Short communication RESPONSES OF RED NUCLEUS NEURONS TO PERIPHERAL STIMULATION IN CHLORALOSE ANESTHETIZED CATS. Janusz RAJKOWSKI
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1 ACTA NEUROBIOL. EXP : Short communication RESPONSES OF RED NUCLEUS NEURONS TO PERIPHERAL STIMULATION IN CHLORALOSE ANESTHETIZED CATS Janusz RAJKOWSKI Department of Neurophysiology, Nencki Institute of Experimental Biology, Pasteura 3, Warsaw, Poland Key words: red nucleus, unit activity, chloralose Abstract. Spontaneous and evoked activity of red nucleus neurons is described in chloralose anesthetized cats. It is suggested that some effects, e.g. burst discharges and prolonged inhibitory-excitatory responses, were induced by the use of chloralose. In chloralose anesthetized animals a prolonged modulation of neuronal activity through peripheral stimulation was recorded in various structures, i.e. red nucleus (RN) (8, ll), interpositus nucleus (IN) (2) and others (1, 4, 9). The aim of the present study was to investigate in more detail the influence of chloralose anesthesia upon cell activity in the somatosensory system. Experiments were performed on 25 cats anesthetized with alpha-chloralose (80 mglkg). The animals were paralysed with flaxedil and artificially ventilated. In three animals no relaxant was used to enable assessment of anesthetic depth (through observing paw withdrawal reflex, corneal reflexes, respiratory rate etc.). End-tidal C02 and body temperature were continuously monitored throughout the experiment. Three insulated steel needles exposed at the tip were inserted into the right (i.e. contralateral to the recording side) IN to test orthodromic responses of the RN neurons. In some cats the right rubrospinal tract was stimulated with bipolar electrodes at the C2 level to permit antidromic identification of RN cells. Nucleus interpositus and spinal cord stimulations were 6 - Acta Neurobiol. Exp. 2/42
2 carried out with single square pulses of 0.1 ms duration and current intensity of between PA. Both forelimbs and the right hindlimb were stimulated with single square pulses (0.5 ms; ma) delivered to the central footpad by a pair of subcutaneous needle electrodes. Extracellular single unit recordings from the left RN were performed with tungsten microelectrodes, inserted vertically. With exception of a few cases the recording began 4 h after surgery had been completed. An ANOPS laboratory computer was used to obtain interval histograms (IHs) for spontaneous activity, or poststimulus-time histograms (PSTHs) (32 stimulus presentations, 0.5, 1, or 2s scan length). At the end of the experiment, the position of the microelectrode was marked by electsocoagulation for later histological analysis. A sample of 285 units was analysed during these experiments. They represented a wide spectrum of resting discharge frequencies, ranging a d l int. e Fig. 1. Sample of red nucleus neuron activity: a, interval hi.stograms of eight spontaneously active neurons recorded in a single experiment; each histogram is expressed as a rough envelope of the original ANOPS recording (see inset); b and c, olscilloscopic recordings of a neuron with rhytmic background discharges (b) and burst activity (c); d-k, complete survey of PSTH patterns following footpad stimulation record,ed from different units in a single experiment (bin width 2 ms, stimulus onset a t zero time). Time from chloralose administration (in minutes): d, 180; e, 190; f, 320; g, 330; h, 500; i, 580; j, 620; k, 790.
3 from 0 to 1101s. In Fig. la sample IHs, recorded from 8 cells in a single experiment, are shown superimposed. About two-third of all the recorded neurons were spontaneously active, with an average rate of spikes 431s; the remaining neurons did not show any spontaneous activity. Typical responses of RN neurons to contralateral forelimb stimulation, expressed as facilitation or depression of the neuronal firing, were recorded in form of PSTHs (Fig. Id-k). Three most prominent features were distinguished in the responses: (i) a short-latency excitation, (ii) an inhibition and (iii) a long-latency, late excitation. The most typical patterns of responses are specified below; they represent different units and all of them could occur in any single experiment. The response pattern consisting of an early excitation alone occurred in of neurons (Fig. If), they were mostly the units that had no spontaneous activity. The two component (excitatory-inhibitory) response occurred in of Short-latency excitation Inhibition Long-latency excitation 10 e I units I Latency Duration ms Fig. 2. Response parameters of right red nucleus neurons to pad stimulation: a-e, latency and f-j, duration of each of three components (early excitation, inhibition, late excitation). All histograms are related to the left forelimb stimulation, except for b and g, right forelimb, and c and h, right hindlimb. Because of stimulus site unspecificity the late components evoked from only one leg are presented.
4 neurons (Fig. le and g). The majority of recorded units (44"/o) responded with a late burst of activity (Fig. ld and h-k). In most of belonging to that group spontaneously active units, the response pattern consisted of a short-latency burst, an inhibition and a long-latency burst (Fig. li), often followed by later, less pronounced, modulation in discharge frequency. On the other hand, in neurons lacking background activity the response appeared in form of an early and late excitation (Fig. lj), or sometimes a late excitation alone. Additionally. in 4OIo of all the recorded neurons inhibition was found as the only response. Also other, less pronounced forms of responses could be distinguished. From each histogram recorded in the experiments, the latency and duration of each response component were measured. The distributions of these response parameters, comprising all the units recorded, are presented in Fig. 2. The receptive field of most units was wide, involving the whole body, and only in 18O/o of cells was the receptive field restricted to one leg. Stimulation of different legs resulted in significant differences only between t'le latencies of the early excitation, and the late components were essentially unchanged when altering the stimulation site. Moreover, the response patterns of different RN units, even spatially distant ones, were almost identical, when recorded close in time (see 11). Although somatosensory stimulation was most frequently employed alone, other stimulus modalities (acoustic or visual) were also checked, and those evoked essentially similar response patterns. Moreover, stimulation of the contralateral IN which typically elicited a monosynaptic excitation, was also followed in 46O/o of neurons by a late response, composed of inhibition and subsequent excitation (see also 10). It seems that differences between the characteristics of these responses reflect only different stimulus effectiveness. Each experiment could be characterized according to the predominant pattern of spontaneous activity and the predominant response pattern. These two characteristics were found to be correlated with each other which is expressed in the following classification: in 4 experiments no activity was recorded except for injury potentials; in 5 preparations with low background activity, only short-latency excitations could be evoked; in 6 preparations showing regular spontaneous discharges, the cells responded to stimulation with an excitatory-inhibitory pattern; in 10 cats the neurons displayed usually bursts in their spontaneous activity, with irregular and long-lasting interburst intervals, and in these experiments the long-latency excitatory response prevailed over the other patterns of responses. The background activity was changing throughout the experimental session. Unfortunately, that aspect was investigated casually and docu-
5 mented in form of oscilloscope recording - allowing only for some general remarks to be made here. The changes could be traced only in those recording sessions which lasted at least 8h. At the begining of the experiment, a few hours after chloralose administration most cells were silent and they responded only to peripheral stimulation or discharged in consequence of injury of the neuron. These neurons which were spontaneously active, had a tendency to fire with long and rather regular intervals (Fig. lb). However, several hours after injection of the anesthetic the neuronal activity had changed: the number of spontaneously active neurons increased and they began to discharge with high frequency bursts (Fig. lc). The changes in spontaneous activity throughout the experiment were parallelled by changes in pattern of response. Figure Id-k presents a complete survey of PSTH patterns recorded from different neurons in a single experiment. Typically, 4 to 8 h after the injection of the anesthetic the responses consisted of a simple early excitation (Fig. If), or an early excitation followed by a long-lasting inhibition (Fig. le and g). Later, 6 to 12 h after administration of chloralose, the long-lasting, longlatency secondary excitation appeared (Fig. 1 i-k). Still later, from the begining of the experiment, both inhibition and late excitation shortened and subsequent bursts occured (Fig. lk). The described typical patterns of responses fit well with the similar results of other authors, concerning RN (8). This pattern of RN activity is a precise reproduction of that existing in IN (3, and our own, unpublished observations), which is expected in light of the known relationships that exist between the two structures (12). An activity described in this and in the other cited papers is characterized by some very specific features: (i) spontaneous activity occurs in bursts, (ii) response forms characteristic response pattern with prolonged inhibitory-excitatory sequence ard (iii) the reaction involves numerous brain stem neurons in a synchronized manner (11). All these features seem typical for chloralose preparation, as opposed to some other experimental conditions (e.g. under barbiturates, our own observation). However it should be noted here, that spontaneous burst activity or late burst responses were also observed in other preparations (5, 7). Additionally, it was observed that both the spontaneous activity pattern and the response pettern changed with time after induction of chloralose, thus these patterns can be related to the assessed depth of anesthesia. "Profound" anesthesia resulted in suppression of both the spontaneous activity and the response to stimulation. "Deep" anesthesia was characterized by regular background activity and short-latency excitatory or excitatory-inhibitory response. Spontaneous burst activity
6 and all the response patterns with late burst can be considered as typical for "moderate" anesthesia. "Light" anesthesia was marked by the shortening of spontaneous bursts and shortening of excitatory-inhibitory-exc~tatory complex. It is our suggestion that different patterns characterize different anesthesia levels, rather than other factors which may influence the response. This assumption is based on results of our previous experiments (ll), when the reverse process was observed, i.e. the typical chloralose neuronal activity, characterized by spontaneous burst activity and excitatory-inhibitory-excitatory response, developed in consequence of chloralose injection. Although it has been suggested that similar compound responses occur in unanesthetized animals (8), our further observations (in preparation), and also experiments of Armstrong concerning IN (2, 3) show that there are significant differences in realctivity between normal and chloralose preparation. Response to somatcrsensory stimuli in unanesthetized cats is characterized by short and labile activity-inactivity sequence and small receptive field, whereas in the cat under chloralose it appears in characteristically generalized form. In conclusion, the observed characteristic compound and long-lasting reactions of RN neurons could be interpreted as a consequence of chloralose anesthesia. This investigation was supported by Project of the Polish Academy of Sciences. 1. ALBE-FESSARD, D. and KRUGER, L Duality of unit discharges from cat centrum medianum im response to natural and electnic stimulation. J. Neurophysiol. 25: ARMSTRONG, D. M., COGDELL, B. and HARVEY, R. J Effects of afferent volleys from the limbs on the discharge patterns of interpositus neurons in the cats anaesthetized with alpha-chlorelose. J. Physiol. 248: 48961'7. 3. ARMSTRONG, D. M. and RAWNSON, J. A Responses of neurons in nucleus interpositus of the cerebellum to cutaneous nerve volleys in the awake cat. J. Physiol. 289: BACH-Y-RITA, P Convergent and long-latency unit responses in the rebicular formation of the cat. Exp. Neurol. 9: FAINGOLD, C. L Enhancement of mesencephalic reticular neuronal respanses to sensory stimuli with pentylenetetrazol. Neuropharmacology 19: GOODMAN, S. J. and MANN, E. G. 1967, Reticular and thalamic multiple unit activity dufiing wakefulnes~s, sleep and anesthesia. Exp. Neurol. 19: KAYAMA, Y. and IWAMA, K The EEG, evoked potential, and singleunit activity during ketamine anesthesia in cats. Anesthesiology 36: MASSION, J. and ALBE-FESSARD, D Dualit6 des voies sensorielles affhrents controlant l'activit6 du noyau rouge. ~lectroencephalgr. Clin. Neurophysiol. 15:
7 9. MASSION, J., ANGAUT, P. and ALBE-FESSARD, D Activites evoquees chez le chat dans la region du muoleus ventralis lateralis par diverses stimulations sensorielles. I. Etude macro-physiologique. Electroencephalogr. Clin. Neurophysiol. 19: RAJKOWSKI, J. and TARNECKI, R Interaction of peripheral and cerebellar inputs to red nucleus neurms. Acta Neurobiol. Exp. 39: RAJKOWSKI, J The influence of chloralose anesthesia on the activity of red nucleus neurons in cats. Acta Neurobiol. Exp. 40: TOYAMA, K., TSUKAHARA, N. and UDO, M Nature of the cerebellar ~nfluences upon the red nucleus neurones. Exp. Brain Res. 4: Accepted 10 October 1981
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