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Summary of responses to full-turn rotation in 2 subgroups of group Up RS neurons—ipsilateral to UL (A 1 , A 2 ) and contralateral to UL (B 1 , B 2 ). The responses were characterized by the number of neurons activated in each angular step in each of the animals and then averaged over all 7 animals. The responses are presented as a function of pitch angle. Angle of 0° corresponds to the horizontal, back-up orientation of the lamprey. Each step of rotation was divided into 3 intervals (see inset in Fig. 1B). In each of the steps, the dynamic response (activity during rotation) is shown by a black bar; the early and late static responses are shown by 2 successive shaded bars. A 1 , B 1 : responses before UL. A 2 , B 2 : responses after UL. Designations as in Fig. 1B.
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A postural control system in the lamprey is driven by vestibular input and maintains a definite orientation of the animal during swimming. After a unilateral labyrinthectomy (UL), the lamprey continuously rolls toward the damaged side. Important elements of the postural network are the reticulospinal (RS) neurons that are driven by vestibular input...
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A postural control system in the lamprey is driven by vestibular input and maintains the dorsal-side-up orientation of the animal during swimming. After a unilateral labyrinthectomy (UL), the lamprey continuously rolls toward the damaged side. Normally, a recovery of postural equilibrium ("vestibular compensation") takes about 1 mo. However, illumi...
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... The RS neurons responding to nose-up pitch tilt are driven mainly by an excitatory input from the contralateral labyrinth. By contrast, nose-down RS neurons receive excitatory inputs from both labyrinths (Pavlova and Deliagina, 2003). About a quarter of RS neurons respond to both roll and pitch tilts suggesting that these neurons are partly shared by the pitch and roll control systems (Pavlova and Deliagina, 2003;Zelenin et al., 2007). ...
... By contrast, nose-down RS neurons receive excitatory inputs from both labyrinths (Pavlova and Deliagina, 2003). About a quarter of RS neurons respond to both roll and pitch tilts suggesting that these neurons are partly shared by the pitch and roll control systems (Pavlova and Deliagina, 2003;Zelenin et al., 2007). ...
Different species maintain a particular body orientation in space due to activity of the closed-loop postural control system. In this review we discuss the role of neurons of descending pathways in operation of this system as revealed in animal models of differing complexity: lower vertebrate (lamprey) and higher vertebrates (rabbit and cat). In the lamprey and quadruped mammals, the role of spinal and supraspinal mechanisms in the control of posture is different. In the lamprey, the system contains one closed-loop mechanism consisting of supraspino-spinal networks. Reticulospinal (RS) neurons play a key role in generation of postural corrections. Due to vestibular input, any deviation from the stabilized body orientation leads to activation of a specific population of RS neurons. Each of the neurons activates a specific motor synergy. Collectively, these neurons evoke the motor output necessary for the postural correction. In contrast to lampreys, postural corrections in quadrupeds are primarily based not on the vestibular input but on the somatosensory input from limb mechanoreceptors. The system contains two closed-loop mechanisms - spinal and spino-supraspinal networks, which supplement each other. Spinal networks receive somatosensory input from the limb signaling postural perturbations, and generate spinal postural limb reflexes. These reflexes are relatively weak, but in intact animals they are enhanced due to both tonic supraspinal drive and phasic supraspinal commands. Recent studies of these supraspinal influences are considered in this review. A hypothesis suggesting common principles of operation of the postural systems stabilizing body orientation in a particular plane in the lamprey and quadrupeds, that is interaction of antagonistic postural reflexes, is discussed.
... However, several studies have revealed robust responses to rotations in the yaw plane in the different components of the postural reflex arc: the primary vestibular afferents, the descending vestibulospinal and reticulospinal neurons, and the effector spinal motor neurons (Lowenstein, 1970;Rovainen, 1979;Wannier et al. 1998;Zelenin et al. 2003;Pflieger & Dubuc, 2004;Zelenin, 2005;Karayannidou et al. 2007). These studies made it clear that angular movements in the yaw plane in the lamprey have as robust an effect on the postural neural network as they have for movements in the pitch and roll planes (Deliagina & Pavlova, 2002;Pavlova & Deliagina, 2003). Several publications have addressed the question: What is the source of these responses to horizontal angular stimuli, given the missing horizontal canal? ...
In jawed (gnathostome) vertebrates, the inner ears have three semicircular canals arranged orthogonally in the three Cartesian planes: one horizontal (lateral) and two vertical canals. They function as detectors for angular acceleration in their respective planes. Living jawless craniates, cyclostomes (hagfish and lamprey) and their fossil records seemingly lack a lateral horizontal canal. The jawless vertebrate hagfish inner ear is described as a torus or doughnut, having one vertical canal, and the jawless vertebrate lamprey having two. These observations on the anatomy of the cyclostome (jawless vertebrate) inner ear have been unchallenged for over a century, and the question of how these jawless vertebrates perceive angular acceleration in the yaw (horizontal) planes has remained open. To provide an answer to this open question we reevaluated the anatomy of the inner ear in the lamprey, using stereoscopic dissection and scanning electron microscopy. The present study reveals a novel observation: the lamprey has two horizontal semicircular ducts in each labyrinth. Furthermore, the horizontal ducts in the lamprey, in contrast to those of jawed vertebrates, are located on the medial surface in the labyrinth rather than on the lateral surface. Our data on the lamprey horizontal duct suggest that the appearance of the horizontal canal characteristic of gnathostomes (lateral) and lampreys (medial) are mutually exclusive and indicate a parallel evolution of both systems, one in cyclostomes and one in gnathostome ancestors.
... A subsequent lesion of the labyrinth on the other side induced a postural reaction on the newly lesioned side, although all vestibular inputs were now absent. Later studies showed that circuit and biochemical plasticity at different level of the CNS, including the spinal cord, may contribute to vestibular compensation (Deliagina 1997a,b;Dieringer 1995;Pavlova and Deliagina 2003;Pavlova et al. 2004;Straka and Dieringer 1995;Vibert et al. 1999a,b). Of particular interest is a paper (Galiana et al. 1984) showing how a simple change in the weighting of excitability between the vestibular nuclei could account for the Bechterew phenomenon. ...
The recovery of voluntary quadrupedal locomotion after an incomplete spinal cord injury can involve different levels of the CNS, including the spinal locomotor circuitry. The latter conclusion was reached using a dual spinal lesion paradigm in which a low thoracic partial spinal lesion is followed, several weeks later, by a complete spinal transection (i.e., spinalization). In this dual spinal lesion paradigm, cats can express hindlimb walking 1 day after spinalization, a process that normally takes several weeks, suggesting that the locomotor circuitry within the lumbosacral spinal cord had been modified after the partial lesion. Here we detail the evolution of the kinematic locomotor pattern throughout the dual spinal lesion paradigm in five cats to gain further insight into putative neurophysiological mechanisms involved in locomotor recovery after a partial spinal lesion. All cats recovered voluntary quadrupedal locomotion with treadmill training (3-5 days/wk) over several weeks. After the partial lesion, the locomotor pattern was characterized by several left/right asymmetries in various kinematic parameters, such as homolateral and homologous interlimb coupling, cycle duration, and swing/stance durations. When no further locomotor improvement was observed, cats were spinalized. After spinalization, the hindlimb locomotor pattern rapidly reappeared, but left/right asymmetries in swing/stance durations observed after the partial lesion could disappear or reverse. It is concluded that, after a partial spinal lesion, the hindlimb locomotor pattern was actively maintained by new dynamic interactions between spinal and supraspinal levels but also by intrinsic changes within the spinal cord.
... It was shown earlier that RS neurons of the roll-and pitch-related populations receive their main vestibular input from the contralateral labyrinth Pavlova and Deliagina 2003). The second aim of the present study was to examine the relative role of the two labyrinths for generation of the yaw-related responses in RS neurons. ...
... These influences seem to be transmitted by the afferents in the posterior branch of the contralateral vestibular nerve (Pflieger and Dubuc 2004). Earlier it was shown that the RS neurons responding to tilts in the roll plane and to nose-up tilts in the pitch plane also receive their main vestibular input from the contralateral labyrinth Pavlova and Deliagina 2003). ...
When swimming, the lamprey maintains a definite orientation of its body in the vertical planes, in relation to the gravity vector, as the result of postural vestibular reflexes. Do the vestibular-driven mechanisms also play a role in the control of the direction of swimming in the horizontal (yaw) plane, in which the gravity cannot be used as a reference direction? In the present study, we addressed this question by recording responses to lateral turns in reticulospinal (RS) neurons mediating vestibulospinal reflexes. In intact lampreys, the activity of axons of RS neurons was recorded in the spinal cord by implanted electrodes. Vestibular stimulation was performed by periodical turns of the animal in the yaw plane (60 degrees peak to peak). It was found that the majority of responding RS neurons were activated by the contralateral turn. By removing one labyrinth, we found that yaw responses in RS neurons were driven mainly by input from the contralateral labyrinth. We suggest that these neurons, when activated by the contralateral turn, will elicit the ipsilateral turn and thus will compensate for perturbations of the rectilinear swimming caused by external factors. It is also known that unilateral eye illumination elicits a contralateral turn in the yaw plane (negative phototaxis). We found that a portion of RS neurons were activated by the contralateral eye illumination. By eliciting an ipsilateral turn, these neurons could mediate the negative phototaxis.
... Also, alterations in the activity of postural mechanisms caused by the vestibular deficit (e.g., Refs. 18,27,62,63) or spinal cord injury (46) have been investigated to better understand the postural mechanisms per se and the process of recovery of postural function, and to search means of promoting recovery. Specific aspects of the physiology and pathophysiology of postural control in humans are out of the scope of this paper (for review, see Ref. 38). ...
... Thus UL results in disappearance of the equilibrium point in the rollcontrol system. Experiments with recording vestibular responses in the same individual RS neurons before and soon after UL confirmed this suggestion (27,62). ...
The body posture during standing and walking is maintained due to the activity of a closed-loop control system. In the review, we consider different aspects of postural control: its functional organization, the distribution of postural functions in different parts of the central nervous system, and the activity of neuronal networks controlling posture.
Removal of a vestibular organ (unilateral labyrinthectomy, UL) in the lamprey results in a loss of equilibrium, so that the animal rolls (rotates around its longitudinal axis) when swimming. Owing to vestibular compensation, UL animals gradually restore postural equilibrium and, in a few weeks, swim without rolling. Important elements of the postural network in the lamprey are the reticulospinal (RS) neurons, which are driven by vestibular input and transmit commands for postural corrections to the spinal cord. As shown previously, a loss of equilibrium after UL is associated with disappearance of vestibular responses in the contralateral group of RS neurons. Are these responses restored in animals after compensation? To answer this question, we recorded vestibular responses in RS neurons (elicited by rotation of the compensated animal in the roll plane) by means of chronically implanted electrodes. We found that the responses re-appeared in the compensated animals. This result supports the hypothesis that the loss of equilibrium after UL was caused by asymmetry in supraspinal motor commands, and the recovery of postural control in compensated animals was due to a restoration of symmetry.
1. Fictive swimming is an experimental model to study early motor development. As vestibular activity also affects the development of spinal motor projections, the present study focused on the question whether in Xenopus laevis tadpoles, the rhythmic activity of spinal ventral roots (VR) during fictive swimming revealed age-dependent modifications after hypergravity exposure. In addition, developmental characteristics for various features of fictive swimming between stages 37/38 and 47 were determined. Parameters of interest were duration of fictive swimming episodes, burst duration, burst frequency (i.e., cycle length), and rostrocaudal delay. 2. Ventral root recordings were performed between developmental stage 37/38, which is directly after hatching and stage 47 when the hind limb buds appear. The location of recording electrodes extended from myotome 4 to 17. 3. Hypergravity exposure by 3 g-centrifugation lasted 9 to 11 days. It started when embryos had just terminated gastrulation (stage 11/19-group), when first rhythmical activity in the ventral roots appeared (stage 24/27-group), and immediately after hatching (stage 37/41-group). Ventral root recordings were taken for 8 days after termination of 3 g-exposure. 4. Between stage 37/38 (hatching) and stage 47 (hind limb bud stage) burst duration, cycle length and rostrocaudal delay recorded between the 10th and 14th postotic myotome increased while episode duration decreased significantly. In tadpoles between stage 37 and 43, the rostrocaudal delay in the proximal tail part was as long as in older tadpoles while in caudal tail parts, it was shorter. During this period of development, there was also an age-dependent progression of burst extension in the proximal tail area that could not be observed between the 10th and 14th myotome. 6. After termination of the 3 g-exposure, the mean burst duration of VR activity increased significantly (p < 0.01) when 3 g-exposure started shortly after gastrulation but not when it started thereafter. Other parameters for VR activity such as cycle length, rostrocaudal delay and episode duration were not affected by this level of hypergravity. 7. It is postulated that (i) functional separation of subunits responsible for intersegmental motor coordination starts shortly after hatching of young tadpoles; and that (ii) gravity exerts a trophic influence on the development of the vestibulospinal system during different periods of embryonic development leading to the formation of more rigid neuronal networks earlier in the spinal than in the ocular projections.
