Modifications of Vestibular Responses of Individual Reticulospinal Neurons in Lamprey Caused by Unilateral Labyrinthectomy

2002 ◽  
Vol 87 (1) ◽  
pp. 1-14 ◽  
Author(s):  
T. G. Deliagina ◽  
E. L. Pavlova
Keyword(s):  
Spinal Cord ◽  
Control System ◽  
Vestibular Stimulation ◽  
Dorsal Side ◽  
Vestibular Compensation ◽  
Directional Sensitivity ◽  
Vestibular Input ◽  
Population Activity ◽  
Postural Control System ◽  
Unilateral Labyrinthectomy

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, illumination of the eye contralateral to UL results in an immediate and reversible restoration of equilibrium. Here we used eye illumination as a tool to examine a functional recovery of the postural network. Important elements of this network are the reticulospinal (RS) neurons, which are driven by vestibular input and transmit commands for postural corrections to the spinal cord. In this study, we characterized modifications of the vestibular responses in individual RS neurons caused by UL and the effect exerted on these responses by eye illumination. The activity of RS neurons was recorded from their axons in the spinal cord by chronically implanted electrodes, and spikes in individual axons were extracted from the population activity signals. The same neurons were recorded both before and after UL. Vestibular stimulation (rotation in the roll plane through 360°) and eye illumination were performed in quiescent animals. It was found that the vestibular responses on the UL-side changed only slightly, whereas the responses on the opposite side disappeared almost completely. This asymmetry in the bilateral activity of RS neurons is the most likely cause for the loss of equilibrium in UL animals. Illumination of the eye contralateral to UL resulted, first, in a restoration of vestibular responses in the neurons inactivated by UL and in an appearance of vestibular responses in some other neurons that did not respond to vestibular input before UL. These responses had directional sensitivity and zones of spatial sensitivity similar to those observed before UL. However, their magnitude was smaller than before UL. Second, the eye illumination caused a reduction of the magnitude of vestibular responses on the UL side. These two factors tend to restore symmetry in bilateral activity of RS neurons, which is the most likely cause for the recovery of equilibrium in the swimming UL lamprey. Results of this study are discussed in relation to the model of the roll control system proposed in our previous studies as well as in relation to the vestibular compensation.

Asymmetry in the Pitch Control System of the Lamprey Caused by a Unilateral Labyrinthectomy

2003 ◽  
Vol 89 (5) ◽  
pp. 2370-2379 ◽  
Author(s):  
E. L. Pavlova ◽  
T. G. Deliagina
Keyword(s):  
Spinal Cord ◽  
Control System ◽  
Postural Control ◽  
Normal Activity ◽  
Excitatory Input ◽  
Vestibular Input ◽  
Postural Control System ◽  
Before And After ◽  
Unilateral Labyrinthectomy ◽  
Induced Changes

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 and transmit commands for postural corrections to the spinal cord. We characterized the effect of UL on vestibular responses in RS neurons elicited by rotation of the animal in the pitch plane. The activity of RS neurons was recorded from their axons in the spinal cord before and after UL. The neurons can be classified into the Up and Down groups activated preferentially with nose-up or nose-down rotation, respectively. After UL, vestibular responses in the group Up changed only slightly on the damaged side and disappeared almost completely on the opposite side. In the group Down, responses on both sides persisted after UL. These results indicate that the left and right subgroups of the group Up neurons receive excitatory input mainly from the contralateral labyrinth. In contrast, the group Down neurons receive excitatory input from both labyrinths. We conclude that the UL-induced changes in vestibular responses to pitch tilt will disturb the normal activity of the postural control system. The UL-induced asymmetry in the bilateral activity of the group Up neurons seems to be an important factor contributing to the loss of equilibrium in UL animals and to their rotation during swimming.

Responses of Reticulospinal Neurons in Intact Lamprey to Pitch Tilt

2002 ◽  
Vol 88 (3) ◽  
pp. 1136-1146 ◽  
Author(s):  
E. L. Pavlova ◽  
T. G. Deliagina
Keyword(s):  
Spinal Cord ◽  
Conduction Velocity ◽  
Longitudinal Axis ◽  
Maximal Activity ◽  
Vestibular Stimulation ◽  
Dynamic Responses ◽  
Vestibular Reflexes ◽  
Postural Control System ◽  
Roll Control ◽  
Response Group

In the swimming lamprey, a postural control system maintains a definite orientation of the animal's longitudinal axis in relation to the horizon (pitch angle). Operation of this system is based on vestibular reflexes. Important elements of the postural network are the reticulospinal (RS) neurons, which are driven by vestibular input and transmit commands for postural corrections from the brain stem to the spinal cord. Here we describe responses to vestibular stimulation (rotation of the animal in the pitch plane) in RS neurons of intact lampreys. The activity of neurons was recorded from their axons in the spinal cord by chronically implanted arrays of macroelectrodes. From the multielectrode recordings of mass activity, discharges in individual axons were extracted by means of a spike-sorting program, and the axon position in the spinal cord and its conduction velocity were determined. Vestibular stimulation was performed by rotating the animal in steps of 45° throughout 360° or by periodical “trapezoid” tilts between the nose-up and -down positions. Typically, the RS neurons exhibited both dynamic responses (activity during movement) and static responses (activity in a new sustained position). The neurons were classified into two groups according to their pattern of response. Group up neurons responded preferentially to nose-up rotation with maximal activity at 0–135° up. Group down neurons responded preferentially to nose-down rotation with maximal activity at 0–135° down. Neurons of the two groups also differed in the position of their axons in the spinal cord and axonal conduction velocity. An increase in water temperature, which presumably causes a downward turn in swimming lampreys, affected the activity in the up anddown groups differently, so that the ratio upresponses to down responses increased. We suggest that theup and down groups mediate the opposing vestibular reflexes and cause the downward and upward turns of the animal, respectively. The lamprey will stabilize the orientation in the pitch plane at which the effects of up and downgroups are equal to each other. In addition to the main test (rotation in the pitch plane), the animals were also tested by rotation in the transverse (roll) plane. It was found that 22% of RS neurons responding to pitch tilts also responded to roll tilts. The overlap between the pitch and roll populations suggests that the RS pathways are partly shared by the pitch and roll control systems.

Postural Control in the Lamprey: A Study With a Neuro-Mechanical Model

2000 ◽  
Vol 84 (6) ◽  
pp. 2880-2887 ◽  
Author(s):  
P. V. Zelenin ◽  
T. G. Deliagina ◽  
S. Grillner ◽  
G. N. Orlovsky
Keyword(s):  
Spinal Cord ◽  
Postural Control ◽  
Mechanical Model ◽  
Dorsal Side ◽  
Postural Control System ◽  
Lateral Tilt ◽  
Normal Orientation ◽  
Postural Stabilization ◽  
Left And Right ◽  
Vestibular Organs

The swimming lamprey normally maintains the dorsal-side-up orientation due to activity of the postural control system driven by vestibular organs. Commands for postural corrections are transmitted from the brain stem to the spinal cord mainly by the reticulospinal (RS) pathways. As shown in previous studies, RS neurons are activated by contralateral roll tilt, they exhibit a strong dynamic response, but much weaker static response. Here we test a hypothesis that decoding of these commands in the spinal cord is based on the subtraction of signals in the left and right RS pathways. In this study, we used a neuro-mechanical model. An intact lamprey was mounted on a platform that restrained its postural activity but allowed lateral locomotor undulations to occur. The activity in the left and right RS pathways was recorded by implanted electrodes. These natural biological signals were then used to control an electrical motor rotating the animal around its longitudinal axis toward the stronger signal. It was found that this “hybrid” system automatically stabilized a normal orientation of the lamprey in the gravitational field. The system compensated for large postural disturbances (lateral tilt up to ±180°) due to wide angular zones of the gravitational sensitivity of RS neurons. In the nonswimming lamprey, activity of RS neurons and their vestibular responses were considerably reduced, and the system was not able to stabilize the normal orientation. However, the balance could be restored by imposing small oscillations on the lamprey, which elicited additional activation of the vestibular organs. This finding indicates that head oscillations caused by locomotor movements may contribute to postural stabilization. In addition to postural stabilization, the neuro-mechanical model reproduced a number of postural effects characteristic of the lamprey: 1) unilateral eye illumination elicited a lateral tilt (“dorsal light response”) due to a shift of the equilibrium point in the vestibular-driven postural network; 2) removal of one labyrinth resulted in a loss of postural control due to an induced left-right asymmetry in the vestibulo-reticulospinal reflexes, which 3) could be compensated for by asymmetrical visual input. The main conclusion of the present study is that natural supraspinal commands for postural corrections in the roll plane can be effectively decoded on the basis of subtraction of the effects of signals delivered by the left and right RS pathways. Possible mechanisms for this transformation are discussed.

Responses of Reticulospinal Neurons in Intact Lamprey to Vestibular and Visual Inputs

2000 ◽  
Vol 83 (2) ◽  
pp. 864-878 ◽  
Author(s):  
T. G. Deliagina ◽  
P. Fagerstedt
Keyword(s):  
Spinal Cord ◽  
Control System ◽  
Conduction Velocity ◽  
Visual Stimuli ◽  
Vestibular Stimulation ◽  
Dynamic Responses ◽  
Reticulospinal Neurons ◽  
Static Responses ◽  
Contralateral Eye ◽  
Group 1

A lamprey maintains the dorsal-side-up orientation due to the activity of postural control system driven by vestibular input. Visual input can affect the body orientation: illumination of one eye evokes ipsilateral roll tilt. An important element of the postural network is the reticulospinal (RS) neurons transmitting commands from the brain stem to the spinal cord. Here we describe responses to vestibular and visual stimuli in RS neurons of the intact lamprey. We recorded activity from the axons of larger RS neurons with six extracellular electrodes chronically implanted on the surface of the spinal cord. From these multielectrode recordings of mass activity, discharges in individual axons were extracted by means of a spike-sorting program, and the axon position in the spinal cord and its conduction velocity were determined. Vestibular stimulation was performed by rotating the animal around its longitudinal axis in steps of 45° through 360°. Nonpatterned visual stimulation was performed by unilateral eye illumination. All RS neurons were classified into two groups depending on their pattern of response to vestibular and visual stimuli; the groups also differed in the axon position in the spinal cord and its conduction velocity. Each group consisted of two symmetrical, left and right, subgroups. In group 1neurons, rotation of the animal evoked both dynamic and static responses; these responses were much larger when rotation was directed toward the contralateral labyrinth, and the dynamic responses to stepwise rotation occurred at any initial orientation of the animal, but they were more pronounced within the angular zone of 0–135°. The zone of static responses approximately coincided with the zone of pronounced dynamic responses. The group 1 neurons received excitatory input from the ipsilateral eye and inhibitory input from the contralateral eye. When vestibular stimulation was combined with illumination of the ipsilateral eye, both dynamic and static vestibular responses were augmented. Contralateral eye illumination caused a decrease of both types of responses. Group 2neurons responded dynamically to rotation in both directions throughout 360°. They received excitatory inputs from both eyes. Axons of the group 2 neurons had higher conduction velocity and were located more medially in the spinal cord as compared with the group 1 neurons. We suggest that the reticulospinal neurons of group 1 constitute an essential part of the postural network in the lamprey. They transmit orientation-dependent command signals to the spinal cord causing postural corrections. The role of these neurons is discussed in relation to the model of the roll control system formulated in our previous studies.

scholarly journals Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

2020 ◽  
Vol 100 (1) ◽  
pp. 271-320 ◽  
Author(s):  
Sten Grillner ◽  
Abdeljabbar El Manira
Keyword(s):  
Spinal Cord ◽  
Control System ◽  
High Speed ◽  
Postural Control System ◽  
The Core ◽  
Level Of Activity ◽  
The Subject ◽  
Command Systems ◽  
The Brain ◽  
Sensory Compensation

The vertebrate control of locomotion involves all levels of the nervous system from cortex to the spinal cord. Here, we aim to cover all main aspects of this complex behavior, from the operation of the microcircuits in the spinal cord to the systems and behavioral levels and extend from mammalian locomotion to the basic undulatory movements of lamprey and fish. The cellular basis of propulsion represents the core of the control system, and it involves the spinal central pattern generator networks (CPGs) controlling the timing of different muscles, the sensory compensation for perturbations, and the brain stem command systems controlling the level of activity of the CPGs and the speed of locomotion. The forebrain and in particular the basal ganglia are involved in determining which motor programs should be recruited at a given point of time and can both initiate and stop locomotor activity. The propulsive control system needs to be integrated with the postural control system to maintain body orientation. Moreover, the locomotor movements need to be steered so that the subject approaches the goal of the locomotor episode, or avoids colliding with elements in the environment or simply escapes at high speed. These different aspects will all be covered in the review.

scholarly journals Effects of galvanic vestibular stimulation on postural limb reflexes and neurons of spinal postural network

2012 ◽  
Vol 108 (1) ◽  
pp. 300-313 ◽  
Author(s):  
L.-J. Hsu ◽  
P. V. Zelenin ◽  
G. N. Orlovsky ◽  
T. G. Deliagina
Keyword(s):  
Vestibular Stimulation ◽  
Afferent Input ◽  
Galvanic Vestibular Stimulation ◽  
Dorsal Side ◽  
Body Orientation ◽  
Cathode Side ◽  
Body Sway ◽  
Postural Control System ◽  
Opposite Pattern ◽  
Neuronal Mechanisms

Quadrupeds maintain the dorsal side up body orientation due to the activity of the postural control system driven by limb mechanoreceptors. Binaural galvanic vestibular stimulation (GVS) causes a lateral body sway toward the anode. Previously, we have shown that this new position is actively stabilized, suggesting that GVS changes a set point in the reflex mechanisms controlling body posture. The aim of the present study was to reveal the underlying neuronal mechanisms. Experiments were performed on decerebrate rabbits. The vertebral column was rigidly fixed, whereas hindlimbs were positioned on a platform. Periodic lateral tilts of the platform caused postural limb reflexes (PLRs): activation of extensors in the loaded and flexing limb and a decrease in extensor activity in the opposite (unloaded and extending) limb. Putative spinal interneurons were recorded in segments L4–L5 during PLRs, with and without GVS. We have found that GVS enhanced PLRs on the cathode side and reduced them on the anode side. This asymmetry in PLRs can account for changes in the stabilized body orientation observed in normal rabbits subjected to continuous GVS. Responses to platform tilts (frequency modulation) were observed in 106 spinal neurons, suggesting that they can contribute to PLR generation. Two neuron groups were active in opposite phases of the tilt cycle of the ipsi-limb: F-neurons in the flexion phase, and E-neurons in the extension phase. Neurons were driven mainly by afferent input from the ipsi-limb. If one supposes that F- and E-neurons contribute, respectively, to excitation and inhibition of extensor motoneurons, one can expect that the pattern of response to GVS in F-neurons will be similar to that in extensor muscles, whereas E-neurons will have an opposite pattern. We have found that ∼40% of all modulated neurons meet this condition, suggesting that they contribute to the generation of PLRs and to the GVS-caused changes in PLRs.

scholarly journals Effects of Galvanic Vestibular Stimulation on Vestibular Compensation in Unilaterally Labyrinthectomized Mice

2021 ◽  
Vol 12 ◽  
Author(s):  
Gi-Sung Nam ◽  
Thanh Tin Nguyen ◽  
Jin-Ju Kang ◽  
Gyu Cheol Han ◽  
Sun-Young Oh
Keyword(s):  
Path Length ◽  
Vestibular Stimulation ◽  
Galvanic Vestibular Stimulation ◽  
Vestibular Compensation ◽  
Ocular Reflex ◽  
Total Path Length ◽  
Vestibulo Ocular Reflex ◽  
Unilateral Labyrinthectomy ◽  
Unilateral Vestibular Deafferentation ◽  
Baseline Values

Objectives: To investigate the ameliorating effects of sinusoidal galvanic vestibular stimulation (GVS) on vestibular compensation from unilateral vestibular deafferentation (UVD) using a mouse model of unilateral labyrinthectomy (UL).Methods: Sixteen male C57BL/6 mice were allocated into two groups that comprise UL groups with GVS (GVS group, n = 9) and without GVS intervention (non-GVS group, n = 7). In the experimental groups, we assessed vestibulo-ocular reflex (VOR) recovery before (baseline) and at 3, 7, and 14 days after surgical unilateral labyrinthectomy. In the GVS group, stimulation was applied for 30 min daily from postoperative days (PODs) 0–4 via electrodes inserted subcutaneously next to both bony labyrinths.Results: Locomotion and VOR were significantly impaired in the non-GVS group compared to baseline. The mean VOR gain of the non-GVS group was attenuated to 0.23 at POD 3 and recovered continuously to the value of 0.54 at POD 14, but did not reach the baseline values at any frequency. GVS intervention significantly accelerated recovery of locomotion, as assessed by the amount of circling and total path length in the open field tasks compared to the non-GVS groups on PODs 3 (p < 0.001 in both amount of circling and total path length) and 7 (p < 0.01 in amount of circling and p < 0.001 in total path length, Mann–Whitney U-test). GVS also significantly improved VOR gain compared to the non-GVS groups at PODs 3 (p < 0.001), 7 (p < 0.001), and 14 (p < 0.001, independent t-tests) during sinusoidal rotations. In addition, the recovery of the phase responses and asymmetry of the VOR was significantly better in the GVS group than in the non-GVS group until 2 weeks after UVD (phase, p = 0.001; symmetry, p < 0.001 at POD 14).Conclusion: Recoveries for UVD-induced locomotion and VOR deficits were accelerated by an early intervention with GVS, which implies that GVS has the potential to improve vestibular compensation in patients with acute unilateral vestibular failure.

scholarly journals The Differential Effects of Acute Right- vs. Left-Sided Vestibular Deafferentation on Spatial Cognition in Unilateral Labyrinthectomized Mice

2021 ◽  
Vol 12 ◽  
Author(s):  
Thanh Tin Nguyen ◽  
Gi-Sung Nam ◽  
Jin-Ju Kang ◽  
Gyu Cheol Han ◽  
Ji-Soo Kim ◽  
...  
Keyword(s):  
Spatial Cognition ◽  
Motor Coordination ◽  
Spatial Working Memory ◽  
Spatial Navigation ◽  
Vestibular Stimulation ◽  
Current Data ◽  
Control Group ◽  
Y Maze ◽  
Lesion Side ◽  
Unilateral Labyrinthectomy

This study aimed to investigate the disparity in locomotor and spatial memory deficits caused by left- or right-sided unilateral vestibular deafferentation (UVD) using a mouse model of unilateral labyrinthectomy (UL) and to examine the effects of galvanic vestibular stimulation (GVS) on the deficits over 14 days. Five experimental groups were established: the left-sided and right-sided UL (Lt.-UL and Rt.-UL) groups, left-sided and right-sided UL with bipolar GVS with the cathode on the lesion side (Lt.-GVS and Rt.-GVS) groups, and a control group with sham surgery. We assessed the locomotor and cognitive-behavioral functions using the open field (OF), Y maze, and Morris water maze (MWM) tests before (baseline) and 3, 7, and 14 days after surgical UL in each group. On postoperative day (POD) 3, locomotion and spatial working memory were more impaired in the Lt.-UL group compared with the Rt.-UL group (p < 0.01, Tamhane test). On POD 7, there was a substantial difference between the groups; the locomotion and spatial navigation of the Lt.-UL group recovered significantly more slowly compared with those of the Rt.-UL group. Although the differences in the short-term spatial cognition and motor coordination were resolved by POD 14, the long-term spatial navigation deficits assessed by the MWM were significantly worse in the Lt.-UL group compared with the Rt.-UL group. GVS intervention accelerated the vestibular compensation in both the Lt.-GVS and Rt.-GVS groups in terms of improvement of locomotion and spatial cognition. The current data imply that right- and left-sided UVD impair spatial cognition and locomotion differently and result in different compensatory patterns. Sequential bipolar GVS when the cathode (stimulating) was assigned to the lesion side accelerated recovery for UVD-induced spatial cognition, which may have implications for managing the patients with spatial cognitive impairment, especially that induced by unilateral peripheral vestibular damage on the dominant side.

Directional sensitivity of neurons in the lumbar spinal cord to neck rotation

1984 ◽  
Vol 323 (1) ◽  
pp. 172-175 ◽  
Author(s):  
E.E. Brink ◽  
I. Suzuki ◽  
S.J.B. Timerick ◽  
V.J. Wilson
Keyword(s):  
Spinal Cord ◽  
Lumbar Spinal Cord ◽  
Directional Sensitivity ◽  
Neck Rotation ◽  
Lumbar Spinal
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