Possible organization pattern of interaction between the generators of cyclic motor activity and inputs from supraspinal and afferent systems

Possible organization patterns of scratching and locomotor generators that allow interpretation of experimentally demonstrated reorganizations in temporal parameters of these generator activities after electrical stimulation of descending and peripheral afferent systems were analyzed with application of mathematical simulation of neuronal generator systems. The results obtained led to the conclusion that patterns of such reorganizations influenced by signals from suprasegmental and/or peripheral systems may be determined by only two factors: 1) the structure of synaptic connections between interneuronal functional groups underlying these generator associations, and 2) the structure of connections between these groups of interneurons and fibers from suprasegmental and peripheral afferent sources. The existence of inhibitory-excitatory actions from descending and afferent systems upon the neurons of locomotor or scratching generator half-centers is a sufficient condition to ensure phasic changes in the sensitivity of these generators to supraspinal and afferent signals. The locomotor generator, unlike the scratching generator, is apparently characterized by a more complex organization of connections between functional neuronal groupings and descending fibers.Translated from Neirofiziologiya, Vol. 25, No. 1, pp. 45–50, January–February, 1993.     

Mechanisms of the suprasegmental adjustment of the operation of the generators of cyclical motoric reactions

Concousions Analysis of the problem of the organization and mechanisms of the functioning of the system of suprasegmental control of cyclical movements can be recapitulated in the following manner. The systems of control of the cyclical movements (of the locomotion and scratching type) are adaptive control systems in which there are adaptive mechanisms (regulators) of both the spinal and supraspinal levels. The spinocerebellar loop presents as an important component of the supraspinal regulators. The cerebellum apparently plays the role of an adaptive filter in the adaptational mechanism of the supraspinal level, a filter which accomplishes the spatial-temporal filtration of information arriving along its various afferent inputs. That phase and amplitude modulation of the effectiveness of the influence of the corresponding descending systems on the spinal centers of rhythmic movements is accomplished on this basis, modulation which in the final analysis ensures the achievement of a stable state of the limited interaction of the centers with the supraspinal systems. The systems of control of the locomotor and scratching movements differ above all in the quality (degree) of their adaptedness. A higher degree of adaptedness of the system of control is characteristic for the locomotor movements than for the scratching movements.A. A. Bogomolets Institute of Physiology, Ukrainian Academy of Sciences, Kiev. Translated from Neirofiziologiya, Vol. 24, No. 6, pp. 736–755, November–December, 1992.     

Active selection of afferent information as the basic principle of peripheral correction of the activity of spinal rhythmic movement generators

This paper summarizes information obtained in the experimental study of the dynamics of polarization of central primary afferent endings and modifications of segmental responses to afferent stimuli during fictitious locomotion and fictitious scratching in immobilized, decorticated, decerebrate, and spinal cats. Fictitious locomotion was accompanied by tonic hyperpolarization, fictitious scratching by tonic depolarization of central primary afferent endings. Against the background of these long-lasting changes in primary afferent depolarization, it exhibited periodic changes in the rhythm of efferent activity. Periodic changes of depolarization were virtually in phase in different ipsilateral segments of the lumbosacral enlargement. Data on groups of afferent fibers in whose central endings tonic and phasic changes of polarization took place. The appearance of fictitious locomotion was accompanied by a tonic increase, and of fictitious scratching by tonic inhibition of several evoked segmental responses. These tonic changes were a background against which segmental responses were modulated in step with the working rhythm of the locomotion and scratching generators. Many of the changes in evoked segmental responses were shown to be based on modulation of polarization of central endings of primary afferents by locomotion and scratching generators. It is concluded that active tonic and phase-dependent selection of incoming afferent information is effected through modulation of presynaptic inhibition of the generator. The role of this selection in peripheral collection of activity of locomotion and scratching generators is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 16, No. 3, pp. 343–353, May–June, 1984.     

Reorganization of the efferent activity of the locomotor generator controlling forelimb movements for electrical stimulation of the descending systems

The reorganization of the parameters of the efferent activity of the forelimb locomotion generator for electrical stimulation of the descending systems is determined in experiments on decerebrate immobilized cats. This generator is found to be characterized by a stable state at which the sum of influences of the signals from different descending systems on the generator is extremely limited. It is concluded that under the influence of these signals, the reorganizations of the activity of the locomotion generators of different limbs bring the motor program into a dynamic (or nearly dynamic) relationship with the supraspinal inflow, allowing for a sufficient limitation and balancing of the influences of the corresponding descending systems on the interneuronal networks determining the temporal and phase characteristics of the activity of these generators.A. A. Bogomolets Institute of Physiology, Ukrainian Academy of Sciences, Kiev. Translated from Neirofiziologiya, Vol. 23, No. 6, pp. 704–708, November–December, 1991.     

Rearrangement of scratch generator efferent activity during electrical activation of descending systems

Effects of signals proceeding along descending pathways on parameters of scratch generator activity were investigated in decerebrate immobilized cats. Certain phase-linked alterations in these parameters were shown to occur under the effects of electrical activation of the main descending systems. The biggest increase in scratch cycle duration under electrical stimulation of Deiter's nucleus, the red nucleus, and pyramidal tract is produced when stimuli are applied during the first half of the aiming stage. Stimulation during the second half of the aiming phase and at the start of the scratching movement hardly affect the scratching cycle. The main increase in length of scratch cycle during electrical stimulation of the reticular gigantocellularis nucleus is noted when stimuli are presented during the second half of the aiming stage. Electrical activation of descending pathways during the latter induces a rise in intensity in this phase and reduced intensity of the actual scratching stage. Activation of the pathways during this scratching motion causes heightened intensity of the motion while hardly affecting intensity of the aiming phase. The principles of suprasegmental rectification of scratch generator operation are discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 22, No. 3, pp. 300–309, May–June, 1990.     

Investigation of spinal neuronal mechanisms of movement control systems

Morphological and electrophysiological investigations of the means whereby the principal descending motor systems (the cortico-, rubro-, reticulo-, and vestibulo-spinal tracts) are connected with the segmental interneuronal apparatus and motoneurons show that these connections can be based on two different principles. Descending systems either activate motoneurons directly (monosynaptically) or are connected primarily with various interneuron systems, exerting their influence in that case by regulating the activity of simpler or more complex spinal mechanisms. The older descending system (reticulo- and vestibulo-spinal) possess a monosynaptic excitatory action of motoneurons; the evolutionarily newer descending systems, which transmit the most complex motor signals from the cerebral and cerebellar cortex to the spinal cord (cortico- and rubro-spinal), terminate synaptically in every case on interneurons. It is only in primates that a few cortico-spinal fibers form monosynaptic connections with motoneurons. The chief ways of action of the descending systems on interneurons are: control of the afferent inflow into the interneuron system by presynaptic inhibition of the corresponding synapses; control of the interneuron system by postsynaptic interaction with afferent influences; control of motoneurons through the specialized interneuron apparatus. The investigation shows that the last of these mechanisms functions in the cortico- and rubro-spinal, and possibly also in the reticulo- and vestibulo-spinal systems. The functional role of the various means of connection of the descending systems with the spinal neurons in the system of movement control is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 2, No. 2, pp. 189–202, March–April, 1970.     

Partly shared spinal cord networks for locomotion and scratching

Animals produce a variety of behaviors using a limited number of muscles and motor neurons. Rhythmic behaviors are often generated in basic form by networks of neurons within the central nervous system, or central pattern generators (CPGs). It is known from several invertebrates that different rhythmic behaviors involving the same muscles and motor neurons can be generated by a single CPG, multiple separate CPGs, or partly overlapping CPGs. Much less is known about how vertebrates generate multiple, rhythmic behaviors involving the same muscles. The spinal cord of limbed vertebrates contains CPGs for locomotion and multiple forms of scratching. We investigated the extent of sharing of CPGs for hind limb locomotion and for scratching. We used the spinal cord of adult red-eared turtles. Animals were immobilized to remove movement-related sensory feedback and were spinally transected to remove input from the brain. We took two approaches. First, we monitored individual spinal cord interneurons (i.e., neurons that are in between sensory neurons and motor neurons) during generation of each kind of rhythmic output of motor neurons (i.e., each motor pattern). Many spinal cord interneurons were rhythmically activated during the motor patterns for forward swimming and all three forms of scratching. Some of these scratch/swim interneurons had physiological and morphological properties consistent with their playing a role in the generation of motor patterns for all of these rhythmic behaviors. Other spinal cord interneurons, however, were rhythmically activated during scratching motor patterns but inhibited during swimming motor patterns. Thus, locomotion and scratching may be generated by partly shared spinal cord CPGs. Second, we delivered swim-evoking and scratch-evoking stimuli simultaneously and monitored the resulting motor patterns. Simultaneous stimulation could cause interactions of scratch inputs with subthreshold swim inputs to produce normal swimming, acceleration of the swimming rhythm, scratch-swim hybrid cycles, or complete cessation of the rhythm. The type of effect obtained depended on the level of swim-evoking stimulation. These effects suggest that swim-evoking and scratch-evoking inputs can interact strongly in the spinal cord to modify the rhythm and pattern of motor output. Collectively, the single-neuron recordings and the results of simultaneous stimulation suggest that important elements of the generation of rhythms and patterns are shared between locomotion and scratching in limbed vertebrates.     

Alterations produced in the quantitative characteristics of efferent activity parameters of the locomotor generator by decerebellation

Changes in the parameters of activity in hindlimb locomotor generators following decerebellation were quantified during experiments on decerebrate immobilized cats. Eliminating modulating cerebellar influences on nuclei of descending systems was found to lead to a slight increase in the length of activity in the flexor generator half-center and less intensive activity, as well as shortening of the period and more intensive activity in the extensor half-center, together with increased instability in generator operation, reduced statistical dependence between alterations in parameters of activity at the hindlimb half-center generators, and finally intensified effects of afferent inputs on generator activity. A comparison is drawn between the functional role of the spino-cerebellar loop in the operation of locomotor and scratch generators.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 23, No. 2, pp. 142–150, March–April, 1991.     

New vistas on the initiation and maintenance of insect motor behaviors revealed by specific lesions of the head ganglia

In insects, thoracic pattern generators are modulated by the two head ganglia, the supraesophageal ganglion (brain) and the subesophageal ganglion, which act as higher-order neuronal centers. To explore the contribution of each head ganglion to the initiation and maintenance of specific motor behaviors in cockroaches (Periplaneta americana), we performed specific lesions to remove descending inputs from either the brain or the subesophageal ganglion or both, and quantified the behavioral outcome with a battery of motor tasks. We show that ‘emergency’ behaviors, such as escape, flight, swimming or righting, are initiated at the thoracic level independently of descending inputs from the head ganglia. Yet, the head ganglia play a major role in maintaining these reflexively initiated behaviors. By separately removing each of the two head ganglia, we show that the brain excites flight behavior and inhibits walking-related behaviors, whereas the subesophageal ganglion exerts the opposite effects. Thus, control over specific motor behaviors in cockroaches is anatomically and functionally compartmentalized. We propose a comprehensive model in which the relative permissive versus inhibitory inputs descending from the two head ganglia, combined with thoracic afferent sensory inputs, select a specific thoracic motor pattern while preventing the others.     

Spinal motor control system incorporates an internal model of limb dynamics

The existence and utilization of an internal representation of the controlled object is one of the most important features of the functioning of neural motor control systems. This study demonstrates that this property already exists at the level of the spinal motor control system (SMCS), which is capable of generating motor patterns for reflex rhythmic movements, such as locomotion and scratching, without the aid of the peripheral afferent feedback, but substantially modifies the generated activity in response to peripheral afferent stimuli. The SMCS is presented as an optimal control system whose optimality requires that it incorporate an internal model (IM) of the controlled object's dynamics. A novel functional mechanism for the integration of peripheral sensory signals with the corresponding predictive output from the IM, the summation of information precision (SIP) is proposed. In contrast to other models in which the correction of the internal representation of the controlled object's state is based on the calculation of a mismatch between the internal and external information sources, the SIP mechanism merges the information from these sources in order to optimize the precision of the controlled object's state estimate. It is demonstrated, based on scratching in decerebrate cats as an example of the spinal control of goal-directed movements, that the results of computer modeling agree with the experimental observations related to the SMCS's reactions to phasic and tonic peripheral afferent stimuli. It is also shown that the functional requirements imposed by the mathematical model of the SMCS comply with the current knowledge about the related properties of spinal neuronal circuitry. The crucial role of the spinal presynaptic inhibition mechanism in the neuronal implementation of SIP is elucidated. Important differences between the IM and a state predictor employed for compensating for a neural reflex time delay are discussed. Received: 8 February 2000 / Accepted: 24 March 2000     

Dependence of efferent activity parameters on limb position during fictitious scratching in decerebrate cats

The influence of tonic afferent inflow as conditioned by ipsilateral hindlimb position on the efferent activity parameters of the spinal generator governing scratching motion was investigated in immobilized decerebrate cats. A significant correlation was observed between motor activity parameters and ensuing bouts of scratching in the absence of afferent flow (after deafferentation of the limbs). This correlation was less pronounced when afferentation remained intact and declined when the limb was shifted from the "aimed" to either the "overaimed" or "deflecting backwards" placing of the limb. The statistically significant correlations found between the parameters of different stages of motor activity and their dependence on hindlimb positions during actual scratching could be responsible for the stability of intended placing of the limbs during the performance of oscillatory movements. Hindlimb deafferentation would appear closest to "aimed" position judging by the parameters of efferent activity and the nature of correlations between them.A. A. Bogomolets Institute of Physiology. Academy of Sciences of the Ukrainian SSR. Kiev. Translated from Neirofiziologiya, Vol. 15, No. 5, pp. 636–645, September–October, 1986.     

Mathematical model of activity of spinal generators producing rhythmic movement

Different organizational arrangements of scratching and locomotor rhythm generators were simulated by a computer-aided mathematical model. A functional group of neurons (a hemicenter constructed on the basis of a stochastically arranged neuronal network) served as the basis for the generator. Several organizational arrangements of scratching and locomotor rhythm generators are considered: two hemicenters with reciprocal inhibitory connections and tonic excitatory influences on both; two hemicenters with inhibitory-excitatory connections and tonic excitatory influences on only one of these; circular structures consisting of more than two functional groups of neurons with excitatory and inhibitory connections between them. All these arrangements would allow for generation of rhythmic activity with a similar time course to that of scratching and locomotor rhythm. It was found that the transition from locomotor to scratching rhythm could be based on fairly simply organized effects on generator neurons. Principles possibly guiding the construction of spinal generators of scratching and locomotor movements are discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 20, No. 5, pp. 586–597, September–October, 1988.     

Depolarization of primary afferents during fictitious scratching in thalamic cats

The dorsal cord and dorsal root potentials were recorded in immobilized thalamic cats during fictitious scratching evoked by mechanical stimulation of the ear. Depolarization of primary afferents was shown to be simulated by the central scratching generator. Antidromic spike discharges appeared at the peak of the primary afferent depolarization waves in certain afferent fibers. Similar discharges arise in the resting state in response to stimulation of limb mechanoreceptors. It is suggested that during real scratching primary afferent depolarization and antidromic spikes evoked by it may effectively modulate the level of the afferent flow to spinal neurons.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 10, No. 2, pp. 173–176, March–April, 1978.     

Reticulospinal and propriospinal monosynaptic influences on motoneurons in frogs

Monosynaptic effects evoked by electrical stimulation of suprasegmental structures and the ventral and lateral columns were recorded intracellularly from motoneurons of the lumbar and cervical enlargements after isolation of the spinal cord and medulla in frogs. Reticulospinal fibers arising from cells of the medial reticular formation of the medulla and running in the ventro-lateral columns evoke monosynaptic excitation of cervical and lumbar motoneurons. The reticulo-motoneuronal E PSPs do not exceed 2–3 mV in amplitude and do not reach the threshold for action potential generation. Division of the spinal cord and interaction between all synaptic inputs tested in chronic experiments showed that monosynaptic E PSPs evoked by direct stimulation of the ventral and lateral columns are due to activation of the descending system of propriospinal fibers. By transmembrane polarization experiments the equilibrium potentials of the reticulo-motoneuronal and propriospinal monosynaptic E PSPs could be determined.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Leningrad. Translated from Neirofiziologiya, Vol. 5, No. 2, pp. 164–173, March–April, 1973.     

Reordering of scratch generator efferent activity produced by stimulating hindlimb skin afferents in decerebrate immobilized cat

Reordering of the parameters of motor activity produced in the scratch generator by regular electrical stimulation of the ipsilateral hindlimb muscle nerve during different limb positions was investigated in decerebrate immobilized cats. Brief short latency inhibition of currently occurring motor activity was produced in response to stimulation, which did not cause an overall shift in the relationship between the intensity of aiming and scratching motion. Changes in cycle duration and intensity of these activities were phase-locked. Speculations were made on the functional role of the phase-locked nature of motor activity remodeling. The possible existence within the scratch generator of a model of the afferent inflow entering the spinal cord during true scratching is suggested.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 19, No. 3, pp. 382–390, May–June, 1987.     

Experimental morphological study of primary afferent terminals at the base of the dorsal horn of the cat spinal cord

The distribution and ultrastructure of primary afferent terminals in the gray matter of the cervical and lumbar regions of the cat spinal cord were studied by the experimental degeneration method of Fink and Heimer. Most preterminals of primary afferents were shown to be concentrated in the region of the intermediate nucleus of Cajal (central part of Rexed's laminae VI–VII), in the substantial gelatinosa (laminae II–III), and in the nucleus proprius of the dorsal horn (central and medial parts of lamina IV). Fewer are found in the region of the motor nuclei. The number of degenerating axon terminals in the lateral parts of laminae IV and V differed: 31.5 and 0.4% respectively of all axon terminals. Many terminals of primary afferents in lamina IV contribute to the formation of glomerular structures in which they exist as terminals of S-type forming axo-axonal connections with other terminals. These results are in agreement with electrophysiological data to show that interneurons in different parts of the base of the dorsal horn differ significantly in the relative numbers of synaptic inputs formed by peripheral afferents and descending systems.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 5, No. 4, pp. 406–414, July–August, 1973.     

Rearrangement of efferent activity of the locomotor generator under electrical activation of descending systems in immobilized cats

The effects of signals travelling through vestibulo-, rubro-, reticulo-, and corticospinal systems on the parameters of locomotor generator activity were investigated in decerebrate immobilized cats. Certain phase-linked alterations in these parameters were found to occur under the effects of electrical stimulation applied to these systems (brief trains of stimuli). The biggest increase in locomotor cycle length was produced by electrical stimulation of Deiter's nucleus — stimulus presentation at the end of the extension phase; stimulation at the flexor stage leads to a shortening of this cycle. Maximum increase in locomotor cycle length produced by electrical stimulation of the red nucleus and nucleus gigantocellaris reticularis together with the pyramidal tract takes place during the first half of the flexion phase. Electrical activation of these descending pathways during the flexion phase induces intensification of this phase and reduced intensity of the extension phase. Activation of the vestibulospinal tract produces increased and reduced intensification of the extension phase respectively. Principles of suprasegmental correction of locomotor and scratch generators are compared.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 23, No. 2, pp. 151–160, March–April, 1991.     

Recording of scratch generator efferent activity produced by cyclic hindlimb movement in decerebrate immobilized cat

The effects were observed on spinal scratch generator activity of the afferent inflow produced in decerebrate immobilized cat by regular passive movement of the hindlimb paw following a trajectory close to that observed during actual scratching. These consisted of substantial alteration in scratch generator efferent activity, which thereby became phase-locked with the afferent flow. Synchronization between efferent scratching activity and passive limb motion has occurred by the first movement cycle and phase-locking was the reverse of that seen during actual scratching.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 19, No. 4, pp. 443–449, July–August, 1987.     

Corticofugal influences on segmental responses of lumbar spinal ventral horn interneurons in cats

Experiments on cats using extra- and intracellular recording methods showed that stimulation of the motor cortex of both hemispheres leads to considerable modulation of responses to stimulation of cutaneous and muscular lower limb afferents in spinal ventral horn interneurons in segments L6, 7. Three types of conditioning corticofugal effect were observed: facilitation, inhibition, and facilitation followed by inhibition (biphasic effect), and inhibitory effects predominated. The duration of facilitation of responses did not exceed 30–40 msec. The characteristics of the time course of inhibition varied: in some cases it began with relatively short intervals (8–15 msec), in other cases with an interval of 30–40 msec; its duration was 125–500 msec, or sometimes more. The effect of cortical stimulation on responses to stimulation of various afferent inputs of the same interneuron was shown to differ. The character of the conditioning corticofugal effect correlated with the latent period of segmental responses: facilitation was observed only in responses with a relatively short latent period (under 5 msec); responses with a longer latent period were mainly inhibited. The type of cortical effect also depended on the function performed by the activated afferent input. It is suggested that differential descending control of segmental polysynaptic responses recorded in ventral horn interneurons with wide convergence of afferent influences takes place in the initial stages of the reflex are. The mechanism of this control is discussed.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neiorofizologiya, Vol. 14, No. 6, pp. 563–571, November–December, 1982.     

Coordination of arm movement during locomotion in ophiurans

During movement of the ophiuranAmphipholis kochii Lutken, any one of its arms can point forward and, consequently, any arm can perform different functions. The arm, when separated from the ophiuran together with the adjacent part of the nerve ring, is capable of complex motor acts, including locomotion. Division of the nerve ring in the ophiuran disturbs coordination of the arms. The results of experiments in which one or more arms were amputated showed that the choice of leading arm and of method of locomotion depends mainly on afferent impulses received from the arms. The results indicate that the neural centers of individual arms possess relative autonomy. Coordinated working of the centers is achieved through their interaction. This interaction ensures the distribution of functions between the arms in accordance with the motor task to be undertaken and coordinates the activity of the arms in time. The dominant role in the distribution of functions between the arms is played by the center of the leading arm, which controls the activity of at least the adjacent centers.Institute of Oceanology, Academy of Sciences of the USSR, Moscow. Institute of Problems in Information Transmission, Academy of Sciences of the USSR, Moscow. Moscow State University. Translated from Neriofiziologiya, Vol. 8, No. 5, pp. 529–537, September–October, 1976.