_'ournal of Neurology, Neurosurgery, and Psychiatry 1992;55:81 1-821

Psychophysical correlates of phantom limbexperience

Joel Katz

Department ofPsychology, TheToronto Hospital,Toronto GeneralDivision, andDepartment ofBehavioural Science,University ofToronto,Toronto, Ontario,CanadaJ Katz

Correspondence to:Dr Katz, Department ofPsychology, The TorontoHospital, Toronto GeneralDivision, 200 ElizabethStreet, CW2-306, Toronto,Ontario M5G 2C4, Canada

Received 28 January 1991and in final revised form7 November 1991.Accepted 20 November1991

AbstractPhantom limb phenomena were corre-lated with psychophysiological measuresofperipheral sympathetic nervous systemactivity measured at the amputationstump and contralateral limb. Amputeeswere assigned to one of three groupsdepending on whether they reportedphantom limb pain, non-painfil phantomlimb sensations, or no phantom limb atall. Skin conductance and skin tempera-ture were recorded continuously duringtwo 30 minute sessions while subjectscontinuously monitored and rated theintensity of any phantom limb sensationor pain they experienced. The results fromboth sessions showed that mean skin tem-perature was significantly lower at thestump than the contralateral limb in thegroups with phantom limb pain and non-painfil phantom limb sensations, but notamong subjects with no phantom limb atall. In addition, stump skin conductanceresponses correlated significantly with theintensity of non-painful phantom limbparesthesiae but not other qualities ofsensation or pain. Between-limb meas-ures of pressure sensitivity were not sig-nificantly different in any group. Theresults suggest that the presence of aphantom limb, whether painfil or pain-less, is related to the sympathetic-efferentoutflow of cutaneous vasoconstrictorfibres in the stump and stump neuromas.The hypothesis of a sympathetic-efferentsomatic-afferent mechanism involvingboth sudomotor and vasoconstrictorfibres is proposed to explain the relation-ship between stump skin conductanceresponses and non-painful phantom limbparesthesiae. It is suggested that increasesin the intensity of phantom limb pares-thesiae follow bursts ofsympathetic activ-ity due to neurotransmitter release ontoapposing sprouts of large diameter prim-ary afferents located in stump neuromas,and decreases correspond to periods ofrelative sympathetic inactivity.The resultsof the study agree with recent suggestionsthat phantom limb pain is not a unitarysyndrome, but a symptom class with eachclass subserved by different aetiologicalmechanisms.

(7 Neurol Neurosurg Psychiatry 1992;55:811-82 1)

More than 90% of amputees report a persist-ing, sensory awareness ofthe cut off part.1 This

phenomenon has been termed the phantomlimb and is usually described as having atingling or numb quality. For many amputees,however, a distressing problem is pain in thephantom limb. Recent surveys based on severalthousand amputees reveal that 70% continueto experience phantom limb pain years afteramputation.2 In the long term only 7% ofpatients are helped by the more than 50 typesof therapy used to treat phantom limb pain.3This intractability reflects our ignorance aboutthe mechanisms that contribute to phantomlimb pain.

Recently, Sherman et al4 have argued thatphantom limb pain is not a unitary syndrome,but a symptom class, with each class subservedby different aetiological mechanisms. Forexample, one class of phantom limb painwhich is characterised by a cramping quality isassociated with EMG spike activity in musclesof the stump whereas burning phantom limbpain shows no such association.4 Katz andMelzack5 have identified a class of phantomlimb pain which resembles in quality andlocation a pain experienced in the limb beforeamputation. Although the precise physiologicalmechanisms that underlie these somatosensorypain memories are unknown, the presence ofpre-amputation pain clearly is a necessarycondition for these phantom pains todevelop.Another class of phantom limb pain may

come about through involvement of the sym-pathetic nervous system. Sympatheticallymaintained pains have been attributed tosympathetically-triggered ephaptic transmis-sion,6 sympathetic activation of sensitised noci-ceptors7 or low threshold mechanoreceptorswhich terminate on sensitised spinal cordcells,8 and injury-induced alteration in thepattern of postganglionic cutaneous vasocon-strictor neurons which lose their normal ther-moregulatory function leading to trophicchanges and ischaemia.6Evidence of sympathetic involvement among

amputees comes from studies which phar-macologically block9 or surgically interrupt'0the sympathetic supply to the involved limbproducing at least temporary alleviation ofpain. Transient relief from phantom limb painhas been reported with propranalol, a beta-adrenergic blocking agent."1 Electrical ormechanical stimulation of the lumbar sym-pathetic chain produces intense pain referredto the phantom limb,'2 13 whereas sensationsare referred to the abdomen or flank in patientsexperiencing pain without amputation.'2

Surprisingly few studies have compared cor-

811

relates of peripheral sympathetic nervous sys-

tem activity at the stump and contralaterallimb of human amputees. Sliosberg"4 exam-

ined 141 amputees and found that the stumpwas cooler than the intact limb in 94 patientsbut he did not relate the temperature differ-ences to the presence or absence of phantomlimb pain. Kristen et al" reported that a

"patchy asymmetrical temperature" distribu-tion of stump thermograms was significantlymore frequent among stump pain sufferersthan in patients who were free from stumppain, but thermograms were no different forpatients with or without phantom limb pain.Nystr6m and Hagbarth'6 made micro-neurographic recordings of activity from mus-

cle nerve fascicles of the peroneal nerve in a

patient with a below-knee amputation whosuffered from intense cramping pain referredto the phantom foot. Although bursts ofactivity in sympathetic fibres were accentuatedby the Valsalva manoeuvre, the phantom painremained unchanged suggesting that, in thispatient, the cramping pain was independent ofperipheral sympathetic nervous system activ-ity.

In contrast, Sherman et al'7 18 recentlyobserved a negative correlation between tem-perature at the stump and the presence ofburning phantom limb and stump pain indi-cating that reduced blood flow to the stump isassociated with increased levels of pain.Repeated measurements of the same patientson different occasions revealed that lowertemperatures at the stump relative to thecontralateral limb were associated with greaterintensities ofphantom limb and stump pain. Inthe majority of cases, however, the relationshipbetween phantom pain and limb temperaturewas confounded by co-existing stump pain,and so it is not possible to unambiguouslyattribute the presence ofphantom limb pain toaltered blood flow at the stump. In addition,decreased blood flow to the stump may be a

feature of all stumps regardless of the patient'sstatus with respect to phantom limb pain.

Further evidence of a link between sym-pathetic nervous system activity at the stumpand phantom limb sensations was furnished byKatz et all9 who demonstrated an associationbetween stump skin conductance and theintensity of non-painful phantom limb pares-thesiae. Stump skin conductance correlatedsignificantly with the intensity ofphantom limbparesthesiae during two 60-minute sessions ina patient with a non-painful phantom limb.Their results suggest that phantom limbparesthesiae may in part be explained by a

cycle of sympathetic-efferent primary afferentactivity. Post-ganglionic sympathetic sudomo-tor and vasomotor fibres located in the stumpmay produce a phasic pattern of neurotrans-mitter release which alters the firing rate ofadjacent primary afferents projecting ontospinal cord cells subserving the portion of thelimb which is missing. Katz et al'9 proposedthat this fluctuating pattern of activity istransmitted rostrally where it is perceived asincreases and decreases in the intensity ofphantom limb paresthesiae.

Taken together, certain qualities ofphantomlimb sensation and pain may have peripheraltriggers involving sympathetic-somatic links,but further study is required to assess thenature of this relationship in amputees withpainful or non-painful phantoms as well as inthose without phantom limbs. This study was

designed to compare skin temperature, skinconductance and pressure sensitivity thresh-olds of the stump and contralateral limb inthree groups of amputees: 1) Group PLP withphantom limb pain; 2) Group PLS with non-

painful phantom limb sensations, and 3)Group No PL with no phantom limb. Basedon previous work by Sherman et al'7 18 it wasproposed that subjects with phantom limb painwould show significantly lower mean skintemperature at the stump relative to the con-tralateral limb. In addition, based on theresults of Katz et al,'9 it was proposed thatmeasurements of stump skin conductanceobtained over time would correlate signifi-cantly with the intensity of non-painfulparesthesiae referred to the phantom limb.

MethodSample The sample and recruitment proce-dures for this study have been described indetail elsewhere.20 The subjects were 28 ampu-tees (18 males and 10 females) who hadundergone amputation of the upper extremity(above-elbow in 2; below in 1) or lowerextremity (above-knee in 16; below in 9). Thereason for amputation was peripheral vasculardisease (including diabetes mellitus) in 12subjects, accident in 9, arterial thrombosis in3, tumour in 2, and one each for radiationdamage and polio. The mean age and timesince amputation was 52-8 years (range: 23 to73 years) and five years (range: 36 days to 46years), respectively. Patients with dementia or

acute psychopathology were excluded.The subjects were assigned to one of three

groups on the initial session based on thepresence or absence of painful or non-painfulphantom limb sensations at the time of testing.Group PLS consisted of 9 amputees whoreported feeling only non-painful phantomlimb sensations, group PLP consisted of 11subjects who reported phantom limb pain, andgroup No PL consisted of 8 amputees whoreported that they did not feel the presence ofa phantom limb at all. Two subjects in groupNo PL and one in group PLP reported stumppain of a burning quality on both sessions. Onesubject in group PLS reported non-painfultingling sensations in the stump on bothsessions. All other subjects were free of stumppain or other stump sensations.

Experimental apparatus Skin conductancemeasurements taken at homologous points onthe stump and contralateral limb wereobtained using a portableThought Technologybiofeedback module with digital display(SC200T) and Ag/AgCl Beckman electrodes.The electrode paste consisted of a mixture ofphysiological saline and a neutral ointmentcream with the recommended concentration ofapproximately 0 05 molar NaCl.2' Surface

812

Psychophysical correlates ofphantom limb experience

skin temperature measurements at the stumpand contralateral limb were obtained using aYellow Springs Instruments (YSI) digital ther-mometer, Model 49TA, and 2 YSI Model409A temperature probes. The Model 49TAhas an ambient temperature range of - 10° to+ 50°C with a resolution of 0-01'C and isaccurate to ± 0-05'C within a range of30'-40'C. Skin conductance and skin tem-perature leads from each limb were connectedto a two-channel electromechanical relay thatswitched channels every 10 seconds. Theoutput from the relay fed into the skin conduc-tance and skin temperature modules whichalternated between displaying informationfrom the stump and contralateral limb every 10seconds.The subject rated changes in perceived

phantom limb intensity of painful or non-painful sensations by turning a dial whichallowed 180 degrees of rotation. The 90 degreesetting was labelled "USUAL", 0 degrees,"LESS", and 180 degrees, "MORE". The dialwas connected to a 1-35 volt mercury batteryvia a 10 000 ohm potentiometer and theoutput fed into a digital volt meter whichregistered 0 through 0-675 to 1-35 voltscorresponding to the 0, 90, and 180 degreesettings of the dial, respectively. Data acquisi-tion was accomplished by videotaping thedigital output of the skin conductance, skintemperature, and phantom limb intensity dis-plays during each 30 minute session. A digitalstopwatch which was started at the beginningof each session, was also filmed to provide areference point when transcribing the raw datavalues for subsequent analysis.

Skin sensitivity to pressure was assessedusing the Semmes-Weinstein pressure aesthesi-ometer (Shaw Laboratories, New York) whichconsists of a set of 20 individual nylon fila-ments of equal length (38 mm) ranging from0-06 to 1 14 mm in diameter. Each filamenthas been assigned a value that represents thelogarithm of the force (in mg) required to bendit maximally when pressed against the skin.The McGill Pain Questionnaire22 was used

to obtain quantitative and qualitative measuresof the experience of pain. The questionnaireyields two global scores, the total pain ratingindex and the present pain intensity. The totalpain rating index is the sum of the rank valuesof the words chosen from 20 sets of qualitativewords, each set containing two to six adjectivesthat describe sensory, affective, evaluative, andmiscellaneous properties of pain. The lists ofpain descriptors are read to the patients whoare asked to choose the word in each categorythat best describes their pain at the moment.The present pain intensity is rated on a scale ofzero to five as follows: 0 = none, 1 = mild,2 = discomforting, 3 = distressing, 4 = hor-rible, and 5 = excruciating.

Procedure The investigator scheduled 2 ses-sions for the same time on consecutive days orwith as few days intervening between sessionsas could be arranged. Subjects were requestedto refrain from smoking and drinking coffeeand alcohol on the days they were to be seen.Those with phantom limb pain were asked not

to take any pain medication on the days theyhad been scheduled in order to maximisepotential between-group differences in skinconductance and temperature, and to obtainan accurate, medication-free description of thepain.Informed written consent was obtained after

the experimental procedures were explained.The subjects removed their prostheses anduncovered the homologous region of the con-tralateral limb 30 minutes before data collec-tion to allow the limbs to adjust to theconditions in the room. The experimentercleaned the stump and contralateral limb withalcohol and placed the skin conductance elec-trodes and temperature probes on the distalportion of the stump approximately 5 cm fromits end, and at mirror-image regions on thecontralateral limb.

Mirror-image points on the two limbs weremarked with a felt-tipped pen to identifystimulation sites for pressure sensitivity. Pres-sure sensitivity thresholds were obtained firstfrom the stump and then the other limb.Strands of hair surrounding the selected pointswere carefully cut before sensory testing toensure that the filaments came in contact withthe skin only. The subjects closed their eyesand stated when they felt they had beentouched. On each trial, a filament was appliedto the designated point on skin for approx-imately one second. Trials were separated byan interval ranging from five to fifteen secondsto reduce the likelihood of anticipatory respon-ses. Filaments were applied in ascending serialorder until the subject had correctly respondedon five consecutive trials. Pressure sensitivitythreshold was defined by the value associatedwith the filament that had been used on thefirst of these five trials (that is, the filamentwith the smallest diameter).The subjects then completed the McGill

Pain Questionnaire and several mood andanxiety rating scales. Video recording of thestopwatch, skin conductance, skin tem-perature, and phantom limb intensity displayswas initiated after the subjects had practisedusing the dial and had begun monitoring theirphantom limb. The subjects were told thatwhenever they registered a change in phantomlimb intensity by turning the dial, they werealso to provide a brief description ofthe qualityof the phantom limb sensation or pain.

Psychophysiological data reduction Thevideotape from each session was reviewed andone value of skin conductance, skin tem-perature and phantom limb intensity wasobtained every 10 seconds for both 30 minutesessions. Mean values of phantom limb inten-sity were transformed by subtracting a con-stant of 0-675 from each. This served torelocate the scores so that the 90 degreeposition of the dial labelled "USUAL" took ona value of 0 0, and deviations from it, in theclockwise and counter-clockwise directions(corresponding to increases and decreases inphantom limb intensity), had maximum valuesof ± 0 675, respectively.The audio portion of the videotape from

each session was transcribed verbatim for each

813

Katz

Pressure Sensitivity Threshold

Session 1 Session 2501 U stump

0 intact limb

4.0 1 T

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PLP PLS No-PL PLP PLS No-PL

Skin Conductance

T31

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Skin Temperature

ResultsGroup differences in psychophysiological meas-urements Figure 1 shows the mean pressuresensitivity thresholds, skin conductance level,and skin temperature, obtained at each limbfor the three groups of amputees on the twosessions. Each variable was entered into a3-way ANOVA using group (PLP, PLS, NoPL) as the independent-samples factor, andSession (1, 2) and Limb (stump, contralateral)as the repeated-measurements factors. Theanalysis of skin temperature revealed a sig-nificant main effect for the limb factor indicat-ing that overall stump skin temperature wassignificantly lower than that of the contralaterallimb. All other main effects and interactionswere not significant (p > 0 05).The theory that stump skin temperature

would be significantly lower than the con-tralateral limb in group PLP was tested byplanned comparisons of the two limbs onsessions 1 and 2. As displayed in fig 1, thestump was significantly cooler than the con-tralateral limb for subjects in group PLP andgroup PLS on both sessions (group PLP: F (1,25) = 9 79, and 10-4 for sessions 1 and 2,respectively, both p < 0 005; group PLS: F (1,25) = 5 05 and 432, both p < 0 05). Forgroup No PL, however, the mean temperaturedifference between the limbs failed to reachsignificance on either session (F (1,25) = 2d17 and 199 for sessions 1 and 2respectively, both p > 0 05). The results indi-cate that the presence of a phantom limb,whether painful or painless, is associated withsignificantly lower skin temperature on thestump than the contralateral limb.

Group differences in the intensity and quality ofphantom limb sensations Table 1 shows themean McGill Pain Questionnaire scores forgroups PLP and PLS corresponding to the

F

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33

32

31

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PLP PLS No-PL.

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Table I Mean McGill Pain Questionnaire (MPQ)present pain intensity scores and pain rating indexes(PRI) for the sensory, affective, evaluative, miscellaneous,and total classes presented for Groups PLP and PLS on

sessions 1 and 2. Standard deviations are contained inbrackets. P-values correspond to theANOVA F-testcomparing group means. Note that unlike Group PLP, thePRIs from Group PLS do not represent pain intensity, butinstead, intensity of non-painful phantom limb sensations.For this reason, all present pain intensity ratings fromGroup PLS have a value of zero, corresponding to theMPQ descriptor "no pain"

PLS No-PL

3roup

Figure I Mean pressure sensitivity thresholds, skin conductance and skin temperature ofthe stump and contralateral limb displayed for the 3 groups of amputees on both sessions.PLP refers to phantom limb pain; PLS, non-painful phantom limb sensations; No PL,no phantom limb at all. Mean stump skin temperature was significantly lower than thecontralateral limb on both sessions for Groups PLP (**p < 0-00S) and PLS(*p < 0O05) but not Group No PL.

subject. Every verbal description of phantomlimb pain (or sensation) was recorded in termsof its quality (for example, tingling, shooting),and time-matched to the correspondingchange in phantom limb intensity which thesubject had registered using the dial.

Session I

Group PLP Group PLS(n)=II (n= 9) p-value

MPQ ClassPRI-Sensory 9 0 (7-3) 3-2 (4-7) 0-004PRI-Affective 2-9 (2-8) 0 0 0 001PRI-Evaluative 1-5 (1 1) 0-6 (0 5) 04001PRI-Miscellaneous 3-7 (2-7) 1-3 (1-6) 0 001PRI-Total 17-1 (11 1) 5-1 (60) 00002Present pain intensity 2-2 (1-1) 00 -

Session 2

Group PLP Group PLS(n = 11) (n = 9) p-value

MPQ ClassPRI-Sensory 9 1 (5 9) 2-8 (2 7) 0 0001PRI-Affective 1-5 (2 4) 0-1 (0-3) 0-06PRI-Evaluative 1-5 (1-0) 0 4 (0-7) 0 001PRI-Miscellaneous 3-6 (3-3) 1-7 (1-5) 0-006PRI-Total 15-7 (11-6) 5-0 (4 0) 0-0004Present pain intensity 1 9 (0 7) 00 -

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Psychophysical correlates ofphantom limb experience

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Figure 2 Plots of the relationship between stump skin conductance and the intensity aphantom limb paresthesiae for two subjects in Group PLS. Skin conductance wasmeasured at the stump over a 30 minute period while the subjects monitored the intensof the phantom limb by turning a diaL Phantom limb intensity ratings have beentransformed so that a value of 0.0 represents the intensity at the start of the session andeviations from it correspond to increases and decreases in phantom limb intensity.Changes in the intensity ofparesthesiae (described as increases and decreases in "numsensations referred to the phantom limb) occur in concert with changes in stump skinconductance. Also shown is the correlation coefficient describing the strength of therelationship between the two variables and the subjects' descriptions of the quality of thphantom sensation. Abbreviations as in fig 1.

intensity ofthe painful or non-painful phant4limb on sessions 1 and 2. As can be seen, mepain rating indexes for group PLP are snificantly higher than those for group PLSboth sessions, consistent with the fact thatformer group comprises subjects with phztom limb pain, and the latter, non-painphantom limb sensations.

In addition to these quantitative differencthe quality of the phantom limbs in the tgroups also differed. Table 2 shows the McCPain Questionnaire adjectives chosen by 3or more of subjects in groups PLS and PLPdescribe the various qualities of phantom lirsensation or pain. The descriptors selectedgroup PLS (for example, "pricking", "tgling", "numb") indicate that the painliphantom limb is defined primarily by pares

esiae whereas the qualities of sensation thatdescribe the painful phantom are more varied.Nevertheless, there is a consistency in thechoice of descriptors between groups: everydescriptor chosen by 33% or more of subjectsin group PLS was also chosen by 33% or more

, subjects in group PLP, although other descrip-c tors were also endorsed by the latter groupa with greater frequency.- Further evidence that the painful phantomE limb embodies more than the basic paresthetic0

c quality characteristic of the painless phantomcomes from an analysis of the different qual-

. ities of sensation subjects reported whenmonitoring their phantom limb during the two30 minute observation periods. Chi squareanalyses using Yates' correction for continuityconfirm that the qualities of sensation reportedby subjects with phantom limb pain were morevaried than those with non-painful phantomlimbs. Taken together, these data reveal thatthe phantom limb experiences of the twogroups have in common a paresthetic quality,although painful phantoms consist of morethan this shared component and includedsensations of pressure, constriction, throbbing,

t pulsating, pumping sensations and somatosen-sory pain memories.

Between-subject correlations ofpain ratings and- psychophysiology. Pearson correlation coeffi-E cients were computed between the psy-

chophysiological measurements taken at theE two limbs and the McGill Pain Questionnairec ratings for all 28 subjects on the two sessions.

Also computed were the correlation coef-ficients describing the relationship between thelimb difference scores and McGill Pain Ques-tionnaire ratings. Limb difference scoresshown in table 3 were obtained by subtractingmeasurements taken at the contralateral limbfrom those at the stump. Negative difference

)f scores indicate that relative to the contralateral~ity limb the stump is lower in temperature, lower

in skin conductance, and more sensitive tod applied pressure.

Correlation coefficients ranged between rb (26) = 0-37 and r (26) = 0-33, indicating that

at most 14% of the variance in pain ratingse could be explained by the psychophysiological

variables. Using Bonferonni's correction formultiple tests of significance, even the highestcoefficient failed to reach significance (all

om p > 0-05). Mean skin temperature, skin con-Man;ig-

on Table 2 McGill Pain Questionnaire (MPQ) descriptorsthe chosen by 33% or more of subjects in Groups PLP andan- PLS to describe the sensations experienced in the phantomIful limb. Note that the adjectives chosen by Group PLP

describe phantom limb pain, and those chosen by GroupPLS describe non-painfid phantom limb sensations

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MPQ Class Group PLP (n = 11) Group PLS (n 9)

Sensory Pricking PrickingSharpHotTingling Tingling

Affective TiringSickeningPunishingWretched

Evaluative Annoying AnnoyingMiscellaneous Numb Numb

Nagging

815

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0 5 10 15 20 25 30

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Figure 3 The relationship between stump skin conductance and phantom limbfor a subject in Group PLS shown for one entire 30 minute session (top panel).of viewing, the bottom panel shows only the first 10 minutes of the same sessiontwo measures showed a prominent tendency to covary. All changes in phantomintensity were described by the subject as increases and decreases in "numbness'experienced in the phantom foot. Abbreviations as in fig 1.

painful phantom limb paresthesiae for 3 sub-jects in group PLS. Figure 4 shows the

0.9 relationship between stump skin conductanceand the intensity of phantom limb pain com-

2 prised of various qualities of sensation for 2, subjects in group PLP. There is a pronounced

0.6 tendency for increases and decreases in the' intensity of phantom limb paresthesiae to beE accompanied by similar changes in stump skin

0.3 = conductance for subjects in group PLS (figs 2E and 3). In contrast, changes in the intensity of0c phantom limb pain and stump skin conduct-

0.0 ance occur independently with little or notendency for the two measures to covary (fig4).

-0.3 Table 4 shows the number of subjects in thetwo groups with significant correlations (usingBonferonni's type I error rate correction formultiple tests of significance) between phan-tom limb intensity and stump skin conduct-ance and temperature. The mean correlationcoefficient between these measures for the twogroups is also shown. The most salient featureof these data is that the majority of subjects in

0.9 group PLS show significant positive correla-tions whereas this is not the case for group PLP

a (table 4). A chi-square analysis comparing the0.6 c frequency of significant and non-significant

c correlations between the groups was significant7, (x2 (1) = 3-65, p < 0-06) indicating that thereE is a significant positive relationship between

0.3 =I stump skin conductance and phantom limbO intensity for proportionally more subjects ina group PLS than group PLP (for example, figsIL 2-4).

A one way between-groups ANOVA wascarried out on the mean correlation coefficient

4-3 between phantom limb intensity and stumpskin conductance (sessions 1 and 2 combined).Group PLS demonstrated a significantly stron-

intensity ger linear relationship than group PLP (F (1,For ease 29) = 7-15, p < 0-01) indicating that, on

when the average, the proportion of the total sharedlimb variance is greater in group PLS than group

PLP. Finally, the relationship between phan-tom limb intensity and stump skin conduct-ance was significantly greater than zero for

ductance, or pressure sensitivity threshold ofeither limb does not appear to be related to theintensity of phantom limb pain or sensations.Nor is the magnitude of the mean differencebetween the limbs associated with the intensityof the McGill Questionnaire pain ratings.There is no simple linear relationship betweenthe psychophysiological measurements andphantom limb pain intensity. Overall, subjectswith large limb difference scores do not reporthigh pain scores and those with little or no

difference between limbs do not report little orno pain.

Relationship between phantom limb intensityand stump skin conductance The relationshipbetween changes in stump skin conductanceand the intensity of phantom pain/sensationacross both 30 minute sessions was assessedfor each subject by Pearson correlation coeffi-cients and by plotting the two variables to-gether as a function of time. Figures 2 and 3show plots of the relationship between stumpskin conductance and the intensity of non-

Table 3 Mean stump-intact limb difference scores forpressure sensitivity thresholds (PST), skin conductance(SC), and skin temperature (ST) presented for the threegroups of amputees on sessions 1 and 2. Standarddeviations are contained in brackets. Stump-intact limbdifference scores were obtained by subtractingmeasurements taken at the intact limb from those at thestump. Negative difference scores indicate that relative tothe intact limb the stump is lower in skin temperature,lower in skin conductance, and more sensitive to appliedpressure

Session I

Group PLP Group PLS Group No PL(n=11) (n = 9) (n = 8)

PST (log mg) 0-31 (1-3) 0-25 (1-2) -0 004 (0 5)SC (umhos) 0-61 (3-0) 0 11 (0 7) 0 43 (0-4)ST ('Celsius) -1-59 (1-8) -1-26 (1-3) -0-88 (1-9)

Session 2

Group PLP Group PLS Group No PL(n =11) (n = 9) (n = 8)

PST (log mg) 0-30 (0-6) -0-21 (0-6) 0-11 (0-7)SC (umhos) 0-02 (1-7) -0-06 (1-5) 0-74 (0-9)ST ('Celsius) -1-75 (1-8) -1-25 (1-5) -0-85 (2-0)

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Psychophysical correlates ofphantom limb experience

Case E06

a

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Minutes

Case E07

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10

MinutesFigure 4 Plots of the relationship between stump skin conductance and various qual;ofphantom limb pain for 2 subjects in Group PLP. There is no relationship between s,skin conductance and the intensity ofphantom limb pain. Abbreviations as in fig 1.refers to somatosensory memory.

group PLS (r (88) = 0-29, p < 0-01) butgroup PLP (r (88) = -O002, p > 0 4Together, these results indicate that phanilimb intensity and stump skin conductancerelated in subjects reporting non-painful phtomr limb sensations (that is, paresthesiae)not in subjects with phantom limb pain (Nreport more varied qualities of sensation).

Table 4 Mean Pearson correlation coefficients (r) for Groups PLP and PLS describithe linear relationship between phantom limb intensity (PLI) and stump skin conduct(SC), and PLI and stump skin temperature (ST). Group correlation coefficients werobtained by averaging the correlations for each subject and are based on a total of 90points over 30 minutes. Also shown for each group is the number of significant(p < 0-002) correlations between PLI and stump SC, and PLI and stump STforsessions I and 2 combined. P-values correspond to the Chi-squared test andANOVAF-test for between-group comparisons offrequencies and means, respectively

Group PLP (n = 11) Group PLS (n = 9) p-val

Correlation coefficient: (r):PLI and stump SC -0-02 029** 0 01PIU and stump ST 0-06 -0-17 ns*

Number of significant rs:PLI and stump SC 6/19 (32%) 8/12 (67%) 0-06PLI and stump ST 8/19 (42%) 5/12 (42%) ns*

*not significant (p > 0 05).**significantly (p < 0-05) different from zero.

It was not possible to determine the tempo-ral primacy of phantom limb intensity andstump skin conductance which would haveanswered the question of whether changes inone preceded or followed changes in the other.

<,, The low sampling rate ofone measurement per,,, limb every 10 seconds was a limitation of the

electromechanical relay which fixed the mini-.E mum possible time lag between consecutive= measurements taken from the same limb at 20E seconds, clearly far too wide a time frame to0C capture the temporal relationship between the

variables.Detailed presentation of stump skin tem-

perature was not undertaken since it was highlynegatively correlated with skin conductanceand thus provided little in the way of uniqueinformation. In addition, examination of plotsof skin temperature and phantom limb inten-sity showed that skin temperature changedvery slowly and lacked the sensitivity apparentin the measure of skin conductance.

Between-limb correlations The relationshipbetween the psychophysiological variablesmeasured at the stump and contralateral limbwas evaluated for each subject by examining

Z. time plots of the two limbs on each session. Inc addition, the Pearson correlation coefficient@ describing the strength of the linear relation-

ship between the two limbs was computed forE each subject for skin conductance and skinE temperature over both 30 minute sessions. The° between-limb correlation coefficients wereX entered into separate 2-way ANOVAs (Groupa. x Session) for skin conductance and skin

temperature. All main effects and interactionterms for both analyses were not significant (allp > 0 05). For the majority of subjects therewas a marked similarity in the pattern ofactivity measured at the stump and the con-

ities tralateral limb suggesting that the processestump responsible for moment-to-moment fluctua-SM tions in skin conductance and skin tem-

perature are governed by a central mechanismand are not limb-specific.

not05).tom Discussionare The relationship between phantom limbs andian- stump skin temperaturebut The significant limb temperature differencewho among phantom limb pain sufferers confirms

Livingston's,9 and more recently Sherman etal's7 1 assertion that phantom limb pain isassociated with reduced blood flow in the

ing stump relative to the contralateral limb. How-eance ever, the presence of a similar temperature

difference in subjects with a painless phantomlimb (defined primarly by paresthesiae) but notamong amputees who report no phantomlimb, raises the possibility that reduced stumptemperature contributes to the paresthetic

ue (dyesthetic) component of the phantom limb,both in groups PLS and PLP, but plays no rolein generating other qualities of phantom limbsensation or pain.

In previous studies of amputees,17 18reduced stump blood flow was confounded bythe presence of both phantom limb pain andstump pain in most patients. With three excep-

817

818

prefrontal cortex amygdala

lateral hypothalamus

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:::::.........:::. :::.:::.:::1.Z\....S. :.f.:..;... :.^... .. ., L. :.!...... .-.:1::::'.''::: ........... --..,.. ::::::::--.::-:\:-:. ::.-

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) SWealC lands*Se F9m a

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Figure 5 Schematic diagram iUlustrating a mechanism of symphathetically-generated phantom limb paresthesiae.Spontaneous activity or excitatory inputs descending from cortex (for example, due to the perception of a salient event,loud noise) increase the discharge rate ofpreganglionic (pg) sympathetic neurons with cell bodies in the lateral horn(LH) of the spinal cord and terminals in the sympathetic ganglion (SG). These neurons excite postganglionicnoradrenergic (NA) cutaneous vasoconstrictor (cvc) and cholinergic (ACh) sudomotor (sm) fibres which impinge oneffector organs (vascular smooth muscle and sweat glands) in the stump and on sprouts from large diameter primaryafferent (pa) fibres which have been trapped in a neuroma. The release ofACh and NA on effectors organs results inincreased electrodermal activity (EDA) and decreased blood flow (BF) to the stump. Release of these chemicals in theneuroma activates primary afferents which project to spinal cord dorsal horn (DH) cells subserving the amputated partsof the limb. These neurons, in turn, feed back to the preganglionic sympathetic neurons and project rostrally where theimpulses contribute to the perception ofphantom limb paresthesiae. IfDH cells have been sensitised due to injurv, ornociceptive primary afferents are activated, then the perception may be one of dysesthesiae. Adaptedfrom Fields"8 withpermission.

tions, two of whom were in group No PL andtherefore did not experience a phantom limb,all subjects in the present series were free ofstump pain. Thus the finding that the lowerstump skin temperature is characteristic ofamputees who report a phantom limb, in theabsence of associated stump pain, points to theimportance of the vasomotor limb of thesympathetic outflow as a contributing factor tothe perception of a phantom. Whether thetemperature difference between the limbsreflects regional sympathetic hyperactivity ordenervation sensitivity cannot be addressed bythe present results since a large proportion ofpatients had peripheral vascular disease with orwithout diabetes mellitus. However, the threegroups of amputees did not differ significantlywith respect to the proportion of patients withperipheral vascular disease.

The relationship between phantom limbs andstump skin conductanceThe absence of a between-limb difference inmean skin conductance levels for groups PLSand PLP may be related to the significantlylower skin temperature of the stump relative tothe contralateral limb since neural activity in

sudomotor and vasoconstrictor fibres are dif-ferentially affected by temperature.23 Thelower stump temperature may have con-tributed to decreased electrodermal activity inthe same way as a cool environment reducesactivity in sudomotor fibres. Warming of thestump (to the temperature of the contralaterallimb) may be expected to result in significantlyhigher levels of skin conductance at the stumprelative to the contralateral limb. On the otherhand, injury is known to produce effects thatspread centrally to affect the contralaterallimnb.24 25 Thus the absence of a between-limbdifference in mean skin conductance levelsmay reflect amputation-induced changes insympathetic function that extend to includethe contralateral limb as well.Although mean levels of stump skin conduc-

tance did not differ significantly from thecontralateral limb in any group, changes instump skin conductance over time correlatedsignificantly with changes in the intensity ofphantom limb paresthesiae among subjects ingroup PLS. Furthermore, the mean correla-tion coefficient between stump skin conduct-ance and phantom limb intensity wassignificantly greater in group PLS than PLP,

tump rpourorna

to cortex,.:'ii

't

rSG

Katz

Psychophysical correlates ofphantom limb experience

and was significantly greater than zero forgroup PLS but not group PLP. These resultsconfirm and extend those of Katz et al'9 whoreported a significant relationship betweenstump skin conductance and phantom limbintensity in a single case study of an amputeewith a non-painful phantom limb defined byparesthesiae. Two theories may explain thesignificant relationship.

Hypothesis 1: Sympathetic activity results inphantom limb paresthesiae The first hypothesisexplains the relationship between sympatheticactivity at the stump and the intensity ofphantom limb sensations by assuming thatneurotransmitter release from sympatheticfibres in the stump and stump neuromasactivates large diameter primary afferents inclose proximity. These afferent impulses giverise to referred paresthesiae upon reachingcentral cells subserving the amputated parts ofthe limb (fig 5).There are several lines of evidence to sup-

port this hypothesis. First, sympathetic activityin the form of skin conductance responses andchanges in skin temperature reflect the activityof post-ganglionic sudomotor and vasomotorfibres, respectively.23 Multiunit sympatheticactivity recorded from skin nerve fascicles inawake humans shows a strong relationship toeffector organ responses including vasocon-striction and sweat gland activity.23 Thesestudies demonstrate that bursts of activity insudomotor and vasomotor fibres are reliablyfollowed by transient electrodermal responsesand plethysmographic signs of vasoconstric-tion within the region of skin subserved by thesympathetic fibres under study.

Second, intraneural recordings from sensorynerve fascicles in conscious humans reveals a

remarkably strong relationship between theperception of non-painful paresthesiae andspontaneous bursting activity in afferentfibres.26 Finally, non-noxious percutaneouselectrical stimulation of afferent nerves locatedin the stump of forearm amputees results inparesthesiae referred to a localised region ofthe phantom hand but not the stump. Sub-sequent alterations in the amplitude of elec-trical stimulation are paralleled bycorresponding perceptual changes in the inten-sity of phantom limb paresthesiae which thesubjects can track reliably using a manualdevice similar to that used in this study.27Taken together, these studies raise the pos-

sibility, outlined in Figure 5, that changes inthe intensity of phantom limb paresthesiaereflect the joint activity of cholinergic (sudo-motor) and noradrenergic (vasomotor) post-ganglionic sympathetic fibres on primaryafferents located in the stump and stumpneuromas. Bursts of activity in sympatheticfibres produce transient vasoconstriction andheightened skin conductance levels. Shortlyafter, afferent fibres in stump neuromas wouldincrease their rate of firing due to the liberationof acetylcholine and noradrenaline. Thus themoment to moment fluctuations in the inten-sity of phantom limb paresthesiae characteris-tic ofthe subjects' response patterns (figs 2 and3), may partly represent a cycle of sym-

pathetic-efferent and somatic-afferent activity.Increases in the intensity of phantom limbparesthesiae would follow bursts of sympath-etic activity due to neurotransmitter releaseand decreases would correspond to periods ofrelative sympathetic inactivity.

Hypothesis 2: Phantom limb sensations result insympathetic activity The second hypothesisexplains the relationship between sympatheticactivity at the stump and the intensity ofphantom limb sensations by assuming thatperipheral sympathetic activity, in the form ofelectrodermal and vasoconstrictive responses,occurs as a result of a perceived change in theintensity of the phantom limb. According tothis hypothesis, the subject's detection of achange in phantom limb pain or other phan-tom limb sensations results in vasoconstrictionand heightened electrodermal activity much asany anticipated and salient signal during avigilance task produces a generalised orientingresponse.28For most subjects in this study, the two

hypotheses cannot be distinguished on thebasis of temporal primacy. In some patients(for example, Case E02 in fig 2) it is clear thatheightened electrodermal activity preceded theperception of increasingly intense paresthesiae.For these patients, a sympathetic-efferentsomatic-afferent cycle of activity may beresponsible for triggering the perception ofphantom limb paresthesiae.

In addition, the second hypothesis assumesthat heightened electrodermal activity occursas the result of a perceived change in thephantom limb and therefore predicts that thedetection of any phantom sensation, whetherpainless or painful, would produce increases inelectrodermal activity. The results indicate,however, that the patterns of stump skinconductance and phantom limb intensity wererelated significantly more frequently amongsubjects in group PLS (who reported phantomlimb paresthesiae) than subjects in group PLP(who reported a host of different qualities ofphantom limb pain) despite the fact that thepainful phantom was more intense and hencemore salient than the non-painful phantom(table 1). These findings are inconsistent withthe second hypothesis which does not dis-tinguish between the effects of different qual-ities of phantom limb sensation on stump skinconductance responses.Given that stump skin conductance levels

were not exaggerated and the two limbsshowed a remarkably similar pattern of electro-dermal responses over time, it is pertinent toask why paresthesiae were experienced in thephantom limb but not the contralateral limb(or other parts of the body). Evidence suggeststhat the threshold for impulse generation islower both in regenerating primary afferents inthe stump and in deafferented central cellssubserving the phantom limb than it is in theintact nervous system. Regenerating sproutswhich have formed a neuroma are exceedinglysensitive to the post-ganglionic sympatheticneurotransmitters noradrenaline29 and acetyl-choline30 and discharge rapidly when thesesubstances are present. In contrast, intact

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Katz

peripheral fibres do not show this chemo-sensitivity, and thus have a higher thresholdcompared with regenerating sprouts. Second,deafferentation results in a loss of inhibitorycontrol over cells in the dorsal horn and morerostral sensory structures3 32 giving rise to theperception of a phantom limb.32 This impliesthat the threshold for detecting sympathet-ically-triggered afferent impulses arising fromstump neuromas should be lower than at other,intact body sites since stump impulses wouldbe subject to less inhibition upon reaching thespinal cord. This fits well with the observationthat the threshold for detecting sensations inthe phantom limb during stimulation of thestump is lower than at the site of stimulationitself.33 Together, these two observations mayexplain the propensity for the phantom limb tobe the site of sympathetically-generatedreferred sensations even in the absence ofregional sympathetic hyperactivity.

Pressure sensitivity thresholds of- amputationstumps The lack of a significant differencebetween pressure sensitivity thresholds at thestump and contralateral limb is surprisingsince amputation stumps have consistentlybeen found to display greater skin sensitivitythan the corresponding region of the con-tralateral limb. Lowered thresholds at thestump have been demonstrated in adults forlight touch, two-point discrimination andpoint localisation after amputations of theupper extremity34 and for two-point discrim-ination following lower extremity amputa-tions.35 Similar results have been found forpressure sensitivity and two-point discrimina-tion thresholds in children with congenitalabsence of limbs.36 37 Most of these studiesincluded patients with amputations due totrauma or accident and measured tactile acuityfrom several points on each limb. It is possiblethat the lack of a significant between-limbdifference in sensitivity thresholds in the pres-ent study stems from the inclusion ofamputeeswith peripheral vascular disease and diabetesmellitus as well as the restricted sampling of asingle region on each limb.

Recent evidence supports the view thatphantom limb pain is not a unitary syndromebut a symptom class with each class subservedby different aetiological mechanisms. Consis-tent with this view, the present study proposesthat one mechanism underlying the perceptionof phantom limb paresthesiae or dysesthesiaeinvolves a sympathetic-efferent somatic-affer-ent cycle in which both postganglionic sudo-motor and vasomotor fibres participate.Fluctuations in the intensity of paresthesiaereferred to the phantom limb reflectcorresponding changes in peripheral sympa-thetic nervous system activity which may occurspontaneously or be induced by emotionally-charged events. Other qualities of phantomlimb sensation or pain (for example, cramping,shooting, somatosensory memory pains)which do not correlate with sympathetic nerv-ous system activity at the stump may betriggered by activity in other peripheral struc-tures (for example, muscle) or more centralneural structures. Simultaneous microelec-

trode recordings of post-ganglionic sympa-thetic and primary afferent fibres inamputation stump neuromas would providevaluable information about the qualities ofreferred phantom sensation that are associatedwith sympathetically-generated afferent activ-ity.

I thank the staff and patients of the following hospitals andinstitutions for their kind and helpful cooperation: CatherineBooth Hospital Centre, Federation des Personnes Amputee duQuebec, J E Hanger Inc, Montreal Convalescent HospitalCentre, Montreal General Hospital, Orthomedics Inc, RoyalVictoria Hospital, St Anne's Veterans Hospital. I am grateful toProfessor Ronald Melzack for his generous support of thisproject and helpful comments when preparing the manu-script.

This study was carried out when the author was a doctoralstudent at McGill University. The research was supported byGrant A7891 from the National Sciences and EngineeringResearch Council of Canada to Professor Ronald Melzack, andby postgraduate scholarships from the Medical ResearchCouncil of Canada, and the Fonds FCAC pour l'Aide et leSoutien a la Recherche (Quebec Government) to the author.Preparation of the manuscript was supported by fellowshipsfrom the Health Research Personnel Development Program ofthe Ontario Ministry of Health and the Medical ResearchCouncil of Canada. The results and conclusions derived hereinare those of the author, and no official endorsement by theOntario Ministry of Health is intended or should be inferred.

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