43
Porn, 19 (1984) 43-48 Elsevier
PAI 00632
Aging and Right-Left Asymmetry in Experimental Pain Measurement M. Neri and E. Agazzani Geriatrics Department, (Received
University of Modena, 41100 Modena (Ita
13 September
1983, accepted
22 November
1983)
Summary
Verbal psychophysical measurements were performed on 100 subjects, both male and female, aged from 20 to 82 years, to ascertain whether different responses to pain exist between the right and left sides of the body in relation to aging and to different capacities of the cerebral hemispheres to process emotions. A single-phase step current applied to the forearm provided a standard noxious stimulus. Sensory threshold (S), pain threshold (P), and tolerance threshold (T) were measured. The sample set was divided into 2 comparable groups either older or younger than 60 years of age. A common trend was found in both groups: right-side scores were consistently lower than the homologous left-side scores. This difference was significant for all thresholds in elderly subjects but only for the pain threshold in the younger subject group. Two-way ANOVA test of the two group scores did not reveal differences due to sex, but age was an influencing factor for sensory and pain thresholds, higher scores being found in the older subject group. An interpretation of the results embodies hemispheric capacities to process verbal and emotional stimuli.
Introduction Sensitivity to noxious stimulation during aging has been the object of many studies, but results are conflicting and as of yet, not definitive [ll]. Pain is more than a sensory phenomenon and is not comparable to any other perception modality. Cognitive and emotional aspects play an important role in noxious stimulation response modalities. Hence, one may agree with Melzack [15] that ‘pain comprises Mailing address: Dr. Mirco 41100 Modena, Italy. 0304-3959/84/$03.00
Neri, Cattedra
di Geriatria,
0 1984 Elsevier Science Publishers
B.V.
Ospedale
Estense,
Viale Vittorio
Veneto,
44
those subjective experiences which have both somatosensory and negative-~lf~~ctlv~ components and that elicit behaviour aimed at stopping the conditions that produce it.’
A great deal of neuropsychological data indicate changes in higher cognitive functions processing abilities during aging. Along with a general slowing-down of psychomotor skills for compiex tasks 1211,some authors f12) have found aging to he a greater burden on right (R) hemisphere functions, while left f L) hemisphere functions, i.e., verbal functions or those which may be verbalized, remain more intact. While functional differences between the two hemispheres with regard to cognitive capacities have been known for some time [20]. the discovery that differences also exist in the evaluation and production of emotional behaviours [8] is more recent. Clinical and experimental evidence has led to the formulation of two interpretative models ]2, for review]. The first foresees greater involvement of the R hemisphere in comparison to the L hemisphere in all aspects of emotional behaviour. The second supposes the R hemisphere to be more involved in the processing of emotions having negative connotations and the L hemisphere to be involved in positive emotions. Moreover, recent discussions [9] have focussed on the question of whether such differences may find a clinical confirmation in the unilateral pain syndromes presenting predominantly on the L side of the body [16]. The possibility that different thresholds for experimental pain stimuli exist between the two sides of the body, and thus that differences linked to aging are manifested, has received little attention. This investigation attempts to address these questions.
Methods
One hundred ~ght-handed volunteer subjects of both sexes ranging in age from 20 to 82 years were tested. A single-phase step current stimulus was applied to the volar surface of the forearm using annular electrodes [18,22]. A 100 Wz train of square wave pulses of 10 msec interval and 5 msec duration was used. The stimulus was increased by 10 PIA every 3 set, from 0 to 500 PA. The circuit has been designed to take into account skin resistance and interference due to electrical noise; output is given in mean voltage values. The modalities and aims of the experiment were explained to the subjects and informed consent was obtained. In a random order, 3 learning trials foliowed by IO expe~mental trials (5 on the L side and 5 on the R side) were carried out. The subjects were instructed to give 3 verbal responses constituting the psychophysical measurements. These were termed sensory threshold (S), pain threshold (P), and tolerance threshold (T). The S value refers to the first sensation of tickling or tingling. The term ‘pain’ alone was not used for the definition of the second threshold (P) since it might lead to ~sinte~retations; instead, we emphasized that the response was to be given when the sensation became unpleasant and the subject would have preferred to avoid it. Lastly, the T value indicated that current intensity was judged to be unbearable.
45
Since anxiety may considerably modify the responses, a Hamilton scale for anxiety (HS) IlO] was administered to the subjects to monitor this variable. The sample was divided into 2 groups, designated A x 60 and B > 60, which included subjects being either less or more than 60 years of age. The groups presented the following characteristics: A: N = 50 (F = 21, M = 29); mean age = 32 years (range: 20-59); mean educational level (calculated in school years) = 14 (range: 2-19); HS = mean 12 + 0.08. B: N = 50 (F = 30, M = 20); mean age = 67 years (range: 60-82); mean education level = 5 school years (range: 2-13); HS = mean 11 + 1.0. The two groups did not have significantly different HS scores (t = 0.39, NS).
Results
Mean values (x) and standard error (SE.) of the scores obtained by the two groups are reported in Table I. If we examine the relationship existing between right and left side values, the presence of a common trend emerges in the two groups for all the parameters considered: R side scores are constantly lower than the L side scores. The f paired test of difference between the means of R and L side scores within each group is only significant (P -c 0.05) for the pain threshold in group A and highly significant (P -c 0.001) for all parameters in group B. Comparing scores from both groups, one may note that group A values are constantly lower than the homologous group B values. Possible in~uencing factors to be taken into account are sex and education level. Regarding the former, the literature reports conflicting data concerning the greater sensitivity of females in evaluating pain and/or emotional stimuli [ 11 ,131. Regarding the latter, group -A and group B have markedly different education levels. These
TABLE
I
OUTCOME
MEASURES
(mean values z and standard
Group A ( < 60 years, N = 50) R
S.E.
error S.E.) Group B ( 160 years, N = 50)
Paired t
x
S.E.
Paired t
2.4 3.0
-4.92
***
2.9 3.4
-5.38
***
S
R L
25.7 27.2
1.7 1.6
-1.81
31.2 36.8
P
R L
43.6 45.5
2.6 2.6
- 2.01 *
47.3 53.3
T
R
56.8
3.5
L
59.2
3.4
* P <: 0.05. *** P 5 0.001. S = sensory threshold;
P = pain threshold;
- 1.80
T = tolerance
57.6
3.3
62.2
3.6
threshold;
- 3.96 ***
R = right; L = left.
AGE
AND
SEX DIFFERENCE5
IN PSY(‘HOf’HYSlCAL
.-.-.~-.~_-_._____ source of
p values -_II_
~___~____
THRESHtfl
_,_~_ -.__.._
_.
IlS _. _~ ~~
R
L
-----~__.-----.-. P .-.-________ R
Sex
1.72
1.02
0.96
Age
7.26 **
5.50 *
6.46 **
5.24 *
3.x
2.39
Sex X age
1.19
1.38
1.08
0.69
0.18
0.2?
variation
df=
s
~.._ __ 7 L
R
1.
0.79
0.67
0.74
92, I.
* P 2 0.05.
** P20.01. S = sensory threshold: P = pain threshold; T = tolerance threshold: R = right: L = left
factors were taken into consideration by using a 2-way analysis of variance (by sex and age), co-varied with education level, for comparison of the two groups. Results are summarized in Table II. Scores from groups A and B are influenced solely by age; no differences attributable to sex were found. The S and P thresholds showed significant differences in both limbs, while the T threshold had non-significant differences.
Discussion The constant presence in elderly subjects of significantly different scores on the two sides of the body supports previous evidence [23] of a better correlation between pain measurements on the right side of the body than on the left but contrasts with findings reported by other investigators. This may be attributable to the use of different types of noxious stimulation [17], to the choice of samples having a much lower mean age [5], or to stimulation of body sites having different hemispheric laterality 171. It is noteworthy that a completely verbal task was required of the subjects in this experimental model, possibly leading to the assumption that the L hemisphere was favoured. However, the type of response required from the subjects was different in the 3 parameters. Indeed, in the case of the S and T thresholds, a binary choice was requested (Yes/no, I do/don’t feel a tickling sensation; Yes/no, I can/can’t tolerate the pain). On the other hand, in the case of pain threshold. specification of both a qualitative nature (Is the sensation unpleasant now? Do you want to avoid it?) and a semantic-type verbal codification of the stimulus was elicited. The R cerebral hemisphere appeared to be more skilled than the contralateral hemisphere in qualitative choices. In light of these considerations, the differences noted between psychophysical parameter scores may be interpreted as a measure of central information processing time. In the case of the R limb thresholds, sensory input and verbal output are both
41
processed by the L hemisphere. Therefore, the information travels a short circuit. On the other hand, in the case of the L limb thresholds. a transcallosal transfer of the information is necessary and consequently, a longer circuit is traversed and more time is required [14]. The two hemispheres appear to have different competencies in exploring the intra- and extra-corporeal space [6, for review]. In effect, there is evidence indicating that only the contralateral hemispace is represented in the L hemisphere and that a global representation is organized on the right. This could result in a more rapid and careful stimulus selection by the L hemisphere. which finds itself operating on a lower number of possible comparisons. In group A the functional differences described above appear only as a general trend for the S and T thresholds, while a probable significance (P -c0.5) is present for the P parameter. Thus, one might conclude that the specific ability of the R hemisphere to perceive emotional qualities of the stimulus must be considered besides the previously described L hemisphere dominance. Results obtained in group B lead to the suspicion that a general factor linked to the aging process exists which tends to accentuate R-L unbalance. However, these results are not sufficient to explain where and how this impairment operates. It may involve either the widespread and often described slowing-down of central processing abilities [l] and transcallosal information crossing [14], or the accentuation of hemispheric sensitivity to contralateral inhibition [20]. The preservation of the same response trend in group B as in young subjects confirms the stability of L hemisphere verbal functions [ 121. One last point meriting comment concerns the differences due to aging found in the two groups. Our findings concur with other neurophysiological evidence, showing no significant modifications linked to sex, at least in older subjects [3]. For some time, reduced efficiency of peripheral receptors for somaesthetic sensitivity has been described during aging [11,18] and can perhaps be called upon here to account for the higher value of the S threshold resulting in group B. However, one may suspect that there exists a central factor capable of systematically producing these effects, thus explaining the homogeneity of the results for the two thresholds. It has been observed that the elderly person requires more time to explore a stimulus and does so with greater ‘caution’ before choosing the behaviour suited to it [19,21]. In the case of the two thresholds in question (S and P), such ‘caution’ may reasonably be considered the common central factor that functionally differentiates the two groups. It was observed that the older subjects of both sexes adopted a higher criterion of pain than the younger group. They seemed to report the tickling sensation and pain only when they were certain that the sensation and pain were present. The younger group appeared to be more liberal in the use of the S and P criterion [ll]. This phenomenon does not play a consistent role in the case of the T threshold. Our findings regarding this question do not concur with others which indicate that the elderly person ‘suffers’ less [4], but on the contrary, reveal that the elderly, when free from peripheral impairments, have the same ability as young people to produce rapid and effective behaviours when the stimulus becomes highly unpleasant.
48
The help provided by the ‘Centro gratefully acknowledged.
di Calcolo’
of the University
of Modem
iz
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