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Pain measurements in right-left cerebral lesions
Neuropsychobgia, Vol. 23, No. 1, pp. 123-126, Printed in Great Britam
1985 0
002&3932/85 %3.00+0.00 1985 Pergamon PressLtd.
NOTE PAIN MEASUREMENTS
IN RIGHT-LEFT
CEREBRAL
LESIONS*
MIRC~ NERI. G. P. VECCHIand M. CASFLLI
Geriatrics
Department.
University
of Modena.
Ospedale Estense. Italy
(Accepted
Viale Vittorio
Veneto,
9, l-41 100 Modena.
2 June 1984)
Abstract--Leftand right-brain damaged (BD) subjects were examined to ascertain whether psychophysical parameters of pain-pain threshold (P), tolerance threshold (T). and pain endurance (Etwere modified by brain damage and whether differences exist between LBD and RBD. Noxious stimulus was provided by electrical stimulation. Results showed that P and T scores for the paralysed arms were consistently higher than those of the contralateral side. This was not simply due to modified sensitivity alone; in the RBD group hemi-inattention and aphasia in the LBD group also played a role. A significantly hightened value of pain endurance was found only in the healthy arm in the RBD group.
INTRODUCTION DIFFERENTtheoretical models concerning possible hemispheric specialization for emotions have been proposed. One postulates a general dominance of the right hemisphere in the production and decoding of emotional behaviour [g], whereas the other limits right hemisphere competency to behavior having negative connotations [14]. Pain can undoubtedly be considered a paradigm of emotional experience having negative qualities 19). This condition may be measured by pschophysical parameters labelled respectively pain rhwshold (P), defined as the point at which pain is barely perceivable during an ascending stimulatory series, and pain tolerancr threshold(T), recognized as the point at which the individual judges the stimulus as unbearable and would prefer to withdraw from it 1171. These direct parameters vary according to the experimental context 1121. On the contrary, the values of indirect parameters such aspain endurancc~ (E) as reference point seem to be little influenced by contingent factors [ 171. Pain endurance is the arithmetical difference between the tolerance threshold and pain threshold (T-P) and represents a subject’s capacity to endure a stimulus recognized as noxious. It is believed to be more related to personality structure than to temporary emotional traits 113. 171. Evidence exists for a right-left imbalance in evaluating painful stimuli. but contrasting results have been reported regarding the predominance of the sides. In fact. MURRAY [IO, I I] in two subsequent trials utilizing thermal stimuli in young subjects revealed greater sensitivity of the left side of the body. In contrast. VECCHI [15], using electrical stimuli. registered greater sensitivity in the right body side of right-handed subjects, in agreement with a previous report 1167. Clinical research has demonstrated that unilateral cerebral lesion is capable of modifying emotional behaviour. with indifference and euphoria prevailing in cases of right-brain damage (RBD) and depression in cases of left-brain damage (LBD) [6. 71. Significant differences in both direct and indirect parameters may thus be expected for the pain experience. This study aims to ascertain whether direct parameters (P, T) and the indirect parameter (E) undergo modifications in the affected side of the body with respect to the contralateral side in BD subjects.
METHODS No selection was done in forming BD subject disorders serious enough to hinder administration *A version of this paper was presented September 1983.
groups; only patients presenting of the test were excluded.
at the Tenth European
123
Congress
consciousness
of Clinical Gerontology,
and alertness
Budapest.
I 3
1 he main charactcrlstic’r of the group\ wet-c: IY KBD S\. (M= 1. t-=JJ. mean age 60.6 jr: 8 LB11 Ss. (M=J. F=4). mean age 70.0 or; number of montha betucen onset of brain lesion: RBD SI- II -1. SE 2 Y: LBLI- 14.5. SE. 3.4. No significant difference? cxlst between KBI> and LBI) with regard\ IO age and discabe cl” ra I Ion
In the RBD group. 13 S\ presented contraIatc~-al hc~i~l-l~~ilttc~~t~~~~~. i Ss had n(, dcfic~t. I I SsI~ght to moderalc sensory deficit and 5 had severe deficit on the paralysed side. The left scores of these 5 Ss were excluded from the btatibtical anal!G\
ElectI-ical stimulation was chosen as the noxious \t~nr~dus 1I?. 171 The stimulus ~~ns~stcd ofa direct stepcurrent applied tothe\ol;rr\~~rt;~ce oftheforearm \~lthelcctrodes: spcctfically, a IO0c.p.s. train ofsquarcwave pulsesat IOmsec intervals and of 7-1~~s~ duratron wa\ adopted ((‘~stno~~~~nm~t “ANTALGIC” dcb~ce). Output was increased h) I (I /!A every 3 set from 0 to a ma\lmum of500 /IA Skin resistances Mere taken into account b) averaging the output of several cycles; the results were expressed in \~Jlt\ The procedures and am,a ofthe experiment were explamed to the Ss and after three learning trials. IO trials wrrc cart-ied out (five on the left and five on the right) in random order. Subjects were matructed to give two \erbul responses that were recorded ah the pain threshold (I’) and tolerance threshold (T). ‘The term “pain” alone was purposely avoided in the lirst response as it could have led to mlslnterprctatlons Instead. me explaIned that the response ~a\ to be given when the sensation became unpleasant and the sul>jcct ~\ould have preferred to avoid it The T threshold represents the point in which the suhiect no longer tolerated the sf~mulus The Indirect parameter (E) was derived from these two parameters (E-T I’).
RESULTS hlcan values and standard error ofthc psychophysical parameters described above are reported In Table I. Mean values for the paralysed limbs show R common trend: their I’ and T parameter score5 are constantly higher than those of the contralateral side. The differences in mean values were analysed using a I-paired test within each group. In the RBD group both direct parametersshow,ed highly significant differcnces(RPvs LP: /( 13); -5.X. I’
Table
I Mean values and standa~-d error for phychophysic
paramctcrs
Left braln damage Mean s E.
Kight brain damage Mean S.E. R
.37.6
.?,(I
60.5
54
L
5O.Y
3.4
45.7
3.‘)
R
40.4
3.5
6X. I
5’
L
17.7
3 i?
52.4
36
R
Il.7
P
I
I .o
7.5
0.6
0.x
6.6
I0
E L I’= Pain threshold:
h8 T=Tolcrancc
threshold:
E-pain
endurance:
R = right:
L-left
125
NOTE
It is reasonable that the variability found in the scores may be explained by concomitant neurological deficits. Furthermore modifications in emotional behaviour are referred to the time elapsed from the onset of the disorders
[71. To monitor the effect of these variables a two-way ANOVA covaried for the duration of the disorder was used on the scores, Hemi-inattention and PULS were the main effects considered in RBD group analysis. whereas aphasia and PULS were considered in LBD group. Hemi-inattention and aphasia were considered as dichotomic variables. while PULS was assigned one of four values, inversely related to sensory deficit. In the RBD group. the PULS variable was significant for both direct and indirect parameters relating to the paralysed limb [LP: F (2, 9)= 14.3, P
DISCUSSION Brain damage affects pre-existing responses to pain on both sides of the body. The direct parameters values (pain and tolerance thresholds) of the paralysed limb are constantly and significantly higher than those of the contralateral healthy arm. Using the same technique. a pattern was described [ 1S] in normal subjects in which direct right-side measurements were constantly lower than left-side scores, while no significant difference emerged for endurance scores. While left-brain damage induces an inversion of this direct parameters pattern, right-brain damage accentuates it. The present study cannot definitively answer the question of which mechanisms underlie this phenomenon. The results of ANOVA analysis lead us to suppose that sensory deficit alone cannot be considered since it was not a significant main effect in both groups, whereas the cognitive deficits, namely hemi-inattention and aphasia. in RBD and LBD respectively, always constituted a significant source of variation in the group. The balance in endurance value found in normal Ss was also present in LBD subjects, on the contrary RBD patients presented a modification of this pattern. RBD patients presented an increase of right, healthy arm scores, and this cannot be explained by the presence of the above described neurological deficits. It is worthwhile to point out that in our experiment left-brain damage affected only contralateral pain measurements, whereas right-brain damage affected both the direct, paralysed arm, and indirect, healthy arm, pain measurements. This evidence supports the hypothesis (see [S] for review) that an image of both sides of the body is represented in the right hemisphere whereas only the contralateral side is represented in the left hemisphere. Furthermore. the results confirm the important role of the right hemisphere in controlling negative emotional experiences. Indeed. while only direct parameters were modified in the case of LBD Ss, the significantly increased capacity to also endure pain and underrate the negative emotional characteristics of the stimuli by RBD Ss leads to postulate that this hemisphere may play a role not only in the recognition and evaluation ofemotional components of pain but also in the production of adequate “learned” responses to noxious stimuli. of which pain endurance may be considered an index. Acknowledgements-The provided by the “Centro
kind co-operation of R. Cubelli, Ph.D., in the neuropsychologial evaluation and the help di Calcolo Elettronico” of the University of Modena is gratefully acknowledged.
REFERENCES 1. ALBERT, M. L. A simple test of visual neglect. Neurolog! 23, 6588664, 1973. du language dans 2. BASSO, A., FAGLIONI. P. and VIGNOLO, L. Etude controlee de la reeducation comparaison entre aphasiques trait& et non trait&. Rev. Neural. 131, 607-614, 1975. 3. BISIACH,E. and FACLIONI, P. Recognition of random shapes by patients with unilateral lesions as a complexity, association value and delay. Cortex 10, 101-l 10, 1974. and 4. BUCHSBAUM, M. S.. DAVIS, G. C.. COPPOLA. R. and NABER, D. Opiate pharmacology differences. Pain 10, 357-366, 1981. and Cognition. Wiley, Chichester, 1982. 5. DE RENZI, E. Disorders of Space Exploration at manifestations d’indifference au tours des atteints 6. GAINOTTI, G. Reaction catastrophiques Neuropsycholo,yia
7, 195-204,
I’aphasie: function
of
individual
certbrales.
1969.
7. CAINOTTI, G. Emotional behaviour and hemispheric side of the lesion. Corlex 8, 4l- 55, 1972. emotion, and the right hemisphere. In Aspects of Consciousness, 8. LEY, R. G. and BRYDEN, M. P. Consciousness, G. UNDERWOODS, and R. STEVENS(Editors). pp. 215-240. Academic Press, New York, 1981.
126
Norr
aspects of pam In Rc.wurc~/~Puhliwlims: A.c.vocwtior~ /or Rcvc~u~/r 1,~.Vmwm mr/ 9. MIXZACK, R. Psychological Menral Disease--Pain, J. J. BONI~.A (Editor), pp. 143~ 154. Raven Press, New York, 1980. IO. MLIRRAY. F. S. and SA~FFRSTONF.J. F. Pain threshold and lolerance of righ[ and ldi hands. ./. mt~p. /‘/~~~.~io/. P,ry/roi. 1, 83 X6. 1970. I I. MURRAY, F. S. and HA(;I’N, B. C. pain threshold and tolerance of hands and feet. .I. wr,lp /‘J./uiol. /‘.~whol. 71, X3 X6, 1973.
of the pain threshold determined by electrical stimtllation and its clinIcal I?. NO~~RMA~S, S. L. H. Measurement application. Ncwolq~~ 16, IO7 1 10X6. 1966, and pain 13. TIMMERMANS,G. and ST~RURACH, R. A. Factors of human chronic pain: an analysis of personality reaction variables. Science 184, 806 808, 1974. P\! c/ro/. Bull. 1.I9 46. 19x1. 14. TUCKER. D. M. Lateral bram t’unctlon. emotion and conceptualization In Prrirr Th~wp,~~. R. RIZ/I and M. VIX~IIN IS. VK~HI, G. P.. CAL~A’, L. and NERI. M. Age and pain threshold. (Editors). pp. 35 -4X. Elsevier. Amsterdam, 1983. between superficial and deep somatic thresholds of pain with ri 16. WOLFF. B. B. and JARVIK. L. F Relationship note on handedness. A/U J. I’.r,~c~/ro/.77, 5X9 5YY. IYh4. .-l.wrw~rrtirm /or Rc.c~wdr in .VCWO~I~Tim/ 01‘human paIn. In Ro.tetrr~~/r Pd~/ic~cr/irv~.c. 17. WOLFF. B. B. Measurement Afm(cr/ Di.wtr.w Pair,. J. J. Bo~I(,A. (Editor). pp. 173 184. Raven Press. 19X0.
1985 0
002&3932/85 %3.00+0.00 1985 Pergamon PressLtd.
NOTE PAIN MEASUREMENTS
IN RIGHT-LEFT
CEREBRAL
LESIONS*
MIRC~ NERI. G. P. VECCHIand M. CASFLLI
Geriatrics
Department.
University
of Modena.
Ospedale Estense. Italy
(Accepted
Viale Vittorio
Veneto,
9, l-41 100 Modena.
2 June 1984)
Abstract--Leftand right-brain damaged (BD) subjects were examined to ascertain whether psychophysical parameters of pain-pain threshold (P), tolerance threshold (T). and pain endurance (Etwere modified by brain damage and whether differences exist between LBD and RBD. Noxious stimulus was provided by electrical stimulation. Results showed that P and T scores for the paralysed arms were consistently higher than those of the contralateral side. This was not simply due to modified sensitivity alone; in the RBD group hemi-inattention and aphasia in the LBD group also played a role. A significantly hightened value of pain endurance was found only in the healthy arm in the RBD group.
INTRODUCTION DIFFERENTtheoretical models concerning possible hemispheric specialization for emotions have been proposed. One postulates a general dominance of the right hemisphere in the production and decoding of emotional behaviour [g], whereas the other limits right hemisphere competency to behavior having negative connotations [14]. Pain can undoubtedly be considered a paradigm of emotional experience having negative qualities 19). This condition may be measured by pschophysical parameters labelled respectively pain rhwshold (P), defined as the point at which pain is barely perceivable during an ascending stimulatory series, and pain tolerancr threshold(T), recognized as the point at which the individual judges the stimulus as unbearable and would prefer to withdraw from it 1171. These direct parameters vary according to the experimental context 1121. On the contrary, the values of indirect parameters such aspain endurancc~ (E) as reference point seem to be little influenced by contingent factors [ 171. Pain endurance is the arithmetical difference between the tolerance threshold and pain threshold (T-P) and represents a subject’s capacity to endure a stimulus recognized as noxious. It is believed to be more related to personality structure than to temporary emotional traits 113. 171. Evidence exists for a right-left imbalance in evaluating painful stimuli. but contrasting results have been reported regarding the predominance of the sides. In fact. MURRAY [IO, I I] in two subsequent trials utilizing thermal stimuli in young subjects revealed greater sensitivity of the left side of the body. In contrast. VECCHI [15], using electrical stimuli. registered greater sensitivity in the right body side of right-handed subjects, in agreement with a previous report 1167. Clinical research has demonstrated that unilateral cerebral lesion is capable of modifying emotional behaviour. with indifference and euphoria prevailing in cases of right-brain damage (RBD) and depression in cases of left-brain damage (LBD) [6. 71. Significant differences in both direct and indirect parameters may thus be expected for the pain experience. This study aims to ascertain whether direct parameters (P, T) and the indirect parameter (E) undergo modifications in the affected side of the body with respect to the contralateral side in BD subjects.
METHODS No selection was done in forming BD subject disorders serious enough to hinder administration *A version of this paper was presented September 1983.
groups; only patients presenting of the test were excluded.
at the Tenth European
123
Congress
consciousness
of Clinical Gerontology,
and alertness
Budapest.
I 3
1 he main charactcrlstic’r of the group\ wet-c: IY KBD S\. (M= 1. t-=JJ. mean age 60.6 jr: 8 LB11 Ss. (M=J. F=4). mean age 70.0 or; number of montha betucen onset of brain lesion: RBD SI- II -1. SE 2 Y: LBLI- 14.5. SE. 3.4. No significant difference? cxlst between KBI> and LBI) with regard\ IO age and discabe cl” ra I Ion
In the RBD group. 13 S\ presented contraIatc~-al hc~i~l-l~~ilttc~~t~~~~~. i Ss had n(, dcfic~t. I I SsI~ght to moderalc sensory deficit and 5 had severe deficit on the paralysed side. The left scores of these 5 Ss were excluded from the btatibtical anal!G\
ElectI-ical stimulation was chosen as the noxious \t~nr~dus 1I?. 171 The stimulus ~~ns~stcd ofa direct stepcurrent applied tothe\ol;rr\~~rt;~ce oftheforearm \~lthelcctrodes: spcctfically, a IO0c.p.s. train ofsquarcwave pulsesat IOmsec intervals and of 7-1~~s~ duratron wa\ adopted ((‘~stno~~~~nm~t “ANTALGIC” dcb~ce). Output was increased h) I (I /!A every 3 set from 0 to a ma\lmum of500 /IA Skin resistances Mere taken into account b) averaging the output of several cycles; the results were expressed in \~Jlt\ The procedures and am,a ofthe experiment were explamed to the Ss and after three learning trials. IO trials wrrc cart-ied out (five on the left and five on the right) in random order. Subjects were matructed to give two \erbul responses that were recorded ah the pain threshold (I’) and tolerance threshold (T). ‘The term “pain” alone was purposely avoided in the lirst response as it could have led to mlslnterprctatlons Instead. me explaIned that the response ~a\ to be given when the sensation became unpleasant and the sul>jcct ~\ould have preferred to avoid it The T threshold represents the point in which the suhiect no longer tolerated the sf~mulus The Indirect parameter (E) was derived from these two parameters (E-T I’).
RESULTS hlcan values and standard error ofthc psychophysical parameters described above are reported In Table I. Mean values for the paralysed limbs show R common trend: their I’ and T parameter score5 are constantly higher than those of the contralateral side. The differences in mean values were analysed using a I-paired test within each group. In the RBD group both direct parametersshow,ed highly significant differcnces(RPvs LP: /( 13); -5.X. I’
Table
I Mean values and standa~-d error for phychophysic
paramctcrs
Left braln damage Mean s E.
Kight brain damage Mean S.E. R
.37.6
.?,(I
60.5
54
L
5O.Y
3.4
45.7
3.‘)
R
40.4
3.5
6X. I
5’
L
17.7
3 i?
52.4
36
R
Il.7
P
I
I .o
7.5
0.6
0.x
6.6
I0
E L I’= Pain threshold:
h8 T=Tolcrancc
threshold:
E-pain
endurance:
R = right:
L-left
125
NOTE
It is reasonable that the variability found in the scores may be explained by concomitant neurological deficits. Furthermore modifications in emotional behaviour are referred to the time elapsed from the onset of the disorders
[71. To monitor the effect of these variables a two-way ANOVA covaried for the duration of the disorder was used on the scores, Hemi-inattention and PULS were the main effects considered in RBD group analysis. whereas aphasia and PULS were considered in LBD group. Hemi-inattention and aphasia were considered as dichotomic variables. while PULS was assigned one of four values, inversely related to sensory deficit. In the RBD group. the PULS variable was significant for both direct and indirect parameters relating to the paralysed limb [LP: F (2, 9)= 14.3, P
DISCUSSION Brain damage affects pre-existing responses to pain on both sides of the body. The direct parameters values (pain and tolerance thresholds) of the paralysed limb are constantly and significantly higher than those of the contralateral healthy arm. Using the same technique. a pattern was described [ 1S] in normal subjects in which direct right-side measurements were constantly lower than left-side scores, while no significant difference emerged for endurance scores. While left-brain damage induces an inversion of this direct parameters pattern, right-brain damage accentuates it. The present study cannot definitively answer the question of which mechanisms underlie this phenomenon. The results of ANOVA analysis lead us to suppose that sensory deficit alone cannot be considered since it was not a significant main effect in both groups, whereas the cognitive deficits, namely hemi-inattention and aphasia. in RBD and LBD respectively, always constituted a significant source of variation in the group. The balance in endurance value found in normal Ss was also present in LBD subjects, on the contrary RBD patients presented a modification of this pattern. RBD patients presented an increase of right, healthy arm scores, and this cannot be explained by the presence of the above described neurological deficits. It is worthwhile to point out that in our experiment left-brain damage affected only contralateral pain measurements, whereas right-brain damage affected both the direct, paralysed arm, and indirect, healthy arm, pain measurements. This evidence supports the hypothesis (see [S] for review) that an image of both sides of the body is represented in the right hemisphere whereas only the contralateral side is represented in the left hemisphere. Furthermore. the results confirm the important role of the right hemisphere in controlling negative emotional experiences. Indeed. while only direct parameters were modified in the case of LBD Ss, the significantly increased capacity to also endure pain and underrate the negative emotional characteristics of the stimuli by RBD Ss leads to postulate that this hemisphere may play a role not only in the recognition and evaluation ofemotional components of pain but also in the production of adequate “learned” responses to noxious stimuli. of which pain endurance may be considered an index. Acknowledgements-The provided by the “Centro
kind co-operation of R. Cubelli, Ph.D., in the neuropsychologial evaluation and the help di Calcolo Elettronico” of the University of Modena is gratefully acknowledged.
REFERENCES 1. ALBERT, M. L. A simple test of visual neglect. Neurolog! 23, 6588664, 1973. du language dans 2. BASSO, A., FAGLIONI. P. and VIGNOLO, L. Etude controlee de la reeducation comparaison entre aphasiques trait& et non trait&. Rev. Neural. 131, 607-614, 1975. 3. BISIACH,E. and FACLIONI, P. Recognition of random shapes by patients with unilateral lesions as a complexity, association value and delay. Cortex 10, 101-l 10, 1974. and 4. BUCHSBAUM, M. S.. DAVIS, G. C.. COPPOLA. R. and NABER, D. Opiate pharmacology differences. Pain 10, 357-366, 1981. and Cognition. Wiley, Chichester, 1982. 5. DE RENZI, E. Disorders of Space Exploration at manifestations d’indifference au tours des atteints 6. GAINOTTI, G. Reaction catastrophiques Neuropsycholo,yia
7, 195-204,
I’aphasie: function
of
individual
certbrales.
1969.
7. CAINOTTI, G. Emotional behaviour and hemispheric side of the lesion. Corlex 8, 4l- 55, 1972. emotion, and the right hemisphere. In Aspects of Consciousness, 8. LEY, R. G. and BRYDEN, M. P. Consciousness, G. UNDERWOODS, and R. STEVENS(Editors). pp. 215-240. Academic Press, New York, 1981.
126
Norr
aspects of pam In Rc.wurc~/~Puhliwlims: A.c.vocwtior~ /or Rcvc~u~/r 1,~.Vmwm mr/ 9. MIXZACK, R. Psychological Menral Disease--Pain, J. J. BONI~.A (Editor), pp. 143~ 154. Raven Press, New York, 1980. IO. MLIRRAY. F. S. and SA~FFRSTONF.J. F. Pain threshold and lolerance of righ[ and ldi hands. ./. mt~p. /‘/~~~.~io/. P,ry/roi. 1, 83 X6. 1970. I I. MURRAY, F. S. and HA(;I’N, B. C. pain threshold and tolerance of hands and feet. .I. wr,lp /‘J./uiol. /‘.~whol. 71, X3 X6, 1973.
of the pain threshold determined by electrical stimtllation and its clinIcal I?. NO~~RMA~S, S. L. H. Measurement application. Ncwolq~~ 16, IO7 1 10X6. 1966, and pain 13. TIMMERMANS,G. and ST~RURACH, R. A. Factors of human chronic pain: an analysis of personality reaction variables. Science 184, 806 808, 1974. P\! c/ro/. Bull. 1.I9 46. 19x1. 14. TUCKER. D. M. Lateral bram t’unctlon. emotion and conceptualization In Prrirr Th~wp,~~. R. RIZ/I and M. VIX~IIN IS. VK~HI, G. P.. CAL~A’, L. and NERI. M. Age and pain threshold. (Editors). pp. 35 -4X. Elsevier. Amsterdam, 1983. between superficial and deep somatic thresholds of pain with ri 16. WOLFF. B. B. and JARVIK. L. F Relationship note on handedness. A/U J. I’.r,~c~/ro/.77, 5X9 5YY. IYh4. .-l.wrw~rrtirm /or Rc.c~wdr in .VCWO~I~Tim/ 01‘human paIn. In Ro.tetrr~~/r Pd~/ic~cr/irv~.c. 17. WOLFF. B. B. Measurement Afm(cr/ Di.wtr.w Pair,. J. J. Bo~I(,A. (Editor). pp. 173 184. Raven Press. 19X0.