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.     

Cortico- and rubrofugal activation of interneurons forming the propriospinal pathways of the dorsolateral funiculus of the cat spinal cord

Interneurons of the lumbar division of the cat spinal cord responding after a short latent period with intensive excitation to stimulation of the medullary pyramids and red nucleus but not responding (or excited after a long latent period) to stimulation of peripheral nerves were investigated by microelectrode recording. Most of these neurons, located in the lateral zones of Rexed's laminae IV–VII of the gray matter, were identified as propriospinal cells sending axons into the dorsolateral funiculus of the white matter (mean velocity of antidromic conduction in the group 34.6 m/sec). Marked convergence of corticofugal and rubrofugal excitatory influences was found on the overwhelming majority of neurons. Some neurons were activated monosynaptically by fast-conducting fibers of both descending systems. The minimal and mean values of the latent periods of the pyramidal EPSPs for the neurons tested were 4.5 and 6.28 msec, and for the rubral EPSPs 3.3 and 4.94 msec respectively. A distinguishing feature of the activation of these neurons is the intensive potentiation of their synaptic action on the arrival of a series of corticofugal and rubrofugal waves.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 4, No. 5, pp. 489–500, September–October, 1972.     

Spatial distribution of descending propriospinal tract neurons in the cat spinal cord

Quantitative estimates of the density of distribution of interneurons forming descending intersegmental connections in the cat spinal cord were obtained. Neurons were labeled by retrograde axonal transport of horseradish peroxidase injected unilaterally at different segmental levels. The mean number of labeled units per section 50 µ thick, in a given zone, was used as the measure of density. The density of distribution of the propriospinal neurons forming the longest tracts between the cervical and lumbosacral regions of the cord was found to be about half the density of distribution of neurons with short (not more than two segments) axons, and to be several times less than the corresponding value for neurons with axons of intermediate length. No marked local peaks of density of distribution of long-axon neurons were found at the level of the brachial enlargement. The number of neurons with crossed axons in most segments was close to half of the total number of propriospinal units. Zones of transverse section of the spinal cord with maximal concentrations of neurons forming direct and crossed propriospinal tracts of different lengths were determined at different levels. Correlation between the quantitative composition of propriospinal neuron populations with characteristics of influences transmitted by these populations is examined.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 16, No. 1, pp. 96–105, January–February, 1984.     

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.     

Experimental morphological study of endings of propriospinal fibers of the lateral funiculus in the cat cervical spinal cord

The distribution and ultrastructure of terminals of the propriospinal fibers of the lateral funiculus in the cervical segments of the cat spinal cord were studied by the experimental degeneration method. A preliminary lateral hemisection of the spinal cord was carried out 5–6 months earlier at the level of segments C2 or C3 to destroy all the long descending pathways; the lateral funiculus was then divided at the level of C4 or C5. It was shown by the method of Fink and Heimer that terminals of descending and ascending propriospinal pathways damaged by the second division are distributed in the gray matter ipsilaterally in the lateral zones of Rexed's laminase V–VII and also in the dorsolateral motor nuclei. An electron-microscopic study showed that the synapses of the degenerating terminals are mainly axo-dendritic in type and account for 14.5% of the total number of terminals counted. Residual synaptic vesicles in these terminals were spherical in shape. The mean diameter of the degenerating myelinated propriospinal fibers in the lateral funiculus was 10±3 µ. The results of this investigation were compared with those of electrophysiological investigations of the function of propriospinal neurons.     

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.     

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.     

Synaptic connections of fibers of the rubrospinal tract in the cat spinal cord

The ultrastructure of the lateral part of laminae VI and VII of the spinal gray matter (the location of most of the terminal branches of the rubrospinal tract) was investigated in cats under normal conditions and at various times after destruction of the red nucleus. The neuron population of this region is formed by cells fairly homogeneous in size (25–40µ). The structure of the dendritic profiles is simple and they carry only infrequent and small membranous appendages. Most synapses are axo-dendritic. The axon terminals are divided into three groups depending on the size and shape of the synaptic vesicles and the presence of post-synaptic specialization. A few glomerular axon terminals contacting with various structures are found. Small axon terminals located chiefly on dendrites and their appendages show degenerative changes 1–8 days after destruction of the red nucleus. As a rule the degenerating terminals contain round synaptic vesicles. The glomerular terminals do not degenerate.A. A. Bogomol'ets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 6, No. 6, pp. 610–618, November–December, 1974.     

Convergence of forelimb afferent actions on C7-Th1 propriospinal neurones bilaterally projecting to sacral segments of the cat spinal cord

Propriospinal neurones located in the cervical enlargement and projecting bilaterally to sacral segments of the spinal cord were investigated electrophysiologically in eleven deeply anaesthetized cats. Excitatory or inhibitory postsynaptic potentials from forelimb afferents were recorded following stimulation of deep radial (DR), superficial radial (SR), median (Med) and ulnar (Uln) nerves. 26 cells were recorded from C7, 22 from C8 and 3 from Th1 segments. The majority of the cells were located in the Rexed's laminae VIII and the medial part of the lamina VII. In 10 cases no afferent input from the forelimb afferents was found. In the remaining neurones effects were evoked mostly from DR (88%) and Med (63%), less often from SR (46%) and Uln (46%). Inhibitory actions were more frequent than excitatory. The highest number of IPSPs was evoked from high threshold flexor reflex afferents (FRA)--all connections were polysynaptic. However, inhibitory actions were often evoked from group I or II muscle afferents (polysynaptic or disynaptic) and, less frequently, from cutaneous afferents (mostly polysynaptic). Di- or polysynaptic IPSPs often accompanied monosynaptic EPSPs from group I or II muscle afferents. Disynaptic or polysynaptic EPSPs from muscle and cutaneous afferents were also recorded in many neurones, while polysynaptic EPSPs from FRA were observed only exceptionally. Various patterns of convergence in individual neuronal subpopulations indicate that they integrate different types of the afferent input from various muscle and cutaneous receptors of the distal forelimb. They transmit this information to motor centers controlling hind limb muscles, forming a part of the system contributing to the process of coordination of movements of fore--and hind--limbs.     

离体培养的小鼠脊髓固有神经元的突触构筑

An electron microscopic analysis of the synaptic architecture in propriospinal neurons of cultured fetal mouse spinal cord has been undertaken. The size of the perikarya in the cultured spinal cord represents a range from small- to medium sized neurons, which form many synapses each other. There are many axo-dendritic and axo-somatic synapses in the culture but direct dendro-dendritic apposition is rarely seen. Four morphological types of synaptic boutons, S, F, M and G are classified according to criteria used by previous investigators. The ultrastructural details available suggest that the propriospinal neurons receive synaptic input from propriospinal fibers through simple synapses. It may indicate that their impulses can be controlled only postsynaptically.     

Mapping of tachykinins in the cat spinal cord

Using an indirect immunoperoxidase technique, the location of cell bodies and fibers containing substance P, neurokinin A and neurokinin B was studied in the cat spinal cord. The former two neuropeptides showed a widespread distribution throughout the whole spinal cord, whereas the distribution of neurokinin B was more restricted. Neurokinin A-immunoreactive structures showed a more widespread distribution and a higher density than the immunoreactive structures observed to contain substance P. In the cat spinal cord, we observed cell bodies containing neurokinin A, but no cell bodies containing neurokinin B or substance P were found. These cell bodies were located in laminae V (sacral 1 and 2 levels), VI (sacral 1 and 3), VII (lumbar 7, sacral 1 and 3, caudal 1) and X (sacral 1). Laminae I and II showed the highest density of immunoreactive fibers for each of the three tachykinins studied, being in general lamina IV who showed the lowest number of immunoreactive fibers containing substance P, neurokinin A or B. The anatomical distribution of the three tachykinins studied in the cat spinal cord indicates that the neuropeptides could be involved in the neurotransmission and/or in the neuromodulation of nociceptive information, as well as in autonomic and affective responses to pain. Moreover, the involvement of substance P, neurokinin A or B in other functions unrelated to the transmission of pain is also possible (autonomic and motor functions). The distribution of the neuropeptides studied in the cat is compared with the location of the same neuropeptides in the spinal cord of other species. The possible origin of the tachykinergic fibers in the cat spinal cord is also discussed.     

Functional consequences of motor unit recruitment order reversals following spinal cord transection in cat

Motoneuron recruitment order determinations were made for acute, 2-week chronic, and 3-month chronic spinal cats by comparing cutaneous nerve stimulation thresholds for evoking single unit tibialis anterior (TA) electromyogram (EMG) spikes of different sizes. Recruitment order was largely ( approximately 80%) orderly (small spikes recruited at lower stimulus intensities than large spikes) in acute and 3-month chronic spinal animals. However, in 2-week chronic spinal animals recruitment order was reversed, with large units more often recruited at lower stimulus intensities than small units ( approximately 65%). Morphological analyses of TA muscle fibers suggested that fiber size changes were unlikely to account for the dramatic alterations in recruitment order results of the 2-week chronic spinal animals. Additional studies suggested that the recruitment order reversal in the 2-week chronic animals coincided with an enhanced reflex neural output (increased recruitment or reflex gain) for the flexion reflex which compensated for disuse atrophy related decreases in flexor muscle force generation capability in these animals. The data from 2-week chronic spinal animals represent a functionally significant example of deviation from the normal size principle of motoneuron recruitment order as the corresponding reflex gain increases can enhance the rapidity of motor function recovery (standing, locomotion) following spinal injury.     

Relationship between the activity of postsynaptic spinal cord elements and propriospinal and spino-bulbo-spinal reflexes.

The relationship between the activity of the lumbar spinal interneurones and propriospinal (PS) and spino-bulbo-spinal (SBS) efferent reflex responses evoked by somatic (muscle, skin) and splanchnic nerve stimulation was studied in chloralose-anaestetized adult cats. During stimulation of one somatic nerve, the postsynaptic cord elements could be divided into three groups, according to whether their activity was was synchronous with the PS component of the efferent discharge (PS group), with the SBS component (SBS group) or with both (PS-SBS-group). Group SBS and PS-SBS interneurones were localized in the ventral quadrant of the grey matter. On stimulation of different nerves, the same interneurone could in one case respond synchronously with the PS component of the efferent discharge and in another with the SBS component. The membrane of units which did not generate propagated spike potentials during PS or SBS reflex activity was hyperpolarized in this period, or failed to display changes characteristic for postsynaptic inhibition. Convergence of somatic and visceral afferentation was observed in all three groups of postsynaptic elements. In type PS-SBS and SBS units it was massive (occurring in 85% and 100% of the cases respectively). The results confirmed the intimacy of functional contact of PS and SBS systems activated by somatic and visceral afferents.     

Response properties of periodontal mechanosensitive neurons in the trigeminal spinal tract nucleus of the cat.

Periodontal mechanosensitive (PM) units were recorded from the trigeminal spinal tract nucleus (Vst) of the cat. The Vst is divided into three subnuclei: oralis (Vo), interpolaris (Vi), and caudalis (Vc). The receptive fields of PM units in Vo and Vi were arranged in a dorsoventral sequence in the mandibular to maxillary divisions, and those in Vc were arranged in a mediolateral sequence. The majority of Vo units were single-tooth ones, whereas more than half the Vi units and all the Vc ones were multitooth units. The PM units in each subnucleus were predominantly responsive to canine tooth stimulation. Most of the PM units in Vo and Vi gave sustained responses to pressure applied to the tooth, were directionally selective, and were most actively excited by canine tooth stimulation in the caudomedial or rostrolateral direction. Vc units, however, were transient. The threshold intensity for firings by canine tooth stimulation was less than 0.05 N. These findings indicate that only the response properties of PM units in the rostral part of Vst resemble those of the trigeminal main sensory nucleus neurons and primary afferent nerves.     

Acetylcholine estimate in glial cells of the cat spinal cord

Structures containing acetylcholinesterase were found in the motor nuclei of the cervical enlargement of the cat spinal cord by light and electron microscopy in material stained by the Karnovsky-Roots method. The specific response was observed not only in neurons of the motor nuclei, but also in some satellite cells, astrocytic glial cells, and Schwann cells. A positive reaction for acetylcholinesterase was found in some of the satellite cells located close to both cholinergic and noncholinergic neurons. As a result of electron microscopy, an electron-dense deposit of copper ferrocyanide was found on the structures of the nucleolus, on the surface of the inner and outer layers of the nuclear membrane, in the pores of the nuclear membrane, in the perinuclear space, and in the endoplasmic reticulum of the perikaryon of some satellite cells, as well as on the outer and inner surfaces of the cytoplasmic membrane of the Schwann cells.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev, Translated from Neirofiziologiya, Vol. 9, No. 1, pp. 48–51, January–February, 1977.     

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.     

Descending monoaminergic pathways in the primate spinal cord.

The distribution of monoamine axons and terminals within the spinal cord of a primate (Macaca mulatta) was studied with the Falck-Hillarp histofluorescence technique for the demonstration of biogenic amines. Catecholamine and indoleamine varicosities appeared qualitatively similar to those previously reported for the rat although the indoleamine terminals were difficult to visualize and were not studied in great detail. Catecholamine fibers innervate the substantia gelatinosa, marginal layer, intermediolateral cell column, ventral horn and the region surrounding the central canal. The location of monoamine axons, as revealed by spinal cord ligation, corresponds to that in the rat and cat with the exception of the dorsolateral region of white matter where fluorescent axons are not visible in the primate.     

Phrenic nerve afferents elicited cord dorsum potential in the cat cervical spinal cord

Background  

The diaphragm has sensory innervation from mechanoreceptors with myelinated axons entering the spinal cord via the phrenic nerve that project to the thalamus and somatosensory cortex. It was hypothesized that phrenic nerve afferent (PnA) projection to the central nervous system is via the spinal dorsal column pathway.