate the relevant brain regions on engaging in an action observation task. Involvement of the mirror system in the process of phantomization was previously suggested (Berlucchi and Aglioti, 1997) and is at least not incompatible with other researchers’ postulate of an innate component of the experience of having a body (e.g., Abramson and Feibel, 1981; Melzack et al., 1997; Weinstein and Sersen, 1961).

2. Supernumerary phantoms

A “supernumerary phantom” is the phenomenal experience of a body part in the absence of its peripheral loss (or congenital absence), but as an entity displaced from the respective physical limb. The condition has also been labeled “pseudo(poly)melia” or simply an illusory “reduplication of body parts” (Weinstein et al., 1954). The phenomenon is most frequently observed after brain damage that leaves an individual paralyzed along one side of the body (i.e., hemiplegia, see also next section). Often a neglect syndrome (i.e., an attentional deficit toward the contralesional hemispace) is present as well, and many patients with supernumerary phantom limbs show signs of denial of their own paralysis (i.e., anosognosia; Babinski, 1914; Ramachandran, 1995; Vuilleumier, 2004). Representative cases are described in Brock and Merwarth (1957), Ehrenwald (1930), Donnet et al. (1997), Halligan, et al. (1993), Vuilleumier et al. (1997b) and Worthington and Beevers (1996). A relevant case was contributed by Sellal et al. (1996), whose patient complained about several supernumerary phantom arms (Fig. 3). Although the etiology of brain damage is commonly a vascular incident or a space-occupying lesion, supernumerary phantoms have also been decribed after traumatic brain injury (Rogers and Franzen, 1992; Weinstein et al., 1954), during the course of a demyelating disease (Mayeux and Benson, 1979) or as an epileptic manifestation (Hécaen and de Ajuriaguerra, 1952; Riddoch, 1941).
Although phenomenologically similar, supernumerary phantoms and phantoms after the loss of a limb differ in important respects. First, pain is frequently associated with the latter but is only exceptionally an attribute of the former (e.g., Canavero et al., 1999; Pinéas, 1932). Second, as “real” as amputation phantoms may feel, they are always recognized as illusory percepts. Reality monitoring is less perfect in the case of supernumerary phantoms after brain damage, the presence of which is often commented on in delusional ways. Thus, patients sometimes refer to the phantom as a “spare limb” (e.g., Grossi et al., 2002; Worthington and Beevers, 1996) or claim that they “grew it for protection” (Weinstein et al., 1954, p. 50). Alternatively, hostile actions as sometimes initiated by an anarchic limb (Marcchetti and della Sala, 1998) have been ascribed to supernumerary phantom limbs (e.g. Hari et al., 1998). Third, amputation phantoms are never seen by mentally healthy amputees, whereas some patients with supernumerary phantoms have reported a visual, in addition to a somesthetic awareness, of their “extra” limb (e.g., Critchley, 1953, pp. 244-245; Halligan and Marshall, 1995; Halligan et al., 1993; Lenz, 1958; Miyazawa et al., 2004; Todd and Dewhurst, 1955, p. 54). This visual component, even if a rare symptom, offers an important agument for the conceptual similarity between phantoms of single limbs and the phantom double that is not only felt but also seen in extracorporeal space (see section four).

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Current theories of supernumerary phantom limbs emphasize the dissociation between an established sensorimotor representation of a limb and a drastically changed pattern of afferent and efferent signals in brain-limb communication together with a distorted representation of space (Vuilleumier et al., 1997b). These authors examined a patient who experienced four legs after extirpation of a right parietal lobe tumor. She was markedly impaired at identifying body parts on a schematic diagram of a human figure. However, this impairment was only evident when the figure was displayed in a frontview (but not in a backview), indicating a failure of the patient to perform perspective transformations of her own body (Parsons, 1987). Such transformations are reportedly mediated by the parietal lobe (Zacks et al., 1999; Blanke et al., 2005). A neuroimaging investigation of supernumerary phantoms was undertaken by McGonigle et al.(2002). In a stroke patient experiencing a left “ghost arm” (originally described in Hari, et al., 1998) that could be deliberately abolished when the patient either looked at or moved the real left arm, these authors showed that the illusion of a supernumerary phantom was accompanied by activation of right hemisphere motor areas, previously implicated in the preparation of motor actions in normal subjects.

As an “as if”-experience supernumerary phantoms are also reported after spinal cord injury. For instance, paraplegic or tetraplegic persons may feel their legs or arms, respectively, “as if they were not paralyzed”. Insight into the illusory character of the phantom percept is, however, always preserved. Here, the spatial location of the phantom is dissociated from the location of the actual limb (as long as vision of the latter is precluded). Valuable case descriptions can be found in Bors (1951), Conomy (1973), Ettlin et al. (1980) and Ohry et al. (1989). For an overview on phantoms in paraplegic patients see Siddall and McClelland (1999), for a neuroimaging approach Alkadhi et al. (2005), who described a high correlation between the vividness of phantom foot movements and the activation volumes of relevant cortical regions during a motor imagery task. Le Chapelain et al. (2001) provoked the phantomization process in paraplegic patients by caloric vestibular stimulation (i.e., immersion of the inner ear with cold water). This procedure activates the vestibular system, whose importance for the experience of the body in space is well-known; already Bonnier (1905) designated the vestibular nerve “the nerve of space”.

Finally, it is important to note that body parts other than limbs (e.g., heads, noses, chins or ears) may be experienced as supernumerary phantoms. Clinical reports are abundant (e.g., Roth, 1944; Weinstein et al., 1954; Ames, 1984), but more intriguing are the findings of “experimental phantomology” on the induction of supernumerary body parts in healthy volunteers (see Jones, 1988, for an overview). Thus, Parker and Schilder (1930) elicited the transitory feeling of a pair of phantom feet while subjects were rapidly decelerated in accelerators, while their subjects felt a phantom head when the accelator was decelerated during an upward movement. Healthy subjects can also be fooled about the position of a limb with the aid of tendon vibration. This principle of “vibratory-myesthetic illusions” was applied by Lackner (1988) to evoke phantom sensations of various body parts. One intriguing demonstration involved the illusory elongation of the lower arm via biceps vibration while subjects were touching their own nose with the fingers. As a result of this conflict – the hand was felt some 30 cm away from the face, yet the sensation of contact with the nose was maintained – subjects reported a phantom nose, up to 30 cm long! Apparently, the brain “filled in” the gap between the perceived hand location and the spatial position of the tip of the nose. This so-called “Pinocchio illusion”, arguably a distortive rather than reduplicative illusion, offers a tool for the investigation of short-term brain plasticity, but may also help understanding individual differences in the susceptibility to experience spontaneous perceptual abberrations regarding the own body (Burrack and Brugger, in press). A rather painful method to induce supernumerary phantom limbs in healthy subjects involves the transient deafferentation of a limb by intravenous regional anaesthesia or pressure-cuff ischemia of one limb (Gross and Melzack, 1978; Melzack and Bromage, 1973). Brasil-Neto et al. (1992) used this method combined with a measurement of the functional reorganization of the corticospinal tract. They found a very rapid adaptation of the nervous system to this experimental “transient amputation” of a limb. Finally, a unique approach to the phenomenon of supernumerary phantom limbs was introduced by the Australian performance artist Stelarc (1995; see also http:/www.stelarc.va.com.au/virtarm /virtarm.htlm). Using virtual reality techniques, he playfully extended his own body by a third arm and provided a phenomenologically important description of how control over and agency for a supernumerary artificial limb may develop. Stelarc’s experimentations are relevant to research on the brain’s assimilation of a prosthesis (e.g., Iriki, Tanaka, and Iwamura, 1996), and support the view that to the brain, prosthetic devices are mere extensions of our bodies, and our real limbs can be conceived of as “natural prostheses” the brain uses to directly interact with the environment.

3. Hemiphantoms

Hemiplegia is a condition in which the entire half of one’s body is paralyzed as a consequence of damage to the contralateral brain hemisphere. As noted in the previous section, a hemiplegic patient does not always recognize this paralysis (“anosognosia”), but may angrily complain about “the other one” with whom she has to share the hospital bed with. Especially in the German and French neurological literature of the first half of the 20th century, this phantom half-body, also called the “hemiplegic twin”, was placed somewhere half-way between the supernumerary phantom limb and the phantom double (to be discussed in section four). The delusional rejection of the ownership of the disabled side of the individual’s own body is commonly the left. This may be because of a prominent role of the right hemisphere in the distinction between oneself and others (Boisson and Luauté, 2004; Paulig et al., 2000). Hemiplegia is not a necessary condition for the experience of one’s hemibody as a phantom. Benedek and von Angyal (1939) described a patient with only a mild hypoesthesia (i.e. an impaired tactile sense) of the left side who nevertheless denied ownership of his left side. He referred to it as “his brother” with whom he felt pity because he appeared to be paralyzed. This tendency to attribute one’s own deficits to other people, whether real or imaginary, was termed “transitivism” by Wernicke (1900). Transitivistic reactions demonstrate that a deficit in one’s own corporeal awareness may be well recognized at an implicit level, without evoking, however, an overt emotional concern about one’s own state of health. In the place of pity for “the other”, anger may rather be expressed, if, for instance, patients complain about having to eat and breath for themselves as well as for the one laying beneath (Ley and Stauder, 1950; Mikorey, 1952; von Stockert, 1944). Such “residual identification” with the part of the body that is claimed to be someone else is also evident in the patients’ frequent emphasis that the illusory person looks similar to themselves, is a family member, carries a similar name, or has the same occupation.

We have recently seen a 57-years old right-handed woman who had suffered a cerebral hemorrhage with a consecutive left-sided sensorimotor hemisyndrome (unpublished observation). She was not completely anosognosic, as she recognized that “something was wrong with the left arm” (which was completely paralyzed) and that she was in hospital “to fix the problem”. Under conditions of normal illumination she had no delusional ideas regarding her left hemibody, but she neglected the entire left side of body and space. In darkness, however, she always felt the presence of her sister to her left side (Fig. 4). During the first three nights, this presence was welcome to the patient because she felt less alone. From the forth night on, however, this changed. The patient later reported that she first kindly asked her sister to move further away because there was not enough space in the bed for the two of them. As her sister would not comply with this wish, the patient got angry and finally bit her sister’s right arm. In actuality she repeatedly bit her own left arm, and the bite marks there prompted the nurse to inquire the next morning. An interview with the patient some 10 days after this incident revealed a still labile insight into the illusory nature of the sister’s presence: when the patient was asked what might have happened that night she pointed to her fronthead, indicating that the fantasy about the sister was probably a matter of her neurological condition. However, when it was pointed out to the patient only a minute later, that the bite marks on her upper arm could no longer be found, she was annoyed and impatiently noted: “I told you several times: I bit my sister, not myself!

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An intriguing experiment about boosting a patient’s tactile sensitivity on the paralyzed side by the announcement that touch will be applied to “the other one”, was communicated by Bottini et al. (2002). The authors stimulated the hands of a blindfolded stroke patient with anosognosia who identified her left-sided hemiphantom as Tiziana, her niece. Each touch stimulus was announced as being applied to (1) the patient’s right hand, (2) the patient’s left hand or (3) the niece’s hand. Right hand stimuli were recognized 100% correctly, left hand stimuli with 0% accuracy as long as attention was directed to the paralyzed hand, but 80% correctly after directing the patient’s attention to a delusion-compatible representation of the same body part. This finding shows that top-down expectations may modulate tactile sensitivity in a hypoesthesic region of the body. At the same time, it elegantly proves that spared tactile sensitivity in a body part does not necessarily lead to a sense of ownership for this particular part.

4. The phantom double: “autoscopic phenomena”

The term “autoscopic phenomena” designates the illusory reduplication of one’s own body (Brugger et al., 1997). Four different types have to be differentiated: (1) the feeling of a presence, (2) the autoscopic hallucination, (3) heautoscopy and (4) the out-of-body experience (OBE). We discuss these different types below. For two more types of autoscopic phenomena, i.e. negative and internal heautoscopy, we must refer the reader to the older literature, as more recent reports are rare (e.g., Sollier, 1903; Comar, 1901; Magrí and Mocchetti, 1967). We only point out here that both negative and internal heautoscopy have their correspondences on the level of single limbs (e.g., Bonnier, 1905; Dorpat, 1971).

The somesthetic phantom double

The phantom double which is only felt, but not seen, is the autoscopic phenomenon most similar to the phantom limb (which is also only represented in the somesthetic modaility). As a phantom limb, also the “felt” being can be localized very precisely in near extrapersonal space. The phenomenon is commonly labelled “feeling of a presence” (Brugger et al., 1996), but is also known as “Anwesenheit” (Thompson, 1982), “concrete awareness” (“leibhafte Bewusstheit”, Jaspers, 1913) and “false proximate awareness” (Koehler and Sauer, 1984). Grüsser and Landis (1991) labeled it a “somesthetic doppelgänger”. In a neurological context, the phenomenon is common in association with migraine (Lippman, 1953; Podoll and Robinson, 2001) and epilepsy (Ardila and Gomez, 1988; Critchley, 1955). An elderly patient of Critchley’s (1953, p. 242) with bilateral cortical atrophy reported that

“….she would wake in the night with the very intense feeling that somebody was in the room – a person she knew; indeed, with whom she was very familiar. Sometimes, she was at a loss to decide who this could be, but on many occasions, it would dawn on her that this person was none other than herself.”

Although identification with one’s own body or self is rarely reported as explicitly as in this case, several phenomenological features justify the conceptualization of the “felt presence” as an extension of one’s own corporeal awareness into extracorporeal space. For instance, there is commonly a synchrony of movements such that the invisible being walks along with the patient and often imitates arm and leg movements (Brugger et al., 1996). Also, as in cases of hemiphantoms, a transitivistic function of felt presences is sometimes obvious. Thus, exhausted mountaineers frequently overcome hopeless situations by caring for “the other” who climbs with them, and whose presence is felt compellingly enough to be offered food (e.g., Smythe, 1934). These observations suggest that the feeling of a presence rests on postural and kinesthetic representations of one’s own body that are falsely localized in extrapersonal space. Ownership over these non-visual components of corporeal awareness does not need to be acknowledged, not even by those persons who explicitly note distinct changes in bodily awareness during the experience (such as sensorimotor weaknesses or feelings of depersonalization; Brugger et al., 1999). As a literary motif, we find the invisible phantom double described in the works of Guy de Maupassant (Le Horla – literally “the one out there”), James Hogg (The Jolly Corner), August Strindberg (Inferno) and Patricia Highsmith (The Talented Mr, Ripley).

The visual phantom double

In contrast to the feeling of a presence, autoscopic hallucinations lack any somesthetic component. Originally labelled “mirror hallucinations” (hallucinations spéculaires, Féré, 1891; Nouet, 1923) they involve the seeing of one’s own body or only one’s face as if reflected in a mirror. Unfortunately, most modern reviews of autoscopic phenomena (e.g., Dening and Berrios, 1994; Devinsky et al., 1989; Leischner, 1961) intermingle autoscopic hallucinations and multimodal phantom body experiences. Yet, in the French neurologic literature of the turn of the 19th century, the unimodal visual character of autoscopic hallucinations was clearly recognized (Sollier, 1903). Correspondingly, autoscopic hallucinations, such as the appearance of one’s face or body against a background, are most frequently seen after visual cortex damage, sometimes with simultaneous impaiment of the temporal lobes (Maximov, 1973). Involvement of the “extrastriate body area” (Downing et al., 2001) in the lateral occipitotemporal cortex seems likely. If the image of oneself is lateralized, it is usually to the left visual field (Brugger et al., 1997), reflecting, perhaps, the dominance of the right hemisphere in the recognition of one’s own face (e.g., Kircher et al., 2001; Keenan et al., 1999 for review). Consistent with the absence of aspects of corporeal awareness other than visual representations, the point in phenomenal space on which the observer’s perspective rests is always body-centered, i.e. the patient describes the hallucination as observed from a regular within-body perspective (Brugger et al., 1997; Blanke et al, 2004). Most importantly, however, the purely visual phantom double is a mirror image of the own body, as reported by a large number of patients (e.g., Flournoy, 1901; Lukianowicz, 1958, case A) and illustrated in the drawing provided by Zamboni et al. (2005; Fig. 5).

brugger_5

The visual-somesthetic phantom double

In heautoscopy, the somesthetic and visual modalities are about equally involved. The term means literally “seeing one’s self” and thus implies the existence of two selves, one that observes, and one that is observed. Unlike in autoscopic hallucinations, visual aspects of bodily reduplication do not predominate. On the contrary, one’s double is typically described as a pale, foggy, ghost-like and transparent figure. More important are feelings of psychological affinity toward one’s second self. As in the feeling of a presence, one’s phantom double is experienced as a space-occupying entity, which is, however, always recognized as “another me”, even if the mere visual features do not match one’s own (“dissimilar heautoscopy”, Sollier, 1903; Grotstein, 1983; “heterosexual heautoscopy”, Carp, 1952; Letailleur et al., 1958). Increasing ownership over the one encountered in extrapersonal space, i.e. the double, is paralleled by increasing feelings of depersonalization and a sense of “hollowness” of or detachment from one’s real body. In many instances, patients are at a loss to decide where in space to localize the “real me”, within the boundaries of the physical body or rather in the phantom body, that is often lateralized to one hemispace (Figure 6).

brugger_6

Heautoscopy has been reported in a variety of neuropsychiatric diseases Menninger-Lerchenthal, 1935; 1946; Grüsser and Landis, 1991). If there is a focal brain lesion, it often comprises one or both parietal lobes. In cases of extensive brain damage, the autonomy of the double is highly developed, such that complex psychological interactions between a patient and her double can occur. The double may either play a comforting role (transitivism) or engange in self-distructive behaviors (Table 1). The latter may manifest itself in a surprising variety of forms. “Heautoscopic suicide” may be self-protective as long as the double is the target of aggressive impulses. It is self-destructive, however, once the double forces the self to commit suicide or stimulates self-mutilation. These forms of heautoscopy have always fascinated belletristic authors. In fact, the motif of the double has produced a huge amount of publications in literary psychology. Both consoling and antagonistic tendencies have been elaborated on in literary accounts (Keppler, 1972 for an overview).

(1) positiv emotional interactions: phantom double reference(s):
…offers company Lukianowicz, 1958
…plays comforting role Wigan, 1884
double helps to overcome the loss of a beloved person Lukianowicz, 1958
(case A); Wells, 1983
double reassures patient that his condition (brain tumor)
is not life-threatening
Brugger et al.
…recommends seeking advice:
hanged double makes patient recognize seriousness of
depressive condition and seek a doctor’s help
Arenz, 2002
…takes symptoms from real self (“heautoscopic transitivism”):
seizure patient watches her double’s epileptic fit
Sengoku et al., 1981
double displays obsessive compulsive symptoms that
patient previously displayed
Müller-Erzbach, 1951
double, not patient, is dying from typhoid fever Hécaen and Green,
1957 (case 5)
double’s suicide attempt is observed by suicidal patient Ostow, 1960 (case A)
Maack and Mullen, 1983
(2) negative emotional interactions: phantom double reference(s):
…is experienced as attacking self physically
self-cutting of tongue is ascribed to the double
Bakker & Murphy, 1964
two patients experience being strangled or beaten up,
respectively, by their double
Siegel, 1992
gives advice to commit suicide:
double lures self into river
Damas Mora et al., 1980
double recommends self-strangling Ostow, 1960 (case B)
double causes patient to jump out of a window Brugger et al., 1994
…is target of self-destructive impulses:
two schizophrenic patients mutilate themselves in an attempt to kill their double
Carp, 1952

Table1: Examples of complex psychological interactions between self and phantom double

We note that antagonistic behaviors have also been reported for single limbs (Marchetti and Della Sala, 1998) or other phantom body parts (Ames, 1984) as well as during hemiphantom experiences (see section 3; Fig. 4). Moreover, as with single body parts, also one’s entire phantom body may be multiplied rather than merely duplicated. Hence, analogous to the multiple supernumerary phantoms mentioned in section 2 is “polyopic heautoscopy”, in which more than one phantom double is seen and felt (Brugger et al., in press, for a case report and review of 14 published cases).

The out-of-body experience

The transition between heautoscopy (seeing one’s phantom double) and an OBE (being one’s phantom double) is blurred. The defining feature of an OBE is the illusory perception of one’s own body from outside. The term “double” is rarely used in a person’s description of an OBE. What is the most characteristic feature is the apparent separation from one’s body, whether this is actually visualized or just known to be at a certain point in space. A proposed mechanism common to both types of autoscopic reduplication is the deficient integration (1) of proprioceptive, tactile and visual aspects of corporeal awareness, and (2) of information pertaining to personal and extrapersonal space (Blanke et al., 2002; 2004). Implication of the temporo-parietal junction, reportedly mediating these integrative functions, is in fact suggested in a large number of clinical case reports of OBEs (Menninger-Lerchenthal, 1946; Blanke et al., 2004). Transcranial magnetic stimulation over this brain site also disrupts shifts between own-body and others’-body perspectives in healthy volunteers (Blanke et al., 2005). In neurologically and psychiatrically healthy subjects OBEs are also reported. A serious pathology does not need to be assumed in the face of a history of occasional OBEs. Frequent OBEs, however, have been documented as precursors of serious neurological disorders (Vuilleumier et al., 1997a; Zurfluh, 1983). An OBE may occur when an individual is convinced that the own death is imminent. Other phenomena pertaining to a proper “near-death experience” may be reported (Noyes and Kletti, 1976). Alternatively, the illusory separation from the physical body is an isolated feature, typically accompanied by a psychological detachment. We see here a profoundly transitivistic function of the OBE: “it is not myself who will die, but this poor creature out there!” (see e.g. Brugger, 2002; Brugger et al., in press; Menz, 1984).

5. Synopsis: investigating the body in the brain

As pointed out by neurologically oriented authors (Berlucchi and Aglioti, 1997) as well as by those emphasizing aspects of the philosophy of self (Gallagher, 2000), the empirical study of the “body in the brain” requires integration of a wide variety of findings from developmental psychology, neurology and psychiatry. We propose that this multidisciplinary approach is best labeled “phantomology”, a term coined by Stanislaw Lem (1964/1981). In his “Summa technologiae”, Lem provided a visionary anticipation of what we nowadays label “virtual reality”. Emphasizing the virtual reality of having a body, he discussed issues like telepresence (“teletaxis”), immersion and even cybersex long before the technical realization of these modes of experience had been achieved. With respect to our inclination to equalize our self with our body, Lem distinguished between the self that is determined by somatosensation and the self defined by motor action. With this distinction he again anticipated an important modern development, i.e. the conceptualization of self-awareness as comprising afferent and efferent components (Tsakiris and Haggard, 2005). Both these components are already present in the phantom limb phenomenon, which has generated a vast body of research. In contrast, experimentation of whole-body phantoms has either faded into oblivion (e.g., Stratton, 1899) or is just about to be developed. The huge though widely scattered literature on autoscopic phenomena is still dominated by clinical observation.

Among the prerequisits of a proper phantomology are thus:

  • the recognition that phantom limb and phantom body form a conceptual unity;
  • the consideration that “congenital phantoms” are a scientific fact and that they may be codetermined by the visual observation of a conspecific’s limbs;
  • the development of experimental procedures to induce and manipulate phantom experiences on the whole-body level (heautoscopy, out-of-body experiences)
  • the acknowledgment of mechanisms like denial and transitivism that defy an explanation in purely neurological terms, but may nevertheless be important determinants of phantomization processes that target the entire body.


Figure Legends:
Fig. 1. Subject AZ was born without lower arms and legs. The shaded areas represented phantom limbs with different vividness ratings for different phantom body parts (scale from 0 = no awareness to 6 = most vivid awareness).
Reproduced, with permission, from Brugger et al., Proceedings of the National Academy of Science of the USA, 97, 2000.

Fig. 2. Cortical activation areas during finger-to-thumb oppositions with the left (top) and right (bottom) phantom hand as compared to a rest condition (see right side for conventional Talairach coordinates and BA = Brodman areas, respectively). Arrows indicate the anatomical region corresponding to the hand representation in able-bodied subjects. They remained silent during phantom finger movements.
PM = premotor
Reproduced, with permission, from Brugger et al., Proceedings of the National Academy of Science of the USA, 97, 2000.

Fig. 3. Selection of drawings of a manekin shown to a 77-year old man, who claimed to have a varying number of left arms after a large right hemisphere infarction. His responses to two questions are indicated on top and underneath the respective drawing. Response in B (to the first question, on top) may indicate some transitivistic tendency (i.e. seeing the own defect on others). The acknowledgment of the drawing in C as a regular body may be due to the fact that the patient neglected the information on the left side of any picture.
Modified after Sellal et al., Revue Neurologique, 152, 1996.

Fig. 4. A patient’s drawing of her hemiphantom, whom she felt laying along her left, paralyzed side and whom she identified as her sister. The large middle figure was drawn by the examiner, the patient added her sister’s head and spontaneously wrote the names of both herself and her sister on top of the respective figures. As illustrated here, the sister was initially experienced as chearful, and her company was welcome. Lateron, her presence was rather considered a nuisance; the patient bit her sister, but in actuality, she bate her own left anesthetic arm.

Fig. 5. In an autoscopic hallucination a person sees her own visual features as reflected in a mirror. There is one unitary self whose observer perspective is body-centered.
Reproduced, with permission, from Zamboni et al., Neurocase, 11, 2005.

Fig. 6. Heautoscopy is more than “seeing oneself”. Body and self appear duplicated, and confusion may exist as to which body contains the real self.
Collage courtesy of Peter Schell, Berlin.

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Peter Brugger, born 1957 in Zurich, Switzerland. Acquired first a teacher's Diploma for Elementary and High School levels, then studied biology at Zurich University. Dissertation on Subjective Randomness: Implications for Neuropsychology and Parapsychology. Postdoctoral training at University California, San Diego and University of Victoria (Canada). Currently head of Neuropsychology Unit of University Hospital Zurich. Main research interests: neurology of paranormal beliefs; representation of body and space (Pfizer Prize for Medical Research 2001 for work on phantoms of congenitally missing limbs). http://www.neurozh.ch/e/groups/brugger00.htm http://www.psy.mpg.de/body/Default.htm