Study of the early somatosympathetic reflex response

Neuroscience Letters, 2 (1976) 319--323

319

© Elsevier/North-Holland, Amsterdam - - Printed in The Netherlands

STUDY OF THE E A R L Y SOMATOSYMPATHETIC R E F L E X RESPONSE V.P. LEBEDEV, N.N. ROSANOV, V.A. SKOBELEV and K.A. SMIRNOV

Laboratory of Circulation, I.P. Parlor Institute of Physiology, Academy of Sciences of the U.S.S.R., Leningrad 199164 (U.S.S.R.)

(Received April 16th, 1976) (Accepted May 25th, 1976)

SUMMARY

Using anesthetized cats, we studied the early components of the somatosympathetic reflex in the white rami communicantes of segments T3 and L2 in response to stimulation of the corresponding segmental somatic nerves. The results show that the early somatosympathetic reflex is a complex and highly organized response consisting of three typical waves. The shortest latency wave of this reflex was investigated in detail and evidence of its monosynaptic nature was obtained. Calculations showed that the efferent part of this reflex c o m p o n e n t may be formed b y sympathetic preganglionic neurons with axonal conduction velocities of a b o u t 10 m/sec or more.

It is well known n o w that strong stimulation of the somatic nerves, especially the segmental ones which enter into the spinal cord at the thoracic and high lumbar levels, elicit in white rami (WR) b o t h short and long latency reflex responses [7,13]. The first, or 'early response' (ER), is considered mainly as an indication of segmental activation of the sympathetic preganglionic neurons and is generally regarded as not differentiated into separate components [1,2,14]. Having registered the ER in lumbar WR we noticed that this reflex reaction consisted of several components with peculiarities which had not been studied previously. The present paper is devoted to a detailed description of the different ER c o m p o n e n t s and to searching for their origin. I t w a s also of interest to discover whether the ER features in lumbar WR are typical of the ER in all sympathetic WR. The experiments were carried o u t on 57 cats anesthetized with a mixture of pentobarbital and a-chloralose (15 and 45 mg/kg, intraperitoneally), immobilized with Flaxedil and artificially ventilated. The ER in dissected L2WR and TsWR was elicited b y stimulation of the corresponding segmental nerves and was recorded unipolarly. In response to a single electrical stimulus applied to the segmental nerves (impulse duration 0.2 msec and strength a b o u t 30--50 times higher than that

320

for low threshold A-fibers) in L2WR and T3WR, the ERs consisting of three typical components were registered (Fig. 1). The second c o m p o n e n t marked as II (ER-II) was the most prominent and constant. In half of the observations the division of ER-II into three parts (ER-IIa, ER-IIb and ER-IIc) was possible. The ER-II in 50% of L2WR records and in 70% of T3WR records were preceded by one or several short discharges labeled ER-I (Fig. 1). After the ER-II in 35.5% experiments with L2WR and in 90% experiments with T3WR the desynchronized waves labeled ER-III appeared. Quantitative characteristics of these different ER components are presented in Table I. It is evident that the ER-I is the true reflex because the electrotonic influences of the nearby somatic nerve from which the WR originates were excluded. The role of dorsal root reflexes in ER-I genesis was also rejected. As it is inherent to different reflexes, the ER-I could be facilitated and inhibited in certain experimental conditions and it was characterized by large posttetanic potentiation. The short duration of the ER-I discharges and their equal amplitudes in consecutive records convinced us that they are formed b y activation of a single, or at the most, a very few WR fibers.

b

B

Fig. 1. Components of the ER in WR. A: the ER in T3WR, averaging 40 responses (ATAC system). Separate components are labeled by Roman numerals and letters, see text, B: examples of the ER in L~WR. Records from three different experiments. Top records: single sweeps; b o t t o m records: superposition o f five sweeps o f the beam. Arrows denote times of stimulation. Calibrations: amplitude, 20 ~V; time, 10 msec (A), 5 msec (B).

321 The data presented in Table I indicate t ha t t he first discharges o f t he ER-I have a latency as short as 4.5 msec and t hat this value is stable. These facts p e r m i t us to suggest t h a t t he ER-I is m o n o s y n a p t i c in origin. This suggestion is c o n f i r m e d b y th e calculation of t he ER-I central delay. As was shown in experiments recording input neurogram in dorsal rootlets, t he ER-I is elicited o n l y b y activation of af f er e nt fibers with a c o n d u c t i o n velocity o f n o t m ore t h a n 30 m/sec. Therefore, the afferent c o n d u c t i o n in our experimental conditions takes a b o u t 1--1.3 msec. The ef f er e nt c o n d u c t i o n time can be correctly calculated if c o n d u c t i o n velocities in different sympathetic preganglionic fiber groups are tak e n into account. L a t e n c y measurements of sympathetic pregangiionic n e u r o n (SPN) discharges in t he lateral horns o f thoracic and lumbar segments d e m o n s t r a t e d t ha t t he majority of these SPNs had axonal c o n d u c t i o n velocities of 3--6 m/sec. Only very few lateral horn SPNs had axons with a c o n d u c t i o n velocity as high as 9--10 m/sec [4,10,12]. According to these data the ef f er e nt c o n d u c t i o n time for SPN axons with 5 - 6 m/sec velocities occupies a b o u t 4 msec, as L2WR and T3WR are a b o u t 22--26 m m long. Hence, in this situation, t he central delay of t he ER-I would be negative and r ath er unreal. Only in the case where the c o n d u c t i o n velocity in SPN axons b eco mes greater t ha n 10 m/sec can the ER-I central delay be equal t o 1.5 msec. This value is identical with the central delay of classical monosynaptic reflexes transmitted through the lumbar intumescence o f the spinal cord [11]. As appears f r o m the calculation presented above, t he ER-I must be a result o f m o n o s y n a p t i c activation of SPNs with an axonal c o n d u c t i o n velocity higher th an 10 m/sec. Since SPNs with such a x o n features do n o t occur in th e spinal lateral horns but do occur in preganglionic nerves [3,4,10] this discrepancy provides a chance t o d e t e c t the SPN outside t he lateral horns. This idea will be co nf i r m e d in the following paper [9]. Concerning th e ER-II and t he ER-III it is evident t hat these reflex responses result f r o m polysynaptic activation o f the SPN. A sustained variability of TABLEI QUANTITATIVE CHARACTERISTICS OF INDIVIDUAL COMPONENTS OF EARLY SOMATOSYMPATHETIC REFLEXES IN T3WR AND L2WR Characteristics

WR ER-I

ER-II

ER-III

a

b

c

Latency (msec)

T3 L2

4.2 ± 0.2 4.83 ± 0.2

10.5 ± 1.2 9.6 ± 0.2

14.2 ± 1.4 13.9 ± 0.4

17.6 ± 1.6 16.2 ± 0.4

21,9 ± 1.3 19.8 ± 0.8

Amplitude (,V)

T3 L~

3.6 ± 0.7 8.6 ± 0.8

14.9 ± 4.3 13.5 ± 1.0

12.2 ± 2.1 12.3 ± 1.0

18.1 ± 7.3 10.9 +_1.0

7.2 ± 1.7 9.5 ± 1.2

Duration (rnsec)

T3 L2

1.0 ± 0.2 2.0 ± 0.2

3.9 ± 1.2 5.2 ± 0.4

3.6 ± 1.1 4.2 ± 0.3

4.6 ± 1.1 3.9 ± 0.4

6.7 ± 1.8 7.5 ± 0.1

322 latency, amplitude and duration in consecutive records characterizes these ER components. It must be noted that the latency of ER-III is similar to the latent period of the spino-bulbo-spinal c o m p o n e n t of somatosomatic reflexes. But unlike the latter the former one does not disappear after spinal transection. These observations were made during registration of ER-III in L2WR after spinal transection at the T10 level. Therefore ER-III must originate in the spinal cord. Though Table I demonstrates a great similarity of quantitative characteristics of the ER-II in T3WR and L2WR there are some differences between these reactions, especially in their postactive alterations. The test ER-II (the ER-II evoked by a testing shock) in L2WR was suppressed to 40% of the control level within 50--100 msec interval after the conditioning ER-II (the ER-II evoked by a conditioning shock). But the amplitude of the testing ER-II in T3WR was less than the conditioning one by only a b o u t 8%, whereas the interval between them was 10 msec. The test response became identical in amplitude to the conditioning one after an interval greater than 15 msec. The ER-II in L2WR and T3WR differed from one another to some extent in their post-tetanic alterations. The ER-II in L2WR was more prominently augmented after 10 sec stimulation with 50 imp./sec frequency than after 300 imp./sec stimulation. The ER-II in T3WR behaves in an opposite fashion. Nevertheless, the time course in both cases was the same and was characterized by initial augmentation in the first 10--15 sec period after the end of the tetanization followed by a short inhibition of around 20--30 sec and then a second wave of augmentation lasting up to 1.5 min. Distinct post-tetanic alterations of ER-III were not observed. The data presented above demonstrate the c o m p o u n d nature of the ER which is seen to consist of mono- and polysynaptic components. It is possible that a similar organization of the ER is inherent in early somatosympathetic reflex responses in all thoracolumbar segments in which WR originate. At any rate, ER records with components identical to those described above were made earlier in T10WR. Unfortunately, the authors who published these records did not investigate these ER components [2]. According to many observations [ 5,6,8], normally single SPNs generate only one discharge during the ER. This fact enables us to suggest that certain ER c o m p o n e n t s are formed b y activation of different groups of SPNs, as follows from the investigation of the origin of the ER-I and the ER-II. It is also possible that different groups of SPNs, as described in the following paper [9], may have separate afferent inputs. Either of these t w o factors could make contributions to the c o m p o u n d ER organization. Obviously this question is of great interest and is the subject of our continuing investigations. REFERENCES 1 Coote, J.H. and Downman, C.B.B., Central pathways of some autonomic reflex discharges, J. Physiol. (Lond.), 183 (1966} 714--729.

323 2 Coote, J.H., Downman, C.B.B. and Weber, W., Reflex discharges into thoracic white rami elicited by somatic and visceral afferent excitation, J. Physiol. (Lond.), 202 (1960) 147--159. 3 Eccles, J.C., The action potential of the superior cervical ganglion, J. Physiol. (Lond.), 85 (1935) 179--206. 4 Fernandez de Molina, A., Kuno, M. and Perl, R., Antidromically evoked responses from sympathetic preganglionic neurones, J. Physiol. (Lond.), 180 (1965) 321--335. 5 J~nig, W. and Schmidt, R.F., Single unit responses in the cervical sympathetic trunk upon somatic nerve stimulation, Pfliigers Arch. ges. Physiol., 314 (1970) 199--216. 6 Kaufman, A. and Koizumi, K., Spontaneous and refex activity of single units in lumbar white rami. In F.F. Kao, M. Vassalle and K. Koizumi (Eds.), Research in Physiology. A liber memorialis in honor of Prof. C. McC. Brooks, Aulo Gaggi, Bologna, 1971, pp. 469--481. 7 Koizumi, K. and Brooks, C.McC., The integration of autonomic system reactions: a discussion of autonomic reflexes, their control and their association with somatic reactions, Ergebn. Physiol., 67 (1972) 1--68. 8 Lebedev, V.P., Some peculiarities of single sympathetic preganglionic neuron discharges in lateral horns of spinal cord elicited by antidromic and 0rthodromic stimulations. In P.G. Kostyuk and V.I. Skok (Eds.), Interneuronal Transmission in Autonomic Nervous System, Kiev, 1972, pp. 76--90 (in Russian). 9 Lebedev, V.P., Petrov, V.I. and Skobelev, V.A., Antidromic discharges of sympathetic preganglionic neurons located outside of spinal cord lateral horns, Neuroscience Letters, 2 (1976) 325--329. 10 Lebedev, V.P., Skobelev, V.A. and Bushmarina, T.A., Features of axons of sympathetic preganglionic neurons in cat lumbar spinal cord, Neirofiziologiya, 6 (1974) 143--151 (in Russian). 11 Lloyd, D.P.C., Neuron patterns controlling transmission of ipsilateral hind limb reflexes in cat, J. Neurophysiol., 6 (1943) 293--315. 12 Polosa, C., The silent period of sympathetic preganglionic neurons, Canad. J. Physiol. Pharmacol., 45 (1967) 1033--1046. 13 Sato, A. and Schmidt, R.F., Somato-sympathetic reflexes: afferent fibers, central pathways, discharge characteristics, Physiol. Rev., 53 (1973)916--947. 14 Sato, A., Tsushima, N. and Fujimori, B., Reflex potentials of lumbar sympathetic trunk with sciatic nerve stimulation in cats, Jap. J. Physiol., 15 (1965) 532--539.