T. G. Deliagina

Spinal and supraspinal postural networks

Different species maintain a particular body orientation in space (upright in humans, dorsal-side-up in quadrupeds, fish and lamprey) due to the activity of a closed-loop postural control system. We will discuss operation of spinal and supraspinal postural networks studied in a lower vertebrate (lamprey) and in two mammals (rabbit and cat). In the lamprey, the postural control system is driven by vestibular input. The key role in the postural network belongs to the reticulospinal (RS) neurons. Due to vestibular input, deviation from the stabilized body orientation in any (roll, pitch, yaw) plane leads to generation of RS commands, which are sent to the spinal cord and cause postural correction. For each of the planes, there are two groups of RS neurons responding to rotation in the opposite directions; they cause a turn opposite to the initial one. The command transmitted by an individual RS neuron causes the motor response, which contributes to the correction of posture. In each plane, the postural system stabilizes the orientation at which the antagonistic vestibular reflexes compensate for each other. Thus, in lamprey the supraspinal networks play a crucial role in stabilization of body orientation, and the function of the spinal networks is transformation of supraspinal commands into the motor pattern of postural corrections. In terrestrial quadrupeds, the postural system stabilizing the trunk orientation in the transversal plane was analyzed. It consists of two relatively independent sub-systems stabilizing orientation of the anterior and posterior parts of the trunk. They are driven by somatosensory input from limb mechanoreceptors. Each sub-system consists of two closed-loop mechanisms - spinal and spino-supraspinal. Operation of the supraspinal networks was studied by recording the posture-related activity of corticospinal neurons. The postural capacity of spinal networks was evaluated in animals with lesions to the spinal cord. Relative contribution of spinal and supraspinal mechanisms to the stabilization of trunk orientation is discussed.

Activity of Different Classes of Neurons of the Motor Cortex during Postural Corrections

The dorsal side-up body orientation in quadrupeds is maintained by a postural system that is driven by sensory feedback signals. The spinal cord, brainstem, and cerebellum play essential roles in postural control, whereas the role of the forebrain is unclear. In the present study we investigated whether the motor cortex is involved in maintenance of the dorsal side-up body orientation. We recorded activity of neurons in the motor cortex in awake rabbits while animals maintained balance on a platform periodically tilting in the frontal plane. The tilts evoked postural corrections, i.e., extension of the limbs on the side moving down and flexion on the opposite side. Because of these limb movements, rabbits maintained body orientation close to the dorsal side up. Four classes of efferent neurons were studied: descending corticofugal neurons of layer V (CF5s), those of layer VI (CF6s), corticocortical neurons with ipsilateral projection (CCIs), and those with contralateral projection (CCCs). One class of inhibitory interneurons [suspected inhibitory neurons (SINs)] was also investigated. CF5 neurons and SINs were strongly active during postural corrections. In most of these neurons, a clear-cut modulation of discharge in the rhythm of tilting was observed. This finding suggests that the motor cortex is involved in postural control. In contrast to CF5 neurons, other classes of efferent neurons (CCI, CCC, CF6) were much less active during postural corrections. This suggests that corticocortical interactions, both within a hemisphere (mediated by CCIs) and between hemispheres (mediated by CCCs), as well as corticothalamic interactions via CF6 neurons are not essential for motor coordination during postural corrections.

Activity of Ia inhibitory interneurons during fictitious scratch reflex in the cat.

(1) The fictitious scratch reflex was observed in decerebrate cats immobilized with Flaxedil. The activity of interneurons in the inhibitory pathways from Ia afferents to motoneurons of antagonistic muscles was recorded during scratching. The selected interneurons were supplied by Ia afferents from m. vastus, posterior biceps-semitendinosus and sartorius. (2) Almost all recorded interneurons showed periodic modulation of activity. Their maximal activity in the scratch cycle usually coincided with the maximal activity of motoneurons of those muscles from which the interneurons receive Ia afferents. Excitation of Ia afferents by passive stretch of the muscle or by electrical stimulation of the muscle nerve resulted in the increase of the interneuron activity, without changing its timing in the scratch cycle.

Encoding and decoding of reticulospinal commands.

In the lamprey, the reticulospinal (RS) system is the main descending system transmitting commands to the spinal cord. We investigated these commands and their effect on the spinal mechanisms. The RS commands were studied by recording responses of RS neurons to sensory stimuli eliciting different motor behaviors. Initiation of locomotion was associated with symmetrical bilateral massive activation of RS neurons, whereas turns in different planes were associated with asymmetrical activation of corresponding neuronal groups. The sub-populations of RS neurons causing different motor behaviors partly overlap. We suggest that commands for initiation of locomotion and regulation of its vigour, encoded as the value of bilateral RS activity, are decoded in the spinal cord by integrating all RS signals arriving at the segmental locomotor networks. Commands for turns in different planes, encoded as an asymmetry in the activities of specific groups of RS neurons, are decoded by comparing the activities of those groups. This hypothesis was supported by the experiments on a neuro-mechanical model, where the difference between the activities in the left and right RS pathways was used to control a motor rotating the animal in the roll plane. Transformation of the descending commands into the motor responses was investigated by recording the effects of individual RS neurons on the motor output. Twenty patterns of influences have been found. This great diversity of the patterns allows the RS system to evoke body flexion in any plane. Since most neurons have asymmetrical projections we suggest that, for rectilinear swimming, RS neurons with opposite asymmetrical effects are co-activated.

Visual input affects the response to roll in reticulospinal neurons of the lamprey.

A body orientation with the dorsal side up is usually maintained by lampreys during locomotion. Of crucial importance for this is the vestibular-driven control system. A visual input can affect the body orientation: illumination of one eye during swimming evokes roll tilt towards the source of light. The aim of the present study was to investigate the interaction of visual and vestibular inputs in reticulospinal (RS) neurons of the brainstem. The RS system is the main descending system transmitting information from the brainstem to the spinal cord. The response of neurons in the middle rhombencephalic reticular nucleus to a unilateral nonpatterned optic input was investigated, as well as the influence of this input on the response of RS neurons to vestibular stimulation (roll tilt). Experiments were carried out on a brainstem preparation with intact labyrinths and, in some cases, intact eyes. Illumination of one eye or electrical stimulation of the optic nerve (10 Hz) resulted in an activation of RS neurons preferentially on the ipsilateral side of the brainstem. The same result was obtained after ablation of the optic tectum, demonstrating that there are asymmetrical visual projections to the lower brainstem which do not involve the tectum. Stimulation of the optic nerve strongly affected the vestibular response in RS neurons. As a rule RS neurons are silent at the normal (dorsal-side-up) orientation of the brainstem and become active with contralateral roll tilt. During continuous optic nerve stimulation, however, the RS neurons on the side of stimulation fire during normal orientation of the brainstem, and the response to contralateral roll tilt increases considerably in many neurons. The effects of the optic input in contralateral RS neurons were less consistent. Any asymmetry in the signals transmitted to the spinal cord by the two (left and right) sub-populations of RS neurons can be expected to evoke a correcting motor response aimed at turning the body around its longitudinal axis to a position at which the symmetry between left and right RS neurons is restored. Normally, the symmetry will occur when the dorsal side is upwards, but with a unilateral visual input it will occur instead at some degree of ipsilateral roll.

Activity of Renshaw cells during fictive scratch reflex in the cat.

SummaryThe experiments were performed on decerebrate curarized cats with a hindlimb either completely deafferented or partly deefferented. Through tactile stimulation of the pinna, a fictive scratch reflex was evoked and activity in muscle efferents was then observed, similar to that in actual scratching. The duration of the cycle was about 250 ms, with extensor activity during a short period of about 50 ms (S phase) and flexor activity during a much longer one (about 200 ms; L phase). Appearance of rhythmic bursts of discharges was preceded by tonic flexor activity (tonic phase of scratching). Discharges of Renshaw cells were recorded extracellularly during these three phases, in parallel with discharges in the gastrochemius-soleus nerve. During the tonic phase of the scratch reflex, some Renshaw cells with input from flexors decreased their activity while others increased. No change in Renshaw cell activity with input from extensors was then observed. During the rhythmic phases of the scratch reflex a majority of Renshaw cells was phasically active. They usually responded once per cycle, with a burst of 1–30 impulses of 50–100 ms duration, most often occurring at the end of the L phase and during the S phase. Bursts of Renshaw cells with input from flexors and of extensors, respectively, overlapped to a high degree. However, maximal firing of extensor-coupled Renshaw cells occurred somewhat later than that of flexor-coupled cells. Flexor-coupled Renshaw cells discharged mainly at the end of the L phase and during the S phase, i.e. when the flexor moto-neurones terminated their activity. Extensor-coupled Renshaw cells reached maximal activity during the S phase, i.e. when the extensor motoneurones were recruited. After spinal transection at C1 level, Renshaw cells responded with an increased number of spikes but without change in timing of the discharges during the scratch cycle. Most of the contralaterally located Renshaw cells studied were also phasically active during the scratch reflex. The role of motoneurones and spinal interneurones in determining the timing of Renshaw cell activity and the role of the latter in control of posture and rhythmic movements are discussed.

Role of dermal photoreceptors and lateral eyes in initiation and orientation of locomotion in lamprey

The response to illumination, and the functional roles of skin photoreceptors and lateral eyes, were examined in the adult river lamprey (Lampetra fluviatilis L.). Illumination of one side of the lamprey evoked a turning movement away from the light source followed by locomotion. The lateral eyes were responsible for directing the movements away from the source of light. A selective illumination of one lateral eye consistently evoked a negative phototactic reaction, whereas a selective illumination of tail skin photoreceptors evoked locomotion, without any preferential orientation relative to the source of light. Experiments were performed by video recording the locomotor responses to localized illumination, and analyzed frame by frame. The horizontal turning movement during negative phototaxis consisted of an asymmetric laterally directed mechanical wave, of higher amplitude and lower velocity than the normal locomotory waves, which was propagated from the rostral to the caudal end of the body.

Analysis of the Central Pattern Generator for Swimming in the Mollusk Clionea

Abstract: The pteropod mollusk Clione limacina swims by rhythmic movements of two wings. The central pattern generator (CPG) for swimming, located in the pedal ganglia, is formed by three groups of interneurons. The interneurons of the groups 7 and 8 are of crucial importance for rhythm generation. They are endogenous oscillators capable of generating rhythmic activity with a range of frequencies typical of swimming after extraction from the ganglia. This endogenous rhythmic activity is enhanced by serotonin. The interneurons 7 and 8 produce one prolonged action potential (about 100 ms in duration) per cycle. Prolonged action potentials contribute to determining the duration of the cycle phases. The interneurons of two groups inhibit one another determining their reciprocal activity. The putative transmitters of groups 7 and 8 interneurons are glutamate and acetylcholine, respectively. Transition from one phase to the other is facilitated by the plateau interneurons of group 12 that contribute to termination of one phase and to initiation of the next phase. Maintaining the rhythm generation and transition from one phase to the other is also promoted by postinhibitory rebound. The redundant organization of the swimming generator guarantees the high reliability of its operation. Generation of the swimming output persisted after the inhibitory input from interneurons 8 to 7 had been blocked by atropine. Activity of the swimming generator is controlled by a set of command neurons that activate, inhibit or modulate the operation of the swimming CPG in relation to a behaviorally relevant context.

Postural performance in decerebrated rabbit

It is known that animals decerebrated at the premammillary level are capable of standing and walking without losing balance, in contrast to postmammillary ones which do not exhibit such behavior. The main goals of the present study were, first, to characterize the postural performance in premammillary rabbits, and, second, to activate the postural system in postmammillary ones by brainstem stimulation. For evaluation of postural capacity of decerebrated rabbits, motor and EMG responses to lateral tilts of the supporting platform and to lateral pushes were recorded before and after decerebration. In addition, the righting behavior (i.e., standing up from the lying position) was video recorded. We found that, in premammillary rabbits, responses to lateral tilts and pushes were similar to those observed in intact ones, but the magnitude of responses was reduced. During righting, premammillary rabbits assumed the normal position slower than intact ones. To activate the postural system in postmammillary rabbits, we stimulated electrically two brainstem structures, the mesencephalic locomotor region (MLR) and the ventral tegmental field (VTF). The MLR stimulation (prior to elicitation of locomotion) and the VTF stimulation caused an increase of the tone of hindlimb extensors, and enhanced their responses to lateral tilts and to pushes. These results indicate that the basic mechanisms for maintenance of body posture and equilibrium during standing are present in decerebrated animals. They are active in the premammillary rabbits but need to be activated in the postmammillary ones.

Control of locomotion in marine mollusc Clione limacina. VI. Activity of isolated neurons of pedal ganglia.

SummaryIn the pteropodial mollusc Clione limacina, the rhythmic locomotor wing movements are controlled by the pedal ganglia. The locomotor rhythm is generated by two groups of interneurons (groups 7 and 8) which drive efferent neurons. In the present paper, the activity of isolated neurons, which were extracted from the pedal ganglia by means of an intracellular electrode, is described. The following results have been obtained: 1. Isolated type 7 and 8 interneurons preserved the capability for generation of prolonged (100–200 ms) action potentials. The frequency of these spontaneous discharges was usually within the limit of locomotor frequencies (0.5–5 Hz). By de- or hyperpolarizing a cell, one could usually cover the whole range of locomotor frequencies. This finding demonstrates that the locomotor rhythm is indeed determined by the endogenous rhythmic activity of type 7 and 8 interneurons. 2. Type 1 and 2 efferent neurons, before isolation, could generate single spikes as well as high-frequency bursts of spikes. These two modes of activity were also observed after isolating the cells. Thus, the bursting activity of type 1 and 2 neurons, demonstrated during locomotion, is determined by their own properties. Type 3 and 4 efferent neurons generated only repeated single spikes both before and after isolation. 3. The activity of the isolated axons of type 1 and 2 neurons did not differ meaningfully from the activity of the whole cells. Furthermore, in the isolated pedal commissure, we found units whose activity (rhythmically repeating prolonged action potentials) resembled the activity of type 7 and 8 interneurons. These units seemed to be the axons of type 7 and 8 interneurons. Thus, different parts of the cell membrane (soma and axons) have similar electric properties.