Synaptic processes in neurons of the cervical enlargement of the cat spinal cord during stimulation of propriospinal pathways of the dorsolateral tract

Responses of motoneurons and interneurons of the cervical enlargement of the cat spinal cord were studied by a microelectrode technique during selective stimulation of propriospinal fibers of the dorsolateral tract of the lateral white column. The long descending and ascending pathways were blocked by preliminary (10–16 days earlier) hemisection of the spinal cord cranially and caudally to the segments studied. Stimulation of the dorsolateral tract at a distance of 15–25 mm from the site of recording evoked complex postsynaptic potentials consisting of several successive waves in the motoneurons. The character of the PSPs was not clearly linked with the function of the motoneurons. By their latent periods the components of the PSPs could be placed in three groups. The "primary" components were reproduced in response to stimulation at 50–100/sec whereas the "secondary" and "tertiary" components were weakened or blocked. It is postulated that the "primary" components are evoked through monosynaptic connections between propriospinal fibers of the dorsolateral tract and motoneurons of the forelimb muscles, while the late components are evoked through polysynaptic pathways, including segmental interneurons. Many of these interneurons, located in the ventral horn and intermediate zone, were strongly excited during stimulation of the dorsolateral tract.A. A. Bogomolets' Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 5, No. 1, pp. 61–69, January–February, 1973.     

Postsynaptic effects evoked by activation of long propriospinal pathways in cervical spinal neurons in cats

Effects induced in motoneurons and interneurons of the cervical enlargements of the cat spinal cord by stimulation of the lateral and ventral funiculi at the lower thoracic level were studied under conditions producing degeneration of fibers of descending brain systems. Stimulation of this sort evoked PSPs (mainly of mixed character) in 57 of 90 motoneurons tested. In nine motoneurons the primary response consisted of monosynaptic EPSPs evoked by activity of fibers of the lateral funiculus, and in the rest it consisted of polysyanptic (at least disynaptic) EPSPs and IPSPs. Polysynaptic effects arising in the neuron in response to stimulation of the lateral and ventral funiculi usually differed only quantitatively. The intensity of excitatory synaptic action on motoneurons of the proximal muscle (especially thoracid) was much greater than that on motoneurons of distal muscles. Nearly all motoneurons with no synaptic action belonged to the latter group. Stimulation of the lateral and ventral funculi facilitated synaptic action induced in motoneurons by stimulation of high-threshold segmental afferents and led to excitation of interneurons located in the vectral quadrant, and had no effect on interneurons in the dorsal regions of gray matter. These effects are regarded mainly as the result of excitation of long ascending propriospinal pathways in the cervical parts of the cord; it is also postulated that some of them are evoked by the arrival of activity along collaterals of descending propiospinal pathways to the neurons in this region.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 11, No. 4, pp. 339–347, July–August, 1979.     

Pyramidal and extrapyramidal synaptic effects upon chronically deafferented motoneurons of the spinal cord of a cat

By means of intracellular recording technique, studies have been made of the electrical activity of -motoneurons of the seventh lumbar segment in cats with chronic rhizotomy of the dorsal root fibers (L₄-S₂). Postsynaptic potentials of the reticular formation of the midbrain, medulla, and ventral columns of the spinal cord were compared with the reactions recorded from nonoperated animals; these potentials were evoked by stimulation of the motor cortex, red nucleus, and Deuters' nuclei. Deafferentiation did not cause statistically reliable variations in the amplitude of the descending monosynaptic E PSPs. Extrapyramidal short-latent disynaptic E PSPs and IPSPs remained also practically unchanged, while the responses of deafferented motoneurons to cortico-spinal impulses were considerably facilitated; this effect was retained in pyramidal cats. Deafferentation was not accompanied by variations in the dependence of the discharge frequency on the depolarizing current strength or by the variation in the threshold and input resistance of the motoneuron membranes. This suggests that intensification of the pyramidal synaptic action upon deafferented motoneurons was caused by the variation on the intermediate neuronal level.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 1, No. 1, pp. 35–46, July–August, 1969.     

Functional properties of propriospinal pathways of the dorsolateral tract of the cat spinal cord

The characteristics of conduction of the excitation wave along propriospinal fibers of the dorsolateral tract of the spinal cord were studied in cats anesthetized with pentobarbital. At a preliminary operation, 10–18 days beforehand, lateral hemisection of the spinal cord was performed, cranially in the lumbar division and caudally and cranially in the cervical division to the segments to be studied, leading to degeneration of the long descending and ascending fibers. During stimulation, the dorsolateral tract developed a composite response consisting of a positive-negative wave recorded up to 60–65 mm (4 or 5 segments) from the point of stimulation. The mean conduction velocity of this wave in the lumbar division was 37.9 m/sec compared with 44.5 m/sec in the cervical division. From its properties as a whole this wave can be regarded as the result of excitation of relatively fast-conducting propriospinal fibers of the dorsolateral tract. If the strength of stimulation was increased, late components began to appear in the response. These were evidently connected with excitation of thinner propriospinal fibers and synaptic activation of other other groups of spinal neurons.A. A. Bogomolets' Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 5, No. 1, pp. 54–60, January–February, 1973.     

Synaptic activation of thoracic spinal interneurons by reticulospinal pathways

Synaptic processes of 119 thoracic spinal interneurons (T10–11) were investigated in anesthetized cats in response to stimulation of the medial and central zones of the gigantocellular nucleus in the medulla and the ventral columns of the spinal cord. Fast (90–130 m/sec) reticulospinal fibers running in the ventral column were found to produce monosynaptic or disynaptic excitation of interneurons of Rexed's layers VII–VIII, which are connected monosynaptically with group I muscle afferents, and interneurons excited both by group I muscle afferents and low-threshold cutaneous afferents. In most neurons of layer IV, connected monosynaptically with low-threshold cutaneous afferents, and in neurons of layers VII–VIII excited by afferents of the flexor reflex no marked postsynaptic processes were observed during stimulation of the reticular formation. Excitatory, inhibitory, and mixed PS Ps during activation of reticulospinal fibers were found in 14 neurons, high-threshold afferents in which evoked predominantly polysynaptic IPSPs. Seventeen neurons activated monosynaptically by reticulospinal fibers and not responding to stimulation of segmental afferents were found in the medial part of the ventral horn (layers VII–VIII).A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 4, No. 6, pp. 566–578, November–December, 1972.     

Corticofugal influences on reticulospinal neurons of the gigantocellular nucleus in cats

It was shown by intracellular recording that stimulation of the motor cortex evokes E PS Ps and I PS Ps in reticulospinal neurons of the gigantocellular nucleus of the cat medulla. The E PS Ps appeared in 94.3% and the I PS Ps in 5.7% of neurons tested. Analysis of the presynaptic pathway showed that 77.4% of E PS Ps studied arose through monosynaptic, and 22.6% through polysynaptic corticoreticular connections. By their latent period, duration, and rise time up to a maximum the monosynaptic E PS Ps were divided into two groups: "fast" and "slow." It is postulated that "fast" E PS Ps are generated in reticulospinal neurons which are activated by fast-conducting fibers and "slow" E PS Ps by slowly conducting corticobulbar fibers. I PS Ps were recorded from reticulospinal neurons that also were inhibited by stimulation of the ventral columns of the spinal cord. The hypothesis is put forward that cortical motor signals in cats can be transmitted to the spinal cord via monosynaptic and polysynaptic connections of "fast" and "slow" pyramidal neurons with reticulospinal neurons.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 8, No. 3, pp. 250–257, May–June, 1976.     

Synaptic effects evoked in motoneurons by stimulation of single propriospinal neurons

Experiments on cats with simultaneous extracellular recording, stimulation of single propriospinal neurons, and intracellular recording of unitary postsynaptic potentials from motoneurons, followed by computer averaging showed that direct stimulation of individual propriospinal cells receiving mono- and disynaptic influences from the medial reticular formation can evoke monosynaptic EPSPs and IPSPs in lower lumbar motoneurons. The amplitude of these EPSPs was 49.6±6.0 and of the IPSPs 28.9±2.9 µV and their synaptic delay was 0.34±0.05 msec. The same propriospinal neuron of the ventral horn of the upper lumbar segments may be connected with several motoneurons of the hind limb muscles.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 9, No. 3, pp. 300–306, May–June, 1977.     

Reticulofugal influences of interneurons in the lateral region of gray matter of the cat spinal cord

Responses of lumbar interneurons located in the most lateral regions of Rexed's laminae IV–VII to stimulation of the medial longitudinal bundle and gigantocellular reticular nucleus of medullary pyramids, red nucleus, and peripheral nerves were investigated in cats anesthetized with pentobarbital. Stimulation of the reticulospinal fibers evoked monosynaptic excitation of many interneurons specialized for transmitting activity of the lateral descending systems, but not of peripheral afferents. Convergence of excitatory influences of all three descending systems (cortico-, rubro-, and reticulospinal) was observed on some cells of this group. In addition, monosynaptic "reticular" E PSPs appeared in interneurons transmitting activity of group Ia muscle fibers and in some interneurons of the flexor reflex afferent system. Stimulation of reticulospinal fibers evoked IPSPs in some neurons of this last group. Neurons not exposed to reticulofugal influences (both specialized neurons and interneurons of segmental reflex arcs) were located chiefly in the dorsal zones of the region studied. Recordings were also obtained from single fibers of the lateral reticulospinal tracts (conduction velocity from 26 to 81 m/sec).A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 5, No. 5, pp. 525–536, September–October, 1973.     

Activity of propriospinal neurons in segments C3 and C4 during fictitious locomotion in cats

Activity of propriospinal neurons in segments C3 and C4 was recorded in immobilized decerebrate cats, whose spinal cord was divided at the lower thoracic level, during locomotor activity of neuronal mechanisms controlling the forelimbs (fictitious locomotion of the forelimbs). Neurons were identified according to antidromic responses to stimulation of the lateral column of the spinal cord at level C6. Antidromic responses also appeared in 70% of these neurons to stimulation of the medullary lateral reticular nucleus. During fictitious locomotion, i.e., in the absence of afferent signals from the limb receptors, rhythmic modulation of the discharge of most neurons was observed, correlating with activity of motoneurons. If the rostral region of the cervical enlargement of the spinal cord was cooled, causing generation of the locomotor rhythm to cease, rhythmic activity of propriospinal neurons in segments C3 and C4 also ceased. The main source of modulation of activity of propriospinal neurons in segments C3 and C4 is thus the central spinal mechanisms controlling activity of the forelimbs.Institute for Problems in Information Transmission, Academy of Sciences of the USSR, Moscow. M. V. Lomonosov Moscow University. Translated from Neirofiziologiya, Vol. 17, No. 3, pp. 320–326, May–June, 1985.     

Analysis of Combined Action of Antagonists of Excitatory and Inhibitory Amino Acids on Motoneuron Postsynaptic Potentials of the Frog Rana ridibunda

The effect of blockers of excitatory and inhibitory amino acid receptors on postsynaptic potentials (PSP) evoked by activation of three synaptic inputs of the lumbar motoneuron (stimulation of the dorsal root, reticular formation, ventral and lateral columns) was studied on preparation of the isolated spinal cord of the frog Rana ridibunda. It has been shown that sensitivity of PSP to antagonists differs in different motoneurons, in the same motoneuron at activation of different inputs, and in the same input in different PSP components. It has been found that many descendent (DC) PSPs resistant to kynurenate or CNQX [1] were inhibited by blockers of inhibitory receptors. In this case the early component of DC-PSP varied considerably by amplitude and changed its polarity from positive to negative on the background of a low transmembrane depolarizing current. These changes were absent under conditions of replacement of chlorine ion by sulfate in the perfusion solution or treatment of the spinal cord with a blocker of inhibitory amino acids. All this allows suggesting that these DC-PSPs or their components were inhibitory. A part of PSPs resistant to kynurenate and CNQX were also resistant to the blockers of inhibitory amino acids (strychnine, picrotoxin, and bicuculline). In some cases, as a result of treatment with convulsants, the same blockers of excitatory receptors inhibited the initially resistant PSPs.     

Synaptic organization of supraspinal control over propriospinal ventral horn interneurons in cat and monkey spinal cord

Synaptic responses evoked in propriospinal neurons of the upper lumbar segments (L₃–L₄) by reticulo-, vestibulo-, and corticospinal impulses were studied in experiments on cats and monkeys. Propriospinal cells, identified by antidromic stimulation, were stained with Procion red, so that they could be localized in the different zones of the ventral horn. Monosynaptic reticular and vestibular excitatory influences were discovered in cats; convergence of these influences on the same neurons was demonstrated. In monkeys bulbospinal monosynaptic effects were supplemented by monosynaptic influences arriving from the motor cortex; convergence of monosynaptic excitatory influences from all supraspinal sources studied was found on some propriospinal neurons. The propriospinal neurons studied also had synaptic inputs from primary afferents.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 9, No. 2, pp. 177–184, March–April, 1977.     

Synaptic effects evoked by supraspinal and intraspinal stimulation in lamprey motoneurons

In experiments onLampetra fluviatilis in response to electrical stimulation of bulbar reticulospinal neurons and descending fibers the postsynaptic potentials of segmental motoneurons and action potentials of single intraspinal axons were recorded intracellularly and the cord dorsum potentials were recorded by a surface electrode. Fast-conducting reticulospinal axons (Müller's axons) were shown to excite spinal motoneurons monosynaptically. Monosynaptic reticulo-motoneuronal EPSPs arise as the result of excitation of a limited number of descending fibers, they reproduce high frequencies of stimulation readily and, in some cases, they are divided into components of which the first may be attributed to an electrical, and the second to a chemical mechanism of transmission. Besides early monosynaptic EPSPs, late, probably polysynaptic, responses also are found.     

Cortico-pyramidal and cortico-extrapyramidal synaptic influences on lumbar motoneurons in monkeys

Postsynaptic potentials evoked by stimulation of the motor cortex or pyramids before and after acute pyramidotomy were investigated in the lumbar motoneurons of monkeys. In response to activation of fibers of the pyramidal tract monosynaptic EPSPs predominated in motoneurons innervating the distal muscles of the hind limbs. Monosynaptic EPSPs in the motoneurons of the distal muscles had a significantly higher amplitude and could be evoked by weaker stimuli than EPSPs in the motoneurons of the proximal muscles. Cortico-motoneuronal EPSPs in the motoneurons of the distal muscles had a less marked frequency potentiation than EPSPs with monosynaptic segmental delay in the motoneurons of the proximal muscles. Cortico-extrapyramidal synaptic responses appeared in the pyramidotomized monkeys during intensive repetitive stimulation of the motor cortex in motoneurons of both distal and proximal muscles. These effects, transmitted by descending projections of the brain stem, may be responsible for the partial preservation of cortical motor control after pyramidotomy.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 4, No. 6, pp. 587–596, November–December, 1972.     

Evoked activity of spinal neurons in the early period after sciatic nerve division

The character of dorsal horn motoneurons and interneurons evoked by stimulation of the dorsal root, and activity of Renshaw cells in response to stimulation of the ventral root were studied in albino rats in the lower lumbar segments of the spinal cord 5 days after sciatic nerve division. A significant increase in the mean amplitude of excitatory postsynaptic potentials of motoneurons was observed on the side of division of the nerve. No significant change in membrane potential and in the threshold of appearance of the action potential of these motoneurons took place. The mean number of action potentials and the duration of discharge of the Renshaw cells and dorsal horn interneurons likewise were not significantly changed.Dnepropetrovsk Medical Institute, Ukrainian Ministry of Health. Translated from Neirofiziologiya, Vol. 24, No. 3, pp. 306–314, May–June, 1992.     

Electrotonic and chemical EPSPs evoked in lamprey motoneurons by descending tract and dorsal root afferent stimulation

Postsynaptic responses evoked by stimulation of the descending tract and dorsal roots were investigated by means of intracellular microelectrodes in experiments on preparation of the isolated lamprey spinal cord. Besides giant reticulospinal (Mullerian) axons, a broad spectrum of descending fibers and dorsal-root afferents were shown to form synaptic inputs with both chemical and electrical mechanisms of transmission with motoneurons, as revealed by the sensitivity of the corresponding PSPs to absence of calcium ions and excess of magnesium ions in the external medium. During combined stimulation electrotonic PSPs may have a rapid temporal course characteristic of elementary responses, but they may also lead to smooth and slow depolarization of the postsynaptic membrane, evidence that they may perform not only a mediator but also an integrative function.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 9, No. 5, pp. 512–517, September–October, 1977.     

Primary afferent depolarization due to selective activation of propriospinal pathways

Depolarization of primary afferent terminals in the lumbosacral portion of the spinal cord evoked by selective activation of propriospinal pathways was investigated in anesthetized cats. The strongest depolarization developed as a result of activation of short (two to five segments) propriospinal pathways in the lateral funiculus; stimulation of the long propriospinal pathways of this funiculus also induced depolarization, but of lower amplitude. Stimulation of propriospinal pathways of the ventral funiculi was ineffective. Significant primary afferent depolarization developed only following the use of a series of stimuli and strong stimulation of the propriospinal pathways. Excitation of these pathways caused depolarization of afferent terminals of both cutaneous and muscular nerves, including muscular sensory fibers of group Ia, although in the latter case its intensity was low. Neuronal mechanisms involved in the generation of this depolarization and its possible functional role are dicussed.     

Synaptic links of propriospinal neurons of the lumbar section of the cat spinal cord

The distribution of propriospinal fiber terminals of the lateral funiculus in the lumbar segments of the cat spinal cord was examined by light and electron microscopy. For the selective demonstration of these terminals, preliminary hemisectioning of the brain at the boundary of the thoracic and lumbar segment, eliminating all the long descending pathways, and subsequent hemisectioning or sectioning of the lateral funiculus at the level of the third lumbar segment was carried out. It was established by staining the degenerating endings (by the Fink—Heimer method) that the terminals of the descending and ascending propriospinal fibers, which form part of the lateral and ventral funiculi, are located mainly in the lateral and medial parts of lamina VII and the dorsal section of lamina VIII, according to Rexed, as well as in the regions adjacent to the dorsolateral and ventromedial motor nuclei. A large number of these terminals is found in the corresponding regions of the gray matter on the contralateral side of the brain. Since, in the case of selective injury of the lateral funiculus the number of degenerating terminals in lamina VIII is noticeably decreased, it can be assumed that the propriospinal neuron terminals of the ventral funiculus are concentrated mainly in lamina VIII. The axons of the propriospinal neurons extend over several segments both in the ascending and in the descending directions. It was shown in an electron microscopic study of the regions in which most of the propriospinal terminals are located that these terminals are of an axo-dendritic nature and terminate in the dendrites of both inter- and motor neurons. Their degeneration can be of the "light" or "dark" type.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR. Translated from Neirofiziologiya, Vol. 3, No. 4, pp. 401–407, July–August, 1971.     

Inhibitory effects of reticulospinal fibers of the lateral funiculus on neurons of thoracic spinal reflex pathways

Experiments on anesthetized cats with partial transection of the spinal cord showed that reticulo-spinal fibers in the ventral part of the lateral funiculus participate in the inhibition of polysynaptic reflexes evoked by stimulation of the ipsi- and contralateral reticular formation. The reticulo-fugal wave in the ventrolateral funiculus evoked comparatively short (up to 70 msec) IPSPs in some motoneurons of the internal intercostal nerve investigated and at the same time evoked prolonged (up to 500 msec) inhibition of IPSPs caused by activation of high-threshold segmental afferents. This wave also led to the appearance of IPSPs in 14 of 91 (15.5 %) thoracic spinal interneurons studied. The duration of these IPSPs did not exceed 100 msec; meanwhile, segment excitatory responses of 21 of 43 interneurons remained partly suppressed for 120–500 msec. It is concluded that the inhibitory action of the lateral reticulo-spinal system on segmental reflexes is due to several synaptic mechanisms, some of them unconnected with hyperpolarization of spinal neurons. The possible types of mechanisms of this inhibition are discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 10, No. 2, pp. 162–172, March–April, 1978.     

Immunohistochemical study on the distribution of serotonin fibers in the spinal cord of the dog

Summary Distribution of serotonin fibers in the spinal cord of the dog was investigated by means of a modified PAP method; a rabbit anti-serotonin serum prepared in the laboratory of the authors was used in this study. Serotonin fibers were revealed as PAP-positive dark-brown elements displaying dot-like varicosities (0.5–2.0 m in diameter). In the spinal cord of the dog, the distribution of serotonin fibers is extensive. These fibers occur more densely in more caudal segments and are most prominent at the sacrococcygeal level. From the level of the cervical spinal cord to the upper lumbar region, the descending serotonin fibers are located immediately under the pia mater in the ventrolateral portion of the lateral funiculus. In more caudal segments, serotonin fibers are dispersed throughout the ventral and lateral funiculi. These longitudinal en passage-fibers send numerous transverse collaterals to the gray matter. Serotonin fibers are distributed abundantly in the laminae I and III of the posterior column, while only a few fibers are found in the lamina II (substantia gelatinosa). In the intermediate zone, two descending serotonin pathways, i.e., lateral and medial longitudinal bundles, are observed to coincide topographically with the nucleus intermediolateralis at C8(T1)-L3(L4) and the nucleus intermediomedialis at C1-Co respectively. The former is particularly prominent and communicates with the contralateral bundle via commissural bundles at intervals of 300–500 m. The large motoneurons in the anterior column, especially those in the nucleus myorabdoticus lateralis within the cervical and lumbar enlargements, are closely surrounded by fine networks of serotonin fibers and terminals.Supported by a grant (No. 56440022) from the Ministry of Education, Science and Culture, Japan     

Responses of motor neurons of lumbar section of spinal cord elicited by the activity of the propriospinal pathways

We have carried out intracellular recording from the motor neurons of the lumbar section of the cat spinal cord with electrical stimulation of the propriospinal axons descending in the dorsolateral funiculus. To prevent activation of the long descending pathways of the lateral funiculus, ipsilateral hemisectioning of the spine was performed in the segments L₁-L₂ 10–14 days before the experiment. Stimulation of the dorsolateral funiculus in two segments cranial to the point of recording elicited in the flexor motor neurons essentially e.p.s.p. and in the extensor neurons i.p.s.p. with a latent period, on the average, of 1.97 and 1.93 msec, respectively. The amplitude of such p.s.p. considerably rose with rise in the frequency of stimulation of the funiculus to 50–100 a second. Activation of the segmental interneurons was observed only in a few cases. It is assumed that the synaptic processes elicited in the lumbar motor neurons are the result of the monosynaptic influences of the propriospinal neurons.A. A. Bogomolets' Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 1, No. 1, pp. 5–14, July–August, 1969.