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

Abstract

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 g...

Firing Properties of Head Direction Cells in the Rat Anterior Thalamic Nucleus: Dependence on Vestibular Input

“…It is noteworthy that intratympanic sodium arsanilate led to the degeneration of the vestibular nerve in rats (Chen et al, 1986) and that the spontaneous activity of central vestibular neurons recovers after bilateral vestibular nerve transection (Waespe et al, 1992) or unilateral surgical labyrinthectomy (Ris et al, 1995). Furthermore, Ris et al (1995) reported that despite compensatory changes after unilateral labyrinthectomy, angular head rotation failed to modulate brainstem vestibular neuron firing rates.…”

“…However, complete recovery of the spontaneous activity of central vestibular neurons has been reported 7 days after unilateral surgical labyrinthectomy in alert guinea pigs (Ris et al, 1995) and 6 months after bilateral transection of the vestibular nerve in alert rhesus monkeys (Waespe et al, 1992). Despite the potential for compensatory activity of the intact side in the unilateral labyrinthectomy studies (Kaufman et al, 1992;Ris et al, 1995), angular head rotation failed to influence expression of Fos in ipsilateral brainstem vestibular circuits (Kaufman et al, 1992) and did not modulate the firing rates of ipsilateral brainstem vestibular neurons (Ris et al, 1995). These data indicate that although unilateral surgical and arsanilate-induced labyrinthectomies disrupt rotation-induced changes in the activity of brainstem vestibular circuitry, brainstem vestibular nuclei remain intact.…”

Long-Term Plasticity of Ipsilesional Medial Vestibular Nucleus Neurons After Unilateral Labyrinthectomy

“…After the loss of vestibular nerve afferents induced in vivo by UL, the mean resting potential of the ipsilesional MVNn should then become more hyperpolarized. In the guinea pig, there is a complete in vivo recovery of the spontaneous discharge of the deafferented MVNn during the first week of compensation (Ris et al 1995(Ris et al , 1997. On the other hand, the in vitro studies demonstrate only moderate modifications of the spontaneous resting discharge and resting membrane potential of the ipsilesional MVNn in slices taken after 1 wk of compensation, restricted to type B neurons (Him and Dutia 2001;Ris et al 2001cRis et al , 2002.…”

“…This imbalance is responsible for the deficits triggered by the lesion. During the first week after UL, the recovery of a normal resting discharge by the ipsilesional medial VNn (MVNn) plays a key role in the disappearance of the static syndrome by restoring the balance between the activity of neurons in both vestibular nuclei (Ris et al 1995(Ris et al , 1997. Because the ipsilesional labyrinth afferents stay silent (Jensen 1979;Sirkin et al 1984), this recovery is a model of plasticity in the CNS.…”

Physiological changes of premotor nonspiking interneurons in the central compensation of eyestalk posture following unilateral sensory ablation in crayfish

“…After a short period, this asymmetry disappears and the behavioral syndromes caused by unilateral labyrinthectomy diminish in parallel with the physiological recovery. (Hamann and Lannou 1987;Smith Fujisawa and Takahata -26-and Curthoys 1988a,b;Ris et al 1995Ris et al , 1997Newlands and Perachio 1990a, b). To explain this physiological recovery of bilaterally symmetrical resting discharge, Vibert and his colleagues (1999) proposed that the vestibular compensation follows a "top-down" strategy: it would first rely on the external cues given by the intact sensor systems, then on an internal reorganization of the vestibular-related networks, and finally on changes in the intrinsic pacemaker properties of the vestibular neurons themselves.…”