Consciousness and Body Image: Lessons From Phantom

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Consciousness and Body Image: Lessons from Phantom Limbs, Capgras Syndrome

and Pain Asymbolia

V. S. Ramachandran

Philosophical Transactions: Biological Sciences, Vol. 353, No. 1377, The Conscious Brain:Abnormal and Normal. (Nov. 29, 1998), pp. 1851-1859.

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THE ROYALQg!SOCIETY

Consciousness and body image: lessons fromphantom limbs, Capgras syndrome and painasymboliaV. S. RamachandranCenter fir Brnzn and Cognztron, Unruertrly of Cn lfo rnzn , San Ilrego, LaJo lla, CA492093-0109, 1JSA ([email protected])

IVords such as 'consciousncss' an d 'sclf' actually encompass a number of' distinct phenomena that arclooscly lumped togcthcr. Thc study of ncurological syndromes allows us to explore tktc neural mechanismsthat might undcrlic dif fcrcn~ spects of sclf, such as body image and emotional responses to sensorystimuli, and perhaps cvcn laughter and humour. Mapping thc 'functional logic' of' thc many differentattributes of human nature on to specific neural circuits in the brain ofrcrs thc best hope of undcrstandinghow thc activity of' neurons givcs rise to conscious cxpcricncc. WC considcr three neurological syndromcs(phan tom limbs, Capgras delusion and pain asymbolia) to illustratc this idca .Keywords: phantom limb; plasticity; body image; somatosensory cortex

received the least at tention. Consider questions such as: 1, INTRODUCTION why do wc laugh? Why do we cry? Why do wc dance? You ncvcr idcntifii yourself' with the shadow cast by O r why do wc apprcciatc art and music.' And thc big your body, or wkh its reflection, or with the bodyyou scc in a dream or in your imagination. 'There-fbrc you should not identify yourself with this livingbody, either.Shankara (788 820 AD) Vweka Chudamani

(Vedic scriptures)In the first half of thc ncxL ccntury, scicncc will confrontits grcatcst challcngc in trying to answer a question thathas been steeped in mysticism and metaphysics formillennia: what is thc nature of'thc sclf'?

Unfortunately, thc word 'sclf'' is like thc word 'happi-ness'; we all know what it is and that it is real, but it isvery hard to dcfinc it or cvcn to pinpoint its charactcris-tics. Like quicksilvcr, thc more you try to grasp it thcmore it tcnds to slip away. When you think of the word'sclf', what pops into your m i n d Whcn T think about'myself: it seems to be something that unites a ll mydiverse sensory impressions and memories together(unity), clairlls to bc 'in charge' of' my lif'c and makcschoices (fk-cc will), and scems to endure as a single entityin space and time inhabiting a single body ('bodyimage '). Tt also sees itself as cmbeddcd in a social context,balancing its chcckbook and might even plan its ownfilneral arrangements. Actually we can make a list of' allthe characteristics of the 'sclf' just as you can for happi-ness-and then look fbr brain structures that arc involvedin each of these aspects. And this, in turn, will one dayenable us to develop a clearer unders tanding of self' andconsciousncss, although I doubt whether there will 1)c asingle, grand, climactic solution in thc same way thatDNA is thc solution to thc riddle of hcrcdity.

It has always seemed very pu~nlingo mc hat thc mostinteresting aspects of' human conscious cxpcriclncc haveI'lzil. '/i(ins.K . SOC.Lond. 11 (1998) 353, 1851 1859

question: what is consciousness? Evcryonc finds thcscquestions fascinating and yct they arc largely ignored bymainstream neurology and cxpcrimcntal psychology.

Thc main concern of'this article will be the question of'how thc self constructs a body image and what wc canlcarn about this process by studying patients withphantom limbs. Thc second half' of thc article is muchmore spcculativc and dcals with two poorly understoodsyndromes: Capgras syndrome and pain asymbolia. Allthree syndromes have been known sincc thc cnd of thcninctccnth ccntury but thcrc has, on the whole, been atcndcncy to regard them as clinical curiosities. In thisarticle T shall show that, fir fiom bcing mcrc oddities,thcsc disordcrs can give us valuable insights into thcfunctional organization of the normal human brain.

2. PHANTOM LIMBS, BODY IMAGE AND NEURALPLASTICITYT shall dcscribc a number of experiments that wc have

conductcd on both normal pcoplc and amputees. 'l'hcscexperiments dcmonstratc that thcre is a tremendousamount of latent plasticity even in thc adult human brainand that onc's body image is surprisingly mallcablc ; rnorcso than anyone would have imagined.

Phantom limbs have probably bccn known sinceantiquity; not surprisingly, there is an clahoratc fblklorcsurrounding thcm. Af'tcr Lord Nelson lost his right armduring an unsucccssf'ul attack on Santa C r u ~c Tcnerif'c,hc cxpcricnccd compelling phantom limb pains,including the sensation of' fingers digging into hisphantom palm. The emcrgcncc of' thcsc ghostly sensa-tions lcd thc Sca Lord to proclaim that his phantom wasa 'direct proof of the cxistence of' thc soul' (Riddoch

1851 O I998 T h e Royai Socicty


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1852 \/: S.Ramachandran Chntczoutnprr a nd body rma


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Cone-ciousness and b o d y image \! S. Kamacliandran 1853

Fignre 3. The Penfield 'homunculus'. Notice that the hand area is bordercd below by the face, and abovc by thr uppcr arm andshoulder- the two regions whrre rcSerence liclds are usually Sound in arm amputees.

modality-specific. For examplc, hot, cold, rubbing,vibration, metal, or massagc on thc Sacc wcrc Sclt as hot,cold, vibration, rubbing, metal and massage at preciselylocalized points in the phantom. 'Touching other bodyparts (e.g. torso, lcgs, chcst) usually did not cvokcsensations in the phantom, but there was often a secondtopographically organized map proximal to the amputa-tion stump. Because the hand area in the Penfield map(figure 3) is flanked on one side by the upper arm and theother side by the face, this is precisely the arran gement ofpoints that one would expect if the aff'erents from theupper arm skin and face skin were to invade the handterritory from each side.

The fact that stimulating certain 'trigger points'(Cronholm 1951) can elicit referred sensation in thephantom has been noted previously in the older clinicalliterature, but the occurrence of a topographicallyorganized map on the Face and modality-specific referralfrom face to phantom was not described. Conserjuently,no attempt was made to relate these findings to somato-topic brain maps, and the referred sensations were oftenattributed either to stump neuromas or to activation of a'diffuse neural matrix' (Melzack 1992). Our own resultssuggest, instead, that referred sensations emerge as adirect consecjuence of the changes in topography afterdeafferentation, an idea that we refer to as 'the remappinghypothesis' (Ramachandran 1993).

Based on the remapping hypothesis, we also predicted(Ra mac han dra n 1993) that after trigeminal nervesection, one should observe a map of the face on theJ'lzil. ' f iax s . K . ,%c. Land. B (1998)

hand, and this has recently bcen shown in an clcgantstudy by Clarkc et al. (1996). Also, aftcr amputat ion oS thcindex fingcr in onc patient a map of thc index lingcr wasfound neatly d raped across the ipsilateral chcck (Aglioti etal. 1994a; Aglioti & Rerluchi 1998). Finally, our suggestionthat these effects are based partly on the unmasking ofpre-existing connections, rather than sprouting, receivessupport from our recent observation that modality-specific referral from the face to the phantom can occureven a few hours after amputatio n (Borsook et al . 1997).

'These findings provide strong support for the remap-ping hypothesis. They might allow us to track thc time-course of perceptual changes in humans and relate thesein a systematic way to anatomy. The occurrence of topo-graphy and modality specificity rules out any possibilityof the referral being due to non-specific arousal.(b )Reflecting on phantom lim bs: synaesthesia

Some patients claim that they can experience vividvoluntary movements (Melzack 1992) in their phantomlimb, presumably because reafference signals from motorcommands sent to the phantom a re monitored in th e cere-bellum and parietal lobes. However, with the passage oftime the phantom becomes 'frozen' or 'paralysed', perhapsbecause of a continuous absence of visual and propriocep-tive confirmation that the commands have been obeyed.Some patients experience excruciatingly painful involun-tary clenching spasms in the phantom; they experiencetheir nails digging into the phantom palm a nd ar e unableto open the hand voluntarily to relieve the pain .


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1854 1: S. Ramachandran C:onsciozcs~7rs,ra n d 110ciy i ~ na~ge

Uk placed a vertical sagittal mirror on the table infront of the patient. If the patient's paralysecl phantomwas, say, on the left side of the mirror, he placed his righthand in an csact mirror-symmetrical location on theright side of the mirror. If he looked into the shiny rightside of the mirror, the reflection of his own hand wasoptically superimposed on the felt location of hisphantom, so that h' had the distinct visual illusion thatthe phantom had been resurrected. IS he now mademirror-symmetric movements while looking in themirror, he receivccl visual feedback that the phantom wasobeying his commancl.

Remarkably, six out of ten patients using this procedureclainled that they could now actually feel not mcrelysee- mo \T em en ts merging in the phantom limb. This wasoften a source o i considerable surprise and clelight to thepatient (Ramachandran& Rogers-Ramachandran 1996).

Indeed, four patients were able to use the visual feed-back provided to them by the mirror to 'unclench' a pain-fully clenched phantom hand. This seemed to relieve theclenching spasm as well as associated cramping pain (theburning and lacerating pains in the phantom remainedunaffected by the mirror procedurc, suggesting that therelief of the clenching was probably not confahulatory inorigin). The elimination of the spasm was a robust effectthat was confirmed on several patients. The elimination ofthc associated pain was also pointed out by them butrequires confirmation with double-blind controls, A 'iventhe notorious susceptibilit-y o i pain to placebo and sugges-tion. In one case, repeatcad usc with the mirror for tenminutes a day for three weeks resulted in a permanent andcomplete disappearance of the phantoin arm and elbow(and a 'telescoping' of fingers into the stump) for the firsttime in ten years. 'The associated pain in the elbow arid~ ' r i s talso variislled. This might bc the first known iristailceo i a successful amputation of a phantoin limb.( c ) Emergence of 'repressed me mo rie sJ n phantom

limbsAnother Sascinating but poorly understood aspect of

phantom limbs concerns not orily the continued existrncro i 'mcmorirs' in thc phantom-of sensatioris that existedin the arm just before the amputation-but also the re-rmergerice oi' long-lost mcmorirs pertaining to that arm.For instance, it is well liilown that patients sometimescoiltiiluc to kc1 a wcddirig ring or a watch band on thephantom. Also, in the first fcm: weeks after armamputation many patic:nts report that they experienceexcruciating clenching spasms in the phantom hand andthat these spasins are oiten accompailied by thcunmistakable sellsation of nails digging into the palm. Itusually takes several minutrs--or sometimes evenhours-to voluntarily uilclench the phantom (unless thesubject uses our mirror device!) but when uriclenchil~geventually does take place, the 'nails digging' sensationvanishes as \%jell.The reason for this is obscure, but onepossibility is that when motor coinil~ands rc sent koni thcpremotor and motor cortex to clench the hand, they arerlormally damped by error feedback from proprioception.I i the l imb is missing, however, such damping is notpossible, so that the motor output is amplified evenfurther, and this overflow or 'sense o ieffort' itself might beexperienced as pain. But why would the 'nails digging'

sensation also be associated with the spasm? This is evenmore dificult to explain, hut one might suppose that themotor commands io unclench the hand and the sensationof the nails digging are linkcd in the brain, even in normalindividuals, by a Hehbian learning mechanism. Further-more, because thc motor output is now amplified, it isconceivable that thc associated memory of nails digging isalso correspondingly atnplificd, giving rise to the cxcru-ciating pain. Thc observation that eliminating the spasms(e.g. with intense, prolonged voluntary effort) alsoabolishts the digging sensation is consistent wit11 this view.What we are dealing with here, then, might be a primitiveform of sensory learning that could conceivably provide anew w7 i y of experimentally approaching more complexforms of memory and learning in the adult brain.

The reactivation of pre-amputation memories in thephantom has been noted before (Katz & Mclzack 1990)hut very little systeinatic work has bcen done on it, andthe significance of the findings for understanding normalmemory seems to have gone largely unrecognized. Forexample, one of our patients reported that before amputa -tion the arthr itic joint pains in her fingers would oftenflarc up when the weather was damp and cold. Remark-ably, whenever thc air became humid the same painswould recur in her phantom fingers. Also, when her handwent into a clenching spasm in the evening, the tllllrrlbwas usually abducted and hyper-extended ('sticking out')but on those occasions when it was llexed into the palm,the spasm was accompanied by the distinct feeling of herthumbnail digging into the fifth digit's pad. 'The curiousimplication of this observation is that even fleetingsensory associatioris may he prrmailently recorded in thebrain; these memory traces might be ordinarily

but inight becon~ c nmasked by the deafferen-tation. ((Also,surprisingly, the traces might be 'gated' bythe felt position of the phantom thumb or even hcretrieved on the basis of an unconscious inference: 'if mythumb is flexed it must touch my fifth digit.')(d) Resurrec tion of long-lost phantoms

We havr also trird the mirror procedurr on digit(finger) amputees with very sinlilar ~ s u l t s .Orir paticnthad his indrx finger aniputatrd 1 cm distal to the head ofthe metacarpal about 40 ymrs before we saw him. Iichad experienced a vivid phantom finger (but no pliaritoinpain) for about a yrar, but it faded completely aficr that.Remarkably, ~she ri e s iw his index finger move in themirror, lle started experiencing proprioceptive sensationsin his index Gngrr {or the Grst time in 39years! Heseemed very intrigued and delighted by all this.(e) Phantoms induced in n ormal indiuiduals

'Thr question of how the brain constructs a 'bodyimage' has been a topic oS considrrable interest to nruro-logists (Head 1918; Brairi 1941; Critchley 1953),psychologists (Schildcr 1950), and even philosophers(Merleau-Ponty 1967; Dennett 1978; O'Shaughnessy1980). Even though this image is constructed fromevanescent and fragmentary evicicncc derived fi-ommultiple sensory systems such as vision, proprioceptionand hearing, we have a stable internal mental construct ofa unitary corporeal scl i that endures in space and time, atleast until its eventual annihilation in death.


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Con ,czou mess an d body irr~o~qeV. S. Ramacliandra~~1855

One key difference between tactile sensatioiis and visualsensations is that the lormer are localized directly on thesensory surfjce where the receptors are actually located,whereas the latter are 'projected' onto the external world;ibr example, when light from a tree hits your retinal recep-tors you localize the tree externally, riot inside youreyeball. Il~deed, vision probably evolved as a 'remotesensing' device that liberates you Gom the requirement ofdirect contact with the object you are trying to localize,whether li)r dodging or for grabbing (Dawkins 1996).

With so ancient a phylogenetic rifi between the twosystems, it would be very surprising if one could 'project'somatic sensations onto the external world, yet anyone whohas used a screwdriver or a raxor and a mirror will realizethat this must be possible, at least to a limited extent. Afterextended use of the screwdriver one often begins to 'feel'the tip of the screwdriver. Similarly, when using a shavingmirror one experiences a pecul iar mental diplopia- -theraxor is felt simultaneously on one's own face but to alimited extent also on one's dop,beLgin


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I856 V. S. Kamachandran Consciom.cne.rcand body image

cannot be based exclusively on an endless hierarchy oflabelled lines and maps. At somc stagc,'pattcrn coding,' i.c.the total spatio-temporal pattern of activity must take overand determine what the subject actually perceives.

The basic presumption of the remapping hypothesis ofreferred scrlsations is that the labelled lines have beer1switched so that the same sensory input now activates anovel set of labelled lines (e.g. the face input activates'hand neurons' in Sl). As we have seen, this is consistentwith both the MEG changcs in sensory rnaps that weobserved as well as with the referred sensations reportedby many patients (see also I


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problem with experiencing enlotions in general. Duringthe interview he experienced joy, fear, impatience,boredorn, and all other emotions th at one would normallyexpect a human being to experience, because his limbicsystem was unaffected. What was deranged is the commu-nication between vision and ernotioii. (Consistent withthis, D.S. iicvcr experienced this delusion when talking topatierits o n th e telephone.)

Oiie objectioii to our interpretation might be thatpatients with bilateral lesiorls of the amygdala do riotsuddeiily develop Capgras syndrome. The reason mighthe that with the entire amygdala damaged, the patient'sbrain has no baseline for comparison: no stimulus evokesa GSR. 7'0 develop the Capgras dclusioii you may need aloss of GSR to certain categories of sensory irnages butnot to others. Consistent with this, our patient D.S.showed a nornlal GSR to threat gestures and loud noises,suggesting that his arnygdala was probably intact.

Patient D.S.'s tendency to duplicatc his parents issurprising enough, hut even rnore remarkably he wouldsornetimes duplicatc himself! O n one occasiorl whenshown an old photograph of himself he said it was 'adifferent person . . . see, he has a moustache and I don't'.O r sometimes, during conversation, he would refer to 'theother David' (he once accused his employer of sendingthe cheque to the other David). Philosophers oftenremirid us that if there is any one aspect of existence thatis completely beyond question, it is the fact that 'I exist'as a single conscious individual. But it seems that eventhis axiomatic foundatioii of one's existence is called intoquestion hy David.

I mention Capgras syndrome because it is a strikingexample of how a completely bizarre, seemingly incom-prehensible psychiatric syndrome can be at least partlyunderstood in terms of the known neuroanatomy of thetemporal lobes. This idea can then he tested using a rela-tively simple technique, GSR, to show that something likethis might in fact be going on in the brain.

4. NEUROLOGY OF LAUGHTER AND HUMOURLaughter and hurnour arc surely just as important a part

of our corlscious experience as any other trait. A Martianethologist visiting our planet would be very puxzled hy thefact that every now and then groups of humans produce anexplosive fit of rhythmic sounds, in certain social situations.\Vhy do people do this? Can studying neurologicalsyndrorncs help to answer this question?

A 'disconnection' syndronle that is just as fascinating asCapgras syndrome is a disorder called 'pain asynlbolia',in which a patient with damage to the insular cortex willsay he can feel the pain of a pinprick hut that 'it no longerhurts'. I was amazed to notice recently that a patientwhom I receiitly saw in India with this disorder riot onlyfailed to experience the aversive quality of the pain hutalso started laughing in response to a pin-prick! So hereagain is a mystery: why would an intelligent, sane humanbeing begin to giggle when pokcd with a needle? Is thisnot the ultimate irony: laughter in responsc to pain? Carlthis syrldrome help us to investigate the evolutiorlaryorigins of laughter and humour?

Cultural factors undoubtedly influence humour aridwhat people find funny--the Erlglish are said to have a

Consriousne.rs and body ir na g~ V. S. Kamachandran 1857

sophisticated 'sense of humour', whereas the Gerrnansand the Swiss rarely find anything amusing.'But even ifthis is true, rnight there still be sorne sort of 'deep struc-ture' urlderlying all hurnour? The details of the phenom-enon vary from culture to culture and are influenced hythe way you were raised, but this docs not rncaii thatthere is no genetically specified mechaiiisrn for laughter, acornrnon dcnorninator uiiderlyiiig all types of hunlour.Indeed, rnany people have suggested that such amechanism does exist and theories on the biologicalorigins of hurnour and laughter have a long history, goingall the way to Schopenhauer and Kant, two singularlyhurnourless German philosophers.

Why a re jokes funny? Despite all their surface divcr-sity, most jokes and funny incidents have the followinglogical structure. Typically you lead the listener along agarden path of expectation, slowly building up tension. Atthe very end, you introduce an unexpected twist thatentails a cornpletc reinterpretation of all the precedirlgresults; moreover, it is critical that the new interpretation,though wholly unexpected, makes as rnuch 'sense' of theentire set of facts as did the origirlally 'expected' interpre-tation. In this regard, jokes have rnuch in cornrnon withscientific creativity, with what Thomas Kuhn calls a'paradigm shift' in response to a single 'anomaly'. (I t isprobably no coincidence that most creative scieiitists havea great sense of humour.) Of course, the aiiomaly in thejoke is the tradit ional punch line and the joke is 'funny'oiily if the listeiicr 'gets' the punch line hy seeing in aflash of insight how a completely new interpretation ofthe same set of facts can incorporate the anomalousending. The longer and inore tortuous the garden path ofexpectation, the 'funnier' the punch line when finallydelivered. Good comedians make use of this principle hytaking their time to build up the tension of the story line,for nothing kills humour more surely than a prematurepunch line.

However, although the introduction of a sudden twistat the end is necessary for the genesis of hurnour, it iscertainly not sufficient. My plane is about to land in SanDicgo and I faster1 my seat belt and get ready for touch-down. Th e pilot suddenly announces that the 'bumps' thathe (and I) had earlier dismissed as air turbulence arcreally due to engine failure and that we need to ernptyfuel before landing. A paradigrn shift has occurred in nlymind, but this certainly does not make nlc laugh. Katherit makes me orientate and prepare for action to cope withthe anomaly. O r consider the tirnc I was staying at sornefriends' house in Iowa City. They were away and I wasalone in unfamiliar surroundings. It was late at night andjust as I was about to doze off; I heard a 'thump' fromdownstairs. 'Probably the wind,' I thought. 'There arc noburglars in this ncighbourhood.'After a few rninutes therewas another thud, louder than the one before. Agaiii I'rationalixcd' it away arid went back to sleep. Twentyminutes later I heard an extremely loud, resoundiiig'bang' and leapt out of bed. What was happening? Aburglar perhaps? Naturally, with my limbic system acti-vated, I 'orientatcd', grabbed a flashlight and ran downthe stairs. Nothirlg funny so far. Then, suddenly I noticeda large flower vase in pieces on the floor and a largetabby cat right next to it - - the obvious culprit! This timeI started laughing because I realized that the 'anomaly' I


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1858 VI S. Ramachandran Con.sciousnes.c an d riro(ly image

had dctcctcd and thc subscyuent paradigm shift were oftrivial consequence. All of the facts could now beexplained in ternis of the cat theory rather than theominous burglar theory.

On the basis of this exaniplc, wc can sharpen the dcfi-nitiori of humour an d laughtcr. Wheri a pcrson strollsalong a gardcn path of cxpcctatiori arid thcrc is a suddentwist at thc cnd that entails a complete reiriterprctatiori ofthe sarnc facts arid the ncw iriterpretatiori has trivialrather than terrifying implications, laughter ensues.

But why laughtcr? Why this cxplosivc, rcpctitivcsourid? To an ethologist, on the other hand, any stereo-typed vocalization alniost always iniplies that theorganism is trying to commuriicatc somcthirig to otklcrsin thc social group. Now what might this bc in thc case oflaughter? 1 suggest that the mairi purposc of laughtermight he for the individual to alert others in the socialgroup (usually kin) that the detected arlomaly is trivial,nothing to worry about. The laughing person in eff'ectannounces her discovcry that thcre has been a fi~lsealarm, that the rest oS you chaps need rlot waste yourprccious energy and resources responding to a spuriousthreat (or, perhaps, also to playfully ccnsurc minor viola-tions of social taboos arid norms).

This 'false-alarm theory' of humour might also explainslapstick. You watch a marl---preferably orlc who is portlyand self-important wa ll


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(dyon~ciousnessn d bog$ ima

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Consciousness and Body Image: Lessons From Phantom