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.     

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.     

Character of activation of medullary reticulospinal neurons by collaterals of pyramidal fibers

The character of activation of medullary reticulospinal neurons by collaterals of pyramidal fibers was investigated in cats anesthetized with pentobarbital (40 mg/kg) or a mixture of chloralose (45 mg/kg) and pentobarbital (15 mg/kg). The experiments were carried out on animals after preliminary destruction of the contralateral red nucleus and division of the ipsilateral dorsolateral fasciculus in segment C₄. A conditioning technique showed that pre- and postsynaptic effects arising in the medullary gigantocellular nucleus to stimulation of the cortex and of the isolated dorsolateral funiculus are due to activation of collaterals of pyramidal fibers projecting into the brain stem. In most reticulospinal neurons tested, stimulation of the fasciculus induced monosynaptic EPSPs. Their generation was due to influences transmitted via fast- and slow-conducting pyramidal fibers. Pyramidal fibers with different conduction velocities are distributed irregularly in the pyramidal tract in the cervical region of the spinal cord. Mainly slowly-conducting fibers are found in its medial zones and fast-conducting pyramidal fibers in its lateral zones. The results are evidence that in cats fibers of the pyramidal tract, running into the spinal cord, can activate medullary reticulospinal neurons directly.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 9, No. 5, pp. 495–503, September–October, 1977.     

Synaptic activation of metabotropic glutamate receptors regulates dendritic outputs of thalamic interneurons

Information gating through the thalamus is dependent on the output of thalamic relay neurons. These relay neurons receive convergent innervation from a number of sources, including GABA-containing interneurons that provide feed-forward inhibition. These interneurons are unique in that they have two distinct outputs: axonal and dendritic. In addition to conventional axonal outputs, these interneurons have presynaptic dendrites that may provide localized inhibitory influences. Our study indicates that synaptic activation of metabotropic glutamate receptors (mGluRs) increases inhibitory activity in relay neurons by increasing output of presynaptic dendrites of interneurons. Optic tract stimulation increases inhibitory activity in thalamic relay neurons in a frequency- and intensity-dependent manner and is attenuated by mGluR antagonists. Our data suggest that synaptic activation of mGluRs selectively alters dendritic output but not axonal output of thalamic interneurons. This mechanism could serve an important role in focal, feed-forward information processing in addition to dynamic information processing in thalamocortical circuits.     

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.     

Tranformation of long reticulofugal spike trains by interneurons connected monosynaptically with the reticulospinal tract

Characteristics of transmission of activity evoked by stimulation of the reticular formation through interneurons located in the ventromedial zones of the gray matter of the lumbar division of the spinal cord and connected monosynaptically with reticulospinal fibers were investigated in cats. Responses of the neurons to relatively low-frequency (not exceeding 80–100/sec) stimulation consisted mainly of stationary discharges; with a further increase in frequency the response became nonstationary (the initial, relatively high-frequency discharge was followed by partial or complete suppression of the discharge). The maximal frequency of the initial phase of the response to high (over 400/sec) frequencies of stimulation was 180–230 spikes/sec. The "transmission factor" (ratio between the frequency of spikes in the response to the frequency of stimulation), calculated for stationary discharges, reached 0.7–0.8 at low frequencies of stimulation, and then decreased significantly. On the basis of the statistical characteristics of the stationary portions of the evoked activity and analysis of these data by the use of a mathematical model, indirect estimates were obtained of the parameters of processes lying at the basis of the transforming properties of this cell population.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 10, No. 3, pp. 278–286, May–June, 1978.     

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.     

Investigation of the functional characteristics of reticulo-spinal fibers of the ventral funiculus

Functional characteristics of single reticulo-spinal fibers of the ventral funiculi were studied at the level of the 10th thoracic segment of the spinal cord in anesthetized (with chloralose and pentobarbital) and decerebrate cats after removal of the cerebellum. The reticulospinal tract of the ventral funiculus consists of a broad spectrum of rhythmically active and "silent" fibers, divided into three groups: fibers with a high (65–110 m/sec), medium (45–60 m/sec), and low (20–40 m/sec) conduction velocity. Spontaneous rhythmic activity is more characteristic of the fibers of the last two groups. The quantitative ratio between rhythmically active and silent fibers was about twice as high in the decerebrate as in the anesthetized animals. Depending on the character of distribution of interspike intervals the spontaneous activity of the reticulo-spinal fibers of the animals of both groups could be classified in three types: I) with a uniform distribution of interval; II) with a tendency toward grouping of spikes into volleys; III) with marked grouping of the intervals. Fibers with low and medium conduction velocities more often had spontaneous activity of types I and II, while fibers with a high conduction velocity more often had activity of types II and III. The possible functional significance of the reticulo-spinal fibers of the ventral funiculi with different conduction velocities and types of spontaneous activity is discussed.     

Inhibition of crossed caudal interneurons by lateral interneurons in lamprey spinal cord during fictive locomotion

Templates of the membrane potential profiles from lateral (LI) interneurons and motoneurons during glutamate- and N-methyl-D-aspartate (NMDA)-induced fictive locomotion showed pronounced plateau phases. In contrast, crossed caudal (CC) interneurons had a less obvious and steeper plateau region that was followed by a clear notch coinciding with the end of the lateral interneuron plateau phase. These results indicate a significant inhibitory input from LI to CC interneurons.     

Synaptic excitation of reticulospinal neurons during the startle reaction in cats anesthetized with chloralose

Synaptic processes in reticulospinal neurons of the pons and medulla during the startle reaction evoked by somatic stimulation were investigated in cats anesthetized with chloralose. The main type of response of reticulospinalneurons was found to be PSPs involving intrareticular (proprioreticular) pathways of varied complexity: oligosynaptic (including supposedly monosynaptic) and polysynaptic. Comparison of EPSP characteristics with parameters of spino-bulbospinal (SBS) discharges recorded simultaneously in the intercostal nerves showed that polysynaptic EPSPs evoked through corresponding proprioreticular pathways were most effective in creating a descending SBS volley. About half the reticulospinal neurons of the pons and medulla were involved at any one time in the synaptic relay process during the startle reflex. The conduction velocity in axons of these neurons varied from 30 to 98 m/sec (means 64.5 Mp 16.5 m/sec). Some distinguishing features of the functional organization of the reticular "center" for the startle reaction are discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 13, No. 6, pp. 594–603, November–December, 1981.     

Synaptic processes in thoracic motoneurons evoked by visceral impulses

Synaptic processes in various functional groups of thoracic motoneurons (segments T9–T11) were investigated in anesthetized (chloralose and Nembutal), decerebrate, and spinal cats. Visceral stimulation in animals with an intact CNS during artificial respiration evokes the development of primary (latent period under 12 msec) and secondary (latent period over 30 msec) PSPs in the motoneurons. The primary PSPs consist of early and principal components. The early component is due to excitation of group A₂ and A visceral afferents, the principal PSP to excitation of the A group. The principal component in motoneurons of the internal and external intercostal muscles and abdominal muscles is excitatory, while in motoneurons innervating the spinal muscles it is excitatory—inhibitory or inhibitory. The secondary PSPs as a rule are excitatory and are due to activation of fibers of the A group. During natural respiration the primary PSPs of motoneurons of the intercostal muscles and abdominal muscles are predominantly inhibitory. In spinal animals no secondary responses are present and the primary becomes entirely excitatory regardless of the functional class of the motoneurons. The mechanisms of reciprocal activation of thoracic motoneurons by visceral impulses in animals during artificial and natural respiration are discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 4, No. 3, pp. 286–295, May–June, 1972.     

Synaptic inputs onto spiking local interneurons in crayfish are depressed by nitric oxide

We have analyzed the action of nitric oxide on the synaptic inputs of spiking local interneurons that form part of the local circuits in the terminal abdominal ganglion of the crayfish, Pacifastacus leniusculus. Increasing the availability of NO in the ganglion by bath applying the NO donor SNAP, or the substrate for its synthesis, L-arginine, caused a depression of synaptic inputs onto the interneurons evoked by electrically stimulating mechanosensory neurons in nerve 2 of the terminal ganglion. Conversely, reducing the availability of NO by bath application of an NO scavenger, PTIO, and an inhibitor of nitric oxide synthase, L-NAME, increased the amplitude of the evoked potentials. These results suggest that elevated NO concentration causes a depression of the synaptic inputs to spiking local interneurons. To determine whether these effects could be mediated through an NO/cGMP signaling pathway we bath applied a membrane permeable analogue of cGMP, 8-br-cGMP, which decreased the amplitude of the inputs to the interneurons. Bath application of an inhibitor of soluble guanlylyl cyclase, ODQ, produced an increase in the amplitude of the synaptic inputs. Our results suggest that NO causes a depression of synaptic inputs to spiking local interneurons probably by acting through an NO/cGMP signaling pathway. Moreover, application of NO scavengers modulates the inputs to these interneurons, suggesting that NO is continuously providing a powerful and dynamic means of modulating the outputs of local circuits.     

Synaptic responses of propriospinal neurons to stimulation of the stepping strip of the dorsolateral funiculus in cats

Synpatic responses were recorded extracellularly from single neurons at levels T12–T13 in response to microstimulation of the stepping strip of the dorsolateral funiculus in the thoracic and cervical portions of the spinal cord in cats decerebrated at the precollicular level [4]. The latent periods of these responses increased when the distance between the stepping point and recording point exceeded 20 mm, and when two stimuli had to be applied in order to evoke responses. Axons of neurons respondingtrans-synaptically to stimulation of the stepping strip were located on the boundary between the lateral and ventral funiculi close to the gray matter. Antidromic responses of neurons sending their axons in the caudal direction were found on average in 37% of cases, provided that the distance between the recording and stimulation points did not exceed 40 mm. Half of the neurons which generated synaptic responses to stimulation of spinal stepping points could be excited also by a series of three to six stimuli, applied to the mesencephalic locomotor point [15]. It is suggested that the neurons discovered may participate in the spread of activity toward the generator of stepping movements of the hind limb.Institute for Problems in Information Transmission, Academy of Sciences of the USSR, Moscow. M. V. Lomonosov Moscow State University. Translated from Neirofiziologiya, Vol. 17, No. 2, pp. 270–278, March–April, 1985.     

Wind-activated thoracic interneurons of the cockroach: II. Patterns of connection from ventral giant interneurons

A number of thoracic interneurons (TIs) have been found to receive inputs from ventral giant interneurons (vGIs). Each of these cells responds to wind with short latency depolarizations. The previous paper described response properties of several TIs to wind stimuli, including those excited by vGIs. The data showed a correlation between the shape of the TI's wind fields and its morphology. The presence of ventral branches located near the midline of the ganglion predicts a strong response to wind on that side. These ventral median (VM) branches are in the proper location to permit overlap with processes from vGIs. Here we describe the patterns of connections between individual vGIs and 13 of the thoracic interneurons located in the meso- and metathoracic ganglia. A correlation was found between the presence of VM branches and excitation by vGIs. TIs were only excited by vGIs on the side(s) on which VM branches exist. However, presence of a VM branch does not imply that all vGIs on that side make connections with the TI. Summation was found between various vGIs that excited each individual thoracic interneuron. In unilateral thoracic interneurons, no sign of inhibition was found from vGIs on the sides opposite that which contained excitatory vGI axons. Neither was there any evidence of inhibition from dorsal giant interneurons. In addition preliminary evidence indicated that left-right homologues do not inhibit one another. Thus, the data suggest that directional wind fields are primarily the result of selective connection from specific vGIs.     

Synaptic transmission in thoracic autonomic ganglia of the dog

Afferent stimulation of one canine thoracic cardiopulmonary nerve can generate compound action potentials in another ipsilateral cardiopulmonary nerve. These compound action potentials persist after acute decentralization of the middle cervical ganglion, indicating that they result from neural activity in the middle cervical ganglion and thoracic nerves. Changing the frequency of stimulation can alter the compound action potentials, suggesting that temporal facilitation or inhibition occurs in this middle cervical ganglion preparation. The compound action potentials can be modified by stimulation of sympathetic preganglionic fibers and by hexamethonium, atropine, phentolamine, propranolol, and (or) manganese. It thus appears that afferent cardiopulmonary nerves can activate efferent cardiopulmonary nerves via synaptic mechanisms in the stellate and middle cervical ganglia. It also appears that these mechanisms involve adrenergic and cholinergic receptors and are influenced by preganglionic sympathetic fibers arising from the cord.