Dual influence of temperature on compound nerve action potential

Dual influence of temperature on compound nerve action potential

Journal of the Neurological Sciences, 1981, 51 : 81 88 81 Elsevier/North-HollandBiomedicalPress D U A L I N F L U E N C E OF T E M P E R A T U R E ...

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Journal of the Neurological Sciences, 1981, 51 : 81 88

81

Elsevier/North-HollandBiomedicalPress

D U A L I N F L U E N C E OF T E M P E R A T U R E ON C O M P O U N D N E R V E ACTION POTENTIAL

A. H. LANG and A. PUUSA Department o]"Clinical Neurophysiology, University Central Hospital of Turku, 20520 Turku 52 (Finland)

(Received 2 December, 1980) (Accepted 23 December, 1980)

SUMMARY Compound neural action potentials (NAPs) were recorded from N. suralis and the digital nerves of N. medianus in man using the antidromic technique. The nerves were cooled either at the site of the recording ("local cooling") avoiding temperature change proximally, or between the stimulating and recording electrodes ("segmental cooling") avoiding temperature change at the recording site. Local cooling was followed by a pronounced increase in NAP amplitude and rise time without any change in the onset latency. The values of Ql0 were identical for both amplitude and rise time changes. Segmental cooling caused a definite fall in the amplitude of NAP and a slight increase in its rise time. The practical consequences of the dual temperature effect on NAP are discussed.

INTRODUCTION In electroneurography the amplitude and the shape of the compound nerve action potential (NAP) are used - along with the sensory nerve conduction velocity (NCV) - as diagnostic criteria in neuropathies. However, the variability of NAP amplitude decreases its diagnostic value compared with NCV. Knowledge of the causes of amplitude variability of NAP is obviously needed. The temperature dependence of NAP measurements has been the subject of only a few systematic studies and the results are somewhat controversial. While Buchthal and Rosenfalck (1966) were unable to show any systematic change in NAP amplitude by changing temperature, Ludin and Beyeler (1977) were able to Correspondence: HeikkiLang, M.D., Departmentof Clinical Neurophysiology,UniversityCentral Hospital of Turku, SF-20520Turku 52, Finland. 0022-510X/81/0000-0000/$02.50© Elsevier/North-HollandBiomedicalPress

82 show a definite increase in NAP amplitude with falling temperature. A corresponding temperature effect has been reported by DiBenedetto (1976). In the present study we have been able to show that NAP measurements change as a function of the temperature but that two different and opposite mechanisms with regard to the NAP amplitude changes seem to operate: a "local" temperature influence affecting the mechanism that generates the NAP, and a "segmental" influence affecting the conducting mechanism of the nerve fibres. METHODS The study was conducted on healthy members of the laboratory staff, aged 23-47 years. NAPs were recorded antidromically from N. suralis behind the lateral malleolus or from the digital nerves of the index finger. In the case of N. suralis, the active needle electrode (model DISA 13L6) was referred to a distant subcutaneous electrode. In N. medianus, bipolar recordings were made using 3 ring electrodes applied to each phalanx of the index finger and NAPs were derived either from the proximal and middle or proximal and distal electrodes (electrode distances about 10 mm and 30 mm, respectively). The nerves were stimulated transcutaneously at the middle of the sura and at the wrist by supramaximal pulses of 0.2 ms duration. NAPs were amplified by standard EMG amplifiers and averaged by a multichannel analyser. The recordings were either photographed from the screen of the analyser or plotted by a table computer also used for calculation and graphic readouts. The aim was to cool the nerves either "'locally" or "segmentally". Local cooling of N. suralis was performed by an ice-water pool constructed of modelling wax and located around the groove behind the lateral malleolus. The cooling was, however, not quite restricted to the recording site due to the relatively long diameter of the pool (about 30 ram). The digital nerves were cooled by wiping the index finger with evaporating liquid, and in this case the cooling was sharply restricted to the recording site only. Segmental cooling was performed by placing an ice pack on the sura between the stimulating and recording site and by holding the hand in the winter air for some minutes. In the first case the temperature at the recording site remained unchanged. The hand-cooling experiment was repeated in a single subject for 2 weeks until 133 recordings at different temperatures were collected. The other experiments were repeated on different subjects 4-5 times and the results were quite comparable. NAPs were recorded before, during and after the cooling procedure, during the phase of slowly rising temperature until the initial temperature level was reached. Care was taken to avoid displacement of the electrodes during the experiment. The temperature at the recording site was monitored in the case of N. suralis by a needle-shaped thermocouple inserted through the skin from outside the icewater pool into the vicinity of the recording electrode. The skin temperature at many points between the stimulating and recording electrodes and around the finger electrodes was also measured. A thermo-electric device was used for temperature measurements, with an accuracy of approximately 0.1 °C.

83 RESULTS

Typical series of recordings are shown in Figs. 1A and B. "Segmental" cooling of tissue between the stimulating and recording sites (Fig. 1A), besides causing a clearcut delay of NAPs, also causes a small but definite amplitude decrease. A slight increase of the rise time seems to take place (Fig. 2) the changes being restored by increasing temperature. "Local" cooling of the tissue at the recording site (Fig. 1B) causes a pronounced increase in the amplitude and the rise time of NAP. NAP is delayed at the same time, but as the cooled nerve segment is relatively long - the temperature falls even outside the pool - the cooling is, in fact, not strictly "local". These changes are also restored by increasing temperature. The results of the experiments shown in Figs. 1A and B are given graphically in Fig. 3. In order to study the effect of a very restricted "local" temperature change at the recording site upon NAP parameters, the index finger was cooled with evaporating liquid. In this case no temperature was observed "segmentally", i.e. at the volar surface of the hand. No change of onset latency occurred, but as can

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be seen in Fig. 4 the increase of NAP amplitude and rise time is evident, even in these bipolar recordings. Using a longer interelectrode distance (over 30 mm) a small kink in the falling phase of NAPs can be seen. With a shorter interelectrode distance (about 10 mm) this irregularity of the NAP shape disappears and the amplitude is somewhat lower and the rise time is shorter. The temperature dependence of the measurements of NAPs examined repetitively in the same subject and using bipolar finger recording and a long interelectrode distance are shown in Figs. 5A-D. The values have been plotted

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separately against the "local" temperature (skin temperature between recording electrodes, A and C) and the "segmental" temperature (average temperature of the volar surface of the hand, B and D). The regression lines do not seem to deviate significantly from linearity. A bigger scatter of the values around the regression line at lower temperatures seems evident. The negative correlation of NAP amplitude to "local" temperature values seems to be higher than to the "segmental" values. No such difference in rise time was found. The values of Q~0 calculated on the basis of the local temperature values (Figs. 5A and C) are for NAP amplitude 1.33 and for NAP rise time 1.35.

DISCUSSION

These results support the observation of Ludin and Beyeler (1977) that temperature changes have a prominent influence on the amplitude and shape of

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NAP. DiBenedetto (1976) also briefly mentions that "a drop in skin temperature from 33 to 27 degrees Centigrade may mean an increase of 10 #V in amplitude" of the antidromically recorded NAP of the digital nerves. It seems clear, however, that the temperature effect must be separated into 2 different components. While a "segmental" fall in tissue temperature between stimulating and recording sites causes an amplitude decrease and a slight increase in the rise time of NAP a strictly local fall in temperature at the recording site causes a pronounced increase in NAP amplitude and its rise time, with no increase in the onset latency. According to De Jesus et al. (1973) the slope of NCV-temperature regression is steeper for fast than for slowly conducting nerve fibres which means that the relative time dispersion of action potentials in nerve fibres of different diameter increases with falling limb temperature. Probably this is the mechanism which gives rise to the changes in amplitude and rise time following "segmental" cooling demonstrated in Fig. 1A. With "local" temperature change restricted to the recording site apparently no change in conduction velocity nor in time dispersion takes place in the nerve fibres, and no delay in the onset latency of NAP occurs. The amplitude and rise time changes are reversible which speaks against an artefact mechanism. This temperature effect seems not to be due to an impedance change with changing temperature (Ludin and Beyeler 1977). An identical Q,~ value both for the amplitude as well as the rise time calculated

87 on the basis of the "local" temperature speaks in favour of an identical biophysical mechanism. An increase in amplitude with falling temperature has also been shown to take place in muscle compound action potentials (Ricker et al. 1977). The basic mechanism of the temperature effect upon nerve and muscle compound potentials is unknown. Results from simulation experiments indicate that the changes in NAP caused by falling temperature can be explained by a combination of decreased amplitude and increased duration of single fibre potentials (Stegeman et al. 1979). The temperature influence upon the extracellularly recorded action potentials of single nerve fibres has been studied experimentally, but the results have been controversial (Gasser 1931; Hodgkin and Katz 1949). In practice, the "segmental" and the "local" temperature influences upon NAP work simultaneously, but depending on the experimental condition their relative effect varies. A fall of both the "segmental" and "local" temperature tends to increase the rise time of NAP which therefore changes more or less linearly. At this point our results (Figs. 5C and D) support those of Ludin and Beyeler (1977) and Buchthal and Rosenfalck (1966). The latter were unable to show any influence of temperature upon NAP amplitude, Ludin and Beyeler (1977) got a regression line of an inverted U-shape, but our results show a linear relationship (Figs. 5A and B). These discrepancies may be explained on the basis of the different experimental conditions. Ludin and Beyeler (1977) recorded NAP at the wrist but measured the temperature in the middle of the forearm. As can be seen in Figs. 5A and B, the correlation between temperature and amplitude of NAP improves the nearer to the recording site the temperature is recorded. Secondly, there may be differences in the temperature dependence of membrane functions along the nerve. In fact, Chatfield et al. (1953) have shown that the influence of temperature upon some enzyme activities of nerve fibres varies significantly along the length of the legs. Murai and Sanderson (1975) observed that the rise time of the antidromically measured NAP of the digital nerves is somewhat longer than the rise time of NAPs recorded orthodromically at the wrist, the onset latencies being equal. They concluded that the difference is a derivation artefact due to the antidromical bipolar recording technique, which can be avoided by using a short (= 10 mm) interelectrode distance which makes the rise time about identical at finger and at wrist. McLeod (1977) has also recommended the use of short interelectrode distances by antidromical NAP recording. These opinions require a comment. Our results show that the NAP rise time also increases with falling temperature when a bipolar recording is adopted (Figs. 4 and 5C and D). The longer rise time of distally recorded NAPs reported by Murai and Sanderson (1975), is very probably due to a somewhat lower temperature superficially in the fingers than in the deep tissue of the wrist. The rise time of NAPs recorded distally can artificially be shortened by making the interelectrode distance so short that the compound potential is recorded at the distal electrode before its peak has arrived at the proximal electrode. This is demonstrated in Fig. 4: a kink on the falling phase of NAP recorded by a long interelectrode distance shows that the potential

88 arrives at the distal electrode after the peak has subsided at the proximal electrode. By making the interelectrode distance shorter the kink disappears and the amplitude and rise time of NAP decrease slightly, obviously due to a derivation artefact. In order to avoid this artefact and to obtain the biggest possible signal the interelectrode distance has to be as long as possible. A distance of 30 mm or more seems to be a "safe" distance. Multiregression analysis is a rational way of taking into account many varying factors simultaneously when making a decision on whether a measurement is normal (Lang et al. 1977; Kuusela and Lang 1979). By measuring both the "local" and the "segmental" skin temperature and by making a "statistical correction" on the rise time and amplitude of NAP the variability of NAP parameters can be effectively reduced (work in preparation). This may considerably increase the diagnostic value of NAP amplitude and rise time measurements. REFERENCES Buchthal, F. and A. Rosenfalck (1966) Evoked action potentials and conduction velocity in h u m a n sensory nerves, Brain Res., 3: l 122. Chatfield, P. O., C.P. Lyman and L. Irving (1953) Physiological adaptation to cold of peripheral nerve in the leg of the herring gull (Larus argentatus), Amer. J. Physiol., 172:639 644. De Jesus, P.V.. I. Hausmanowa-Petrusewicz and R.L. Barchi (1973) The effect of cold on nerve conduction of h u m a n slow and fast nerve fibres, Neurology (Minneap.), 23:1182 1189. DiBenedetto, M. (1976) Electrodiagnostic evidence of subclinical disease states in drug abusers, Arch. phys. Med., 57: 62-66. Gasser, H. S. ( 1931) Nerve activity as modified by temperature changes, Amer. J. Physiol., 9 7 : 2 5 4 270. Hodgkin, A.-L. and B. Katz (1949) The effect of temperature on the electrical activity of the giant axon of the squid, J. Physiol. (Lond.), 109:240 249. Kuusela. V. and A. H. kang (1979) Elimination of systematic variance in laboratory measurements and the P-values A method lk)r reporting laboratory results. In: D. A. B. Lindberg and P. L. Reichcrtz (Eds.), Lecture Notes in Medical Informatics (Medical lnformatics, No. 5), Proceedings, Berlin, 1979, Springer-Verlag, Berlin, 1979, pp. 965. Lang, A . H . , .1. Forsstr6m, S.E. Bj6rkqvist and V. Kuusela (1977) Statistical variation of ncrvc conduction velocity An analysis in normal subjects and uraemic patients, J. neurol. Sci.. 33: 229-241. Ludin, H. P. and F. geyeler (1977) Temperature dependence ot normal sensory nerve action potentials, J. Neurol., 216:173 180. Mckeod, J. G. (1977) Nerve conduction measurements for clinical use. In : H. Van Duijn, D. N. J. Donker and A.C. Van Huffelen (Eds.), Didactic Lectures c~["the 9th blternational Congress ~/ Electroencephalography and Clinical Neurophysiology, Drukkerij Trio, The Hague, pp. 83 98. Murai, Y. and I. Sanderson (1975) Studies of sensory conductions Comparison of latencies of orthodromic and antidromic sensory potentials, J. Neurol. Neurosur~,. P.~:vchiat., 38:1187 1189. Ricker, K., G. Hertel and G. Stodieck (1977) Increased voltage of the muscle action potential o1" normal subjects after local cooling, J. Neurol., 216:33 38. Stegeman, D. F., J. P. C. De Weerd, H. M. Vingerhoets and S. k. H. Notermans (1979) A model for the simulation of c o m p o u n d action potentials of nerves in situ used of explanation of temperature influences, Acta neurol, scand., 60 (Suppl. 73): 154.