Neuronal Activity in the Vestibular Nuclei After Contralateral or Bilateral Labyrinthectomy in the Alert Guinea Pig

1998 ◽  
Vol 80 (5) ◽  
pp. 2352-2367 ◽  
Author(s):  
Laurence Ris ◽  
Emile Godaux
Keyword(s):  
Guinea Pig ◽  
Vestibular Nuclei ◽  
Acute Stage ◽  
Second Order ◽  
Inhibitory Influence ◽  
Type I ◽  
Vestibular Neurons ◽  
Unilateral Labyrinthectomy ◽  
Resting Activity ◽  
Control State

Ris, Laurence and Emile Godaux. Neuronal activity in the vestibular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig. J. Neurophysiol. 80: 2352–2367, 1998. In the guinea pig, a unilateral labyrinthectomy is followed by an initial depression and a subsequent restoration of the spontaneous activity in the neurons of the ipsilateral vestibular nuclei. In two previous works, we have established the time course of these changes in the alert guinea pig using electrical stimulation as a search stimulus to select the analyzed neurons. The latter criterion was important to capture the many ipsilateral neurons that are silent at rest during the immediate postlabyrinthectomy stage. Because it is known that a pathway originating from the vestibular nuclei on one side crosses the midline and functionally inhibits the activity of the vestibular nuclei on the other side, we investigated in the first part of this study the spiking behavior of the neurons in the vestibular nuclei contralateral to the labyrinthectomy using the same procedure as that used for the ipsilateral neurons. The spiking behavior of 976 neurons was studied during 4-h recording sessions in intact animals and 1 h, 1 day, 2 days, or 1 wk postlabyrinthectomy. Neurons selected according to the electrical activation criterion were classified further as type I (their firing rate increased during ipsilateral rotation), type II (their firing rate increased during contralateral rotation), or unresponsive. The resting activity of type I neurons, which was 38.1 ± 20.9 spikes/s (mean ± SD) in the control state, increased statistically significantly 1 h after the lesion (53.3 ± 29.1 spikes/s) and remained at this level 1 wk later (56.0 ± 20.3 spikes/s). The sensitivity of type I units, which was 0.80 ± 0.46 spikes/s per deg/s in the control population, decreased to 0.49 ± 0.26 spikes/s per deg/s 1 h after the lesion and remained at this level 1 wk later (0.50 ± 0.39 spikes/s per deg/s). When all monosynaptically activated neurons (type I, type II, unresponsive) were pooled, the sensitivity to horizontal rotation fell from 0.58 ± 0.51 spikes/s per deg/s in the control state to 0.15 ± 0.25 spikes/s per deg/s 1 h after the lesion and to 0.20 ± 0.32 spikes/s per deg/s 1 wk later. The major findings of the first part of this study in the alert guinea pig are thus in accord with those of Curthoys et al. and Smith and Curthoys in anesthetized guinea pigs. In the second part of this work, we studied the spiking behavior of the neurons in the vestibular nuclei after bilateral labyrinthectomy. After unilateral labyrinthectomy, the resting discharge of the ipsilateral monosynaptically activated vestibular neurons fell from 36.9 ± 21 spikes/s (basal activity) to 6.7 ± 17.0 spikes/s 1 h after the lesion and then recovered, reaching 17.4 ± 18.9 and 40.8 ± 23.7 spikes/s 1 day and 1 wk after the lesion, respectively. These observations raise the two following questions. What are the relative contributions of the loss of the excitatory influence from the ipsilateral labyrinth (destroyed) and of the persistence of the inhibitory influence from the contralateral labyrinth (intact) in the labyrinthectomy-induced depression of activity? And are the left-right asymmetries caused by a unilateral labyrinthectomy the driving force for restoration of activity? Here, we addressed these two questions by studying the spiking behavior of 473 second-order vestibular neurons in the alert guinea pig after a bilateral labyrinthectomy. In the acute stage, 1 h after bilateral labyrinthectomy, the resting discharge of the second-order vestibular neurons was 16.2 ± 22.4 spikes/s. From comparison with the results obtained in the acute stage after a unilateral labyrinthectomy, we inferred that the ipsilateral excitatory influence was between two and three times more powerful than the contralateral inhibitory influence. After bilateral labyrinthectomy as well as after unilateral labyrinthectomy, the resting activity of the second-order vestibular neurons returned to normal, reaching 20.8 ± 23.1 spikes/s 1 day after the lesion and 38.6 ± 21.1 spikes/s 1 wk after the lesion. From this fact, we concluded that the left-right asymmetries caused by a unilateral labyrinthectomy were not the error signals inducing the restoration of activity.

Neuronal activity in the ipsilateral vestibular nucleus following unilateral labyrinthectomy in the alert guinea pig

1995 ◽  
Vol 74 (5) ◽  
pp. 2087-2099 ◽  
Author(s):  
L. Ris ◽  
C. de Waele ◽  
M. Serafin ◽  
P. P. Vidal ◽  
E. Godaux
Keyword(s):  
Guinea Pig ◽  
Vestibular Nucleus ◽  
Head Rotation ◽  
Second Order ◽  
Vestibular Nerve ◽  
Control Group ◽  
Head Velocity ◽  
Vestibular Neurons ◽  
Unilateral Labyrinthectomy ◽  
Control State

1. Neuronal activity was investigated in the left superior vestibular nucleus (SVN), lateral vestibular nucleus (LVN), and rostral part of the medial vestibular nucleus (MVN) in the alert guinea pig after a unilateral (left) labyrinthectomy was performed. Vestibular neurons were recorded either immediately (just-postoperative group, n = 6) or 1 wk after labyrinthectomy (1-wk-postoperative group, n = 6) and compared with the activity recorded in intact animals (control group, n = 6). 2. Animals were prepared for extracellular recording of single-unit activity and for eye movement recording (scleral search coil technique). To enable stimulation of the left vestibular nerve, bipolar silver ball electrodes were chronically implanted either in contact with the bony labyrinth in the control group or close to the stump of the vestibular nerve after labyrinthectomy. Complete labyrinthectomy was performed under halothane anesthesia. 3. The criterion used to select vestibular neurons for analysis was their recruitment by an electric shock on the vestibular nerve. Of the 589 recorded neurons, 424, defined as second-order vestibular neurons, were recruited at monosynaptic latencies (0.85-1.15 ms) and 165 were recruited at polysynaptic latencies. One hundred three second-order vestibular neurons were recorded in the control group, 173 in the just-postoperative group, and 148 in the 1-wk-postoperative group. 4. The activity of the electrically recruited neurons was recorded during sinusoidal horizontal head rotation in the dark (0.3 Hz, 40 degrees/s peak velocity). The behavior of the neurons was analyzed by plotting their firing rate against head velocity. The Y-intercept of the regression line was used to express spontaneous firing rate (resting discharge), and its slope was used to express the sensitivity of the neuron-to-head velocity. 5. In the absence of statistically significant difference between the characteristics of the neuronal discharge of the second-order vestibular neurons recorded in the SVN, LVN, and rostral MVN, the data were pooled. The Resting discharge of these cells amounted to 41.0 +/- 24.7 (SD) spikes/s in the control state, fell to 7.2 +/- 13.9 spikes/s just after labyrinthectomy, and completely returned to normal values 1 wk after surgery (42.5 +/- 21.6 spikes/s). Among the monosynaptically recruited neurons, the percentage of silent units was 0% in the control group, 69% in the just-postoperative group, and 0% in the 1-wk-postoperative group. 6. By contrast, the sensitivity to head velocity of the second-order vestibular neurons, which was 0.69 +/- 0.48 (SD) spikes.s-1/deg.s-1 in the control state and which fell to 0.03 +/- 0.11 spikes.s-1/deg.s-1 just after labyrinthectomy, remained low 1 wk after injury (0.21 +/- 0.26 spikes.s-1/deg.s-1). Moreover, the slight recovery of sensitivity to head rotation was due only to units behaving as type II neurons. 7. The mean resting discharge of the polysynaptically recruited neurons (pooled from the 3 explored nuclei) was 31.6 +/- 19.3 spikes/s in the control group. It decreased to 11.6 +/- 12.1 spikes/s in the just-postoperative group and recovered to 39.8 +/- 20.2 spikes/s in the 1-wk-postoperative group. No neuron was silent at rest either in the control group or in the 1-wk-postoperative group. Just after labyrinthectomy, 35% of the neurons had a null resting activity. The mean sensitivity to head velocity of these neurons was 0.55 +/- 0.42 spikes.s-1/deg.s-1 in the control group. It decreased to 0.05 +/- 0.12 spikes.s-1/deg.s-1 in the just-postoperative group and recovered to 0.22 +/- 0.17 spikes.s-1/deg.s-1 in the 1-wk-postoperative group. 8. We conclude that, at least in the guinea pig, the restoration of the spontaneous activity of the deafferented neurons is complete 1 wk after a unilateral labyrinthectomy and thus probably plays an important role in vestibular compensation...

scholarly journals Responses of non-eye-movement central vestibular neurons to sinusoidal yaw rotation in compensated macaques after unilateral semicircular canal plugging

2016 ◽  
Vol 116 (4) ◽  
pp. 1871-1884 ◽  
Author(s):  
Shawn D. Newlands ◽  
Min Wei ◽  
David Morgan ◽  
Hongge Luan
Keyword(s):  
Eye Movement ◽  
Semicircular Canal ◽  
Vestibular Nuclei ◽  
Type I ◽  
Type Ii ◽  
Central Type ◽  
Vestibular Neurons ◽  
Unilateral Labyrinthectomy ◽  
Resting Activity ◽  
The Difference

After vestibular labyrinth injury, behavioral measures of vestibular performance recover to variable degrees (vestibular compensation). Central neuronal responses after unilateral labyrinthectomy (UL), which eliminates both afferent resting activity and sensitivity to movement, have been well-studied. However, unilateral semicircular canal plugging (UCP), which attenuates angular-velocity detection while leaving afferent resting activity intact, has not been extensively studied. The current study reports response properties of yaw-sensitive non-eye-movement rhesus macaque vestibular neurons after compensation from UCP. The responses at a series of frequencies (0.1–2 Hz) and peak velocities (15–210°/s) were compared between neurons recorded before and at least 6 wk after UCP. The gain (sp/s/°/s) of central type I neurons (responding to ipsilateral yaw rotation) on the side of UCP was reduced relative to normal controls at 0.5 Hz, ±60°/s [0.48 ± 0.30 (SD) normal, 0.32 ± 0.15 ipsilesion; 0.44 ± 0.2 contralesion]. Type II neurons (responding to contralateral yaw rotation) after UCP have reduced gain (0.40 ± 0.27 normal, 0.35 ± 0.25 ipsilesion; 0.25 ± 0.18 contralesion). The difference between responses after UCP and after UL is primarily the distribution of type I and type II neurons in the vestibular nuclei (type I neurons comprise 66% in vestibular nuclei normally; 51% ipsilesion UCP; 59% contralesion UCP; 38% ipsilesion UL; 65% contralesion UL) and the magnitude of the responses of type II neurons ipsilateral to the lesion. These differences suggest that the need to compensate for unilateral loss of resting vestibular nerve activity after UL necessitates a different strategy for recovery of dynamic vestibular responses compared to after UCP.

scholarly journals Differential Spatial Organization of Otolith Signals in Frog Vestibular Nuclei

2003 ◽  
Vol 90 (5) ◽  
pp. 3501-3512 ◽  
Author(s):  
Hans Straka ◽  
Stefan Holler ◽  
Fumiyuki Goto ◽  
Florian P. Kolb ◽  
Edwin Gilland
Keyword(s):  
Spatial Organization ◽  
Vestibular Nucleus ◽  
Field Potential ◽  
Vestibular Function ◽  
Vestibular Nuclei ◽  
Second Order ◽  
Vestibular Neurons ◽  
Dorsal Nucleus ◽  
Sensory Map ◽  
Saccular Nerve

Activation maps of pre- and postsynaptic field potential components evoked by separate electrical stimulation of utricular, lagenar, and saccular nerve branches in the isolated frog hindbrain were recorded within a stereotactic outline of the vestibular nuclei. Utricular and lagenar nerve-evoked activation maps overlapped strongly in the lateral and descending vestibular nuclei, whereas lagenar amplitudes were greater in the superior vestibular nucleus. In contrast, the saccular nerve-evoked activation map coincided largely with the dorsal nucleus and the adjacent dorsal part of the lateral vestibular nucleus, corroborating a major auditory and lesser vestibular function of the frog saccule. The stereotactic position of individual second-order otolith neurons matched the distribution of the corresponding otolith nerve-evoked activation maps. Furthermore, particular types of second-order utricular and lagenar neurons were clustered with particular types of second-order canal neurons in a topology that anatomically mirrored the preferred convergence pattern of afferent otolith and canal signals in second-order vestibular neurons. Similarities in the spatial organization of functionally equivalent types of second-order otolith and canal neurons between frog and other vertebrates indicated conservation of a common topographical organization principle. However, the absence of a precise afferent sensory topography combined with the presence of spatially segregated groups of particular second-order vestibular neurons suggests that the vestibular circuitry is organized as a premotor map rather than an organotypical sensory map. Moreover, the conserved segmental location of individual vestibular neuronal phenotypes shows linkage of individual components of vestibulomotor pathways with the underlying genetically specified rhombomeric framework.

scholarly journals Responses of central vestibular neurons to sinusoidal yaw rotation in compensated macaques after unilateral labyrinthectomy

2013 ◽  
Vol 110 (8) ◽  
pp. 1822-1836 ◽  
Author(s):  
Shawn D. Newlands ◽  
Min Wei
Keyword(s):  
Vestibular Nucleus ◽  
Vestibular Function ◽  
Neuronal Firing ◽  
Type I ◽  
Vestibular Neurons ◽  
Dynamic Function ◽  
Individual Type ◽  
Vestibular Commissures ◽  
Unilateral Labyrinthectomy ◽  
Contralateral Rotation

After vestibular labyrinth injury, behavioral measures of vestibular function partially recover through the process of vestibular compensation. The present study was performed to improve our understanding of the physiology of macaque vestibular nucleus neurons in the compensated state (>6 wk) after unilateral labyrinthectomy (UL). The responses of neurons to sinusoidal yaw rotation at a series of frequencies (0.1–2.0 Hz) and peak velocities (7.5–210°/s) were examined to determine how the behavior of these cells differed from those in animals with intact labyrinths. The sensitivity of neurons responding to ipsilateral rotation (type I) did not differ between the intact and injured sides after UL, although this sensitivity was lower bilaterally after lesion than before lesion. The sensitivity of neurons that increase firing with contralateral rotation (type II) was higher ipsilateral to the UL than before lesion or in the nucleus contralateral to the UL. UL did not increase asymmetry in the responses of individual type I or II neurons to ipsilateral vs. contralateral rotation, nor does it change the power law relationship between neuronal firing and level of stimulation. Increased sensitivities of contralesional type I neurons to the remaining vestibular nerve input and increased efficacy of inhibitory vestibular commissures projecting to the ipsilesional vestibular nucleus appear to be responsible for recovery of dynamic function of central vestibular neurons in compensated animals. The portion of type I neurons on the ipsilesional side is reduced in compensated animals, which likely accounts for the asymmetries in vestibular reflexes and perception that characterize vestibular function after UL.

scholarly journals Tests of linearity in the responses of eye-movement-sensitive vestibular neurons to sinusoidal yaw rotation

2013 ◽  
Vol 109 (10) ◽  
pp. 2571-2584 ◽  
Author(s):  
Shawn D. Newlands ◽  
Min Wei
Keyword(s):  
Eye Movement ◽  
Dynamic Range ◽  
Peak Velocity ◽  
Vestibular Nuclei ◽  
Head Movements ◽  
Type I ◽  
Vestibular Neurons ◽  
Ocular Reflex ◽  
Vestibulo Ocular Reflex ◽  
Vestibular Nuclear Neurons

The rotational vestibulo-ocular reflex in primates is linear and stabilizes gaze in space over a large range of head movements. Best evidence suggests that position-vestibular-pause (PVP) and eye-head velocity (EHV) neurons in the vestibular nuclei are the primary mediators of vestibulo-ocular reflexes for rotational head movements, yet the linearity of these neurons has not been extensively tested. The current study was undertaken to understand how varying magnitudes of yaw rotation are coded in these neurons. Sixty-six PVP and 41 EHV neurons in the rostral vestibular nuclei of 7 awake rhesus macaques were recorded over a range of frequencies (0.1 to 2 Hz) and peak velocities (7.5 to 210°/s at 0.5 Hz). The sensitivity (gain) of the neurons decreased with increasing peak velocity of rotation for all PVP neurons and EHV neurons sensitive to ipsilateral rotation (type I). The sensitivity of contralateral rotation-sensitive (type II) EHV neurons did not significantly decrease with increasing peak velocity. These data show that, like non-eye-movement-related vestibular nuclear neurons that are believed to mediate nonlinear vestibular functions, PVP neurons involved in the linear vestibulo-ocular reflex also behave in a nonlinear fashion. Similar to other sensory nuclei, the magnitude of the vestibular stimulus is not linearly coded by the responses of vestibular neurons; rather, amplitude compression extends the dynamic range of PVP and type I EHV vestibular neurons.

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