Physiological and Anatomical Properties of Mouse Medial Vestibular Nucleus Neurons Projecting to the Oculomotor Nucleus

2006 ◽  
Vol 95 (5) ◽  
pp. 3012-3023 ◽  
Author(s):  
Chris Sekirnjak ◽  
Sascha du Lac
Keyword(s):  
Vestibular Nucleus ◽  
High Sensitivity ◽  
Current Injection ◽  
Head Movements ◽  
Membrane Properties ◽  
Medial Vestibular Nucleus ◽  
Oculomotor Nucleus ◽  
Response Dynamics ◽  
Tracer Injection ◽  
Membrane Hyperpolarization

Neurons in the medial vestibular nucleus (MVN) vary in their projection patterns, responses to head movement, and intrinsic firing properties. To establish whether neurons that participate in the vestibulo-ocular reflex (VOR) have distinct intrinsic physiological properties, oculomotor nucleus (OMN)–projecting neurons were identified in mouse brainstem slices by fluorescent retrograde labeling from the oculomotor complex and targeted for patch-clamp recordings. Such neurons were located in the magnocellular portion of the MVN contralateral to tracer injection, were mostly multipolar, and had soma diameters of around 20 μm. They fired spontaneous action potentials at rates higher than those of other MVN neurons and their spikes were of unusually short duration. OMN-projecting neurons responded to 1-s intracellular current injection with exceptionally high firing rates of >500 spikes/s. Their current–firing relationship was highly linear, with weak firing response adaptation during steady depolarization and little postinhibitory rebound firing after membrane hyperpolarization. Their firing responses were approximately in phase with sinusoidal current injection. The response dynamics of OMN-projecting neurons could be simulated with a simple integrate-and-fire model modified with the addition of small adaptation and rebound conductances. These findings indicate that the membrane properties of OMN-projecting neurons allow them to respond to head movements reliably and with high sensitivity but without substantially altering input dynamics.

Unilateral Labyrinthectomy Modifies the Membrane Properties of Contralesional Vestibular Neurons

2004 ◽  
Vol 92 (3) ◽  
pp. 1668-1684 ◽  
Author(s):  
Mathieu Beraneck ◽  
Erwin Idoux ◽  
Atsuhiko Uno ◽  
Pierre-Paul Vidal ◽  
Lee E. Moore ◽  
...  
Keyword(s):  
Type A ◽  
Head Movements ◽  
Vestibular Compensation ◽  
Membrane Properties ◽  
Medial Vestibular Nucleus ◽  
Type B ◽  
Response Dynamics ◽  
Vestibular Reflexes ◽  
Unilateral Labyrinthectomy ◽  
Firing Properties

Vestibular compensation after a unilateral labyrinthectomy leads to nearly complete disappearance of the static symptoms triggered by the lesion. However, the dynamic vestibular reflexes associated with head movements remain impaired. Because the contralesional labyrinth plays a prominent role in the generation of these dynamic responses, intracellular recordings of contralesional medial vestibular nucleus neurons (MVNn) were done after 1 mo of compensation. Their firing properties and cell type were characterized at rest, and their response dynamics investigated using step, ramp, and sinusoidal current stimulations. The sensitivity of the contralesional MVNn firing rates to applied current was increased, which, along with increased phase leads, suggests that significant changes in active conductances occurred. We found an increased proportion of the phasic type B neurons relative to the tonic type A neurons in the contralesional MVN. In addition, the remaining contralesional type A MVNn response dynamics tended to approach those of type B MVNn. Thus the contralesional MVNn in general showed more phasic response dynamics than those of control MVNn. Altogether, the firing properties of MVNn are differentially modified on the ipsilesional and contralesional sides of the brain stem 1 mo after unilateral labyrinthectomy. Ipsilesional MVNn acquire more “type A–like” tonic membrane properties, which would contribute to the stabilization of the spontaneous activity that recovers in the deafferented neurons during vestibular compensation. The bilateral increase in the sensitivity of MVNn and the acquisition of more “B-like” phasic membrane properties by contralesional MVNn should promote the restoration of the vestibular reflexes generated by the remaining, contralesional labyrinth.

Static and Dynamic Membrane Properties of Lateral Vestibular Nucleus Neurons in Guinea Pig Brain Stem Slices

2003 ◽  
Vol 90 (3) ◽  
pp. 1689-1703 ◽  
Author(s):  
Atsuhiko Uno ◽  
Erwin Idoux ◽  
Mathieu Beraneck ◽  
Pierre-Paul Vidal ◽  
Lee E. Moore ◽  
...  
Keyword(s):  
Vestibular Nucleus ◽  
Type A ◽  
Membrane Properties ◽  
In Vivo Studies ◽  
Medial Vestibular Nucleus ◽  
Intracellular Recordings ◽  
Lateral Vestibular Nucleus ◽  
Type B ◽  
Dynamic Membrane ◽  
Homogeneous Population

In vitro intracellular recordings of central vestibular neurons have been restricted so far to the medial vestibular nucleus (MVN). We performed intracellular recordings of large Deiters' neurons in the lateral vestibular nucleus (LVN) to determine their static and dynamic membrane properties, and compare them with those of type A and type B neurons identified in the MVN. Unlike MVN neurons (MVNn), the giant-size LVN neurons (LVNn) form a homogeneous population of cells characterized by sharp spikes, a low-amplitude, biphasic after-hyperpolarization like type B MVNn, but also an A-like rectification like type A MVNn. In accordance with their lower membrane resistance, the sensitivity of LVNn to current injection was lower than that of MVNn over a large range of frequencies. The main difference between LVNn and MVNn was that the Bode plots showing the sensitivity of LVNn as a function of stimulation frequency were flatter than those of MVNn, and displayed a weaker resonance. Furthermore, most LVNn did not show a gradual decrease of their firing rate modulation in the frequency range where it was observed in MVNn. LVNn synchronized their firing with the depolarizing phase of high-frequency sinusoidal current injections. In vivo studies have shown that the MVN would be mainly involved in gaze control, whereas the giant LVNn that project to the spinal cord are involved in the control of posture. We suggest that the difference in the membrane properties of LVNn and MVNn may reflect their specific physiological roles.

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

2003 ◽  
Vol 90 (1) ◽  
pp. 184-203 ◽  
Author(s):  
Mathieu Beraneck ◽  
Mohammed Hachemaoui ◽  
Erwin Idoux ◽  
Laurence Ris ◽  
Atsuhiko Uno ◽  
...  
Keyword(s):  
Vestibular Nucleus ◽  
Type A ◽  
Vestibular Compensation ◽  
Membrane Properties ◽  
Medial Vestibular Nucleus ◽  
Type B ◽  
Dynamic Membrane ◽  
Vestibular Neurons ◽  
Unilateral Labyrinthectomy

Unilateral labyrinthectomy results in oculomotor and postural disturbances that regress in a few days during vestibular compensation. The long-term (after 1 mo) consequences of unilateral labyrinthectomy were investigated by characterizing the static and dynamic membrane properties of the ipsilesional vestibular neurons recorded intracellularly in guinea pig brain stem slices. We compared the responses of type A and type B medial vestibular nucleus neurons identified in vitro to current steps and ramps and to sinusoidal currents of various frequencies. All ipsilesional vestibular neurons were depolarized by 6–10 mV at rest compared with the cells recorded from control slices. Both their average membrane potential and firing threshold were more depolarized, which suggests that changes in active conductances compensated for the loss of excitatory afferents. The afterhyperpolarization and discharge regularity of type B but not type A neurons were increased. All ipsilesional vestibular cells became more sensitive to current injections over a large range of frequencies (0.2–30 Hz), but this increase in sensitivity was greater for type B than for type A neurons. This was associated with an increase of the peak frequency of linear response restricted to type B neurons, from 4–6 to 12–14 Hz. Altogether, we show that long-term vestibular compensation involves major changes in the membrane properties of vestibular neurons on the deafferented side. Many of the static and dynamic membrane properties of type B neurons became more similar to those of type A neurons than in control slices, leading to an increase in the overall homogeneity of medial vestibular nucleus neurons.

scholarly journals Postnatal Development of Spike Generation in Rat Medial Vestibular Nucleus Neurons

2001 ◽  
Vol 85 (5) ◽  
pp. 1899-1906 ◽  
Author(s):  
Gabe J. Murphy ◽  
Sascha Du Lac
Keyword(s):  
Firing Rate ◽  
Postnatal Development ◽  
Visual Function ◽  
Vestibular Nucleus ◽  
Image Motion ◽  
Membrane Properties ◽  
Medial Vestibular Nucleus ◽  
Spike Generation ◽  
Firing Rates ◽  
The Third

Image stability during self motion depends on the combined actions of the vestibuloocular and optokinetic reflexes (VOR and OKR, respectively). Neurons in the medial vestibular nucleus (MVN) participate in the VOR and OKR by firing in response to both head and image motion. Their intrinsic spike-generating properties enable MVN neurons to modulate firing rates linearly over a broad range of input amplitudes and frequencies such as those that occur during natural head and image motion. This study examines the postnatal development of the intrinsic spike-generating properties of rat MVN neurons with respect to maturation of peripheral vestibular and visual function. Spike generation was studied in a brain stem slice preparation by recording firing responses to current injected intracellularly through whole cell patch electrodes. MVN neurons fired spontaneously and modulated their firing rate in response to injected current at all postnatal ages. However, the input-output properties of the spike generator changed dramatically during the first two postnatal weeks. Neurons younger than postnatal day 10 could not fire faster than 80 spikes/s, modulated their firing rates over a limited range of input amplitudes, and tended to exhibit a nonlinear relationship between input current and mean evoked firing rate. In response to sustained depolarization, firing rates declined significantly in young neurons. Response gains tended to be highest in the first few postnatal days but varied widely across neurons and were not correlated with age. By about the beginning of the third postnatal week, MVN neurons could fire faster than 100 spikes/s in response to a broad range of input amplitudes, exhibited predominantly linear current-firing rate relationships, and adapted little in response to sustained depolarization. Concomitant decreases in action potential width and the time course of the afterhyperpolarization suggest that changes in potassium currents contribute to the maturation of the MVN neuronal spike generator. The results demonstrate that developmental changes in intrinsic membrane properties enable MVN neurons to fire linearly in response to a broad range of stimuli in time for the onset of visual function at the beginning of the third postnatal week.

Effects of toluene on tonic firing and membrane properties of rat medial vestibular nucleus neurones in vitro

1998 ◽  
Vol 779 (1-2) ◽  
pp. 334-337 ◽  
Author(s):  
Anna K Magnusson ◽  
M.Roslan Sulaiman ◽  
Mayank B Dutia ◽  
Richard Tham
Keyword(s):  
Vestibular Nucleus ◽  
Membrane Properties ◽  
Medial Vestibular Nucleus ◽  
Tonic Firing

Membrane and Firing Properties of Glutamatergic and GABAergic Neurons in the Rat Medial Vestibular Nucleus

2004 ◽  
Vol 92 (5) ◽  
pp. 3106-3120 ◽  
Author(s):  
Tomonori Takazawa ◽  
Yasuhiko Saito ◽  
Keisuke Tsuzuki ◽  
Seiji Ozawa
Keyword(s):  
Single Cell ◽  
Firing Pattern ◽  
Vestibular Nucleus ◽  
Cholinergic Neurons ◽  
Gabaergic Neurons ◽  
Membrane Properties ◽  
Medial Vestibular Nucleus ◽  
Pcr Analysis ◽  
Rt Pcr ◽  
Electrophysiological Properties

In previous studies, neurons in the medial vestibular nucleus (MVN) were classified mainly into 2 types according to their intrinsic membrane properties in in vitro slice preparations. However, it has not been determined whether the classified neurons are excitatory or inhibitory ones. In the present study, to clarify the relationship between the chemical and electrophysiological properties of MVN neurons, we explored mRNAs of cellular markers for GABAergic (glutamic acid decarboxylase 65, 67, and neuronal GABA transporter), glutamatergic (vesicular glutamate transporter 1 and 2), glycinergic (glycine transporter 2), and cholinergic neurons (choline acetyltransferase and vesicular acetylcholine transporter) expressed in electrophysiologically characterized MVN neurons in rat brain stem slice preparations. For this purpose, we combined whole cell patch-clamp recording analysis with single-cell reverse transcription–polymerase chain reaction (RT-PCR) analysis. We examined the membrane properties such as afterhyperpolarization (AHP), firing pattern, and response to hyperpolarizing current pulse to classify MVN neurons. From the single-cell RT-PCR analysis, we found that GABAergic neurons consisted of heterogeneous populations with different membrane properties. Comparison of the membrane properties of GABAergic neurons with those of other neurons revealed that AHPs without slow components and a firing pattern with delayed spike generation (late spiking) were preferential properties of GABAergic neurons. On the other hand, most glutamatergic neurons formed a homogeneous subclass of neurons exhibiting AHPs with slow components, repetitive firings with constant interspike intervals (continuous spiking), and time-dependent inward rectification in response to hyperpolarizing current pulses. We also found a small number of cholinergic neurons with various membrane properties. These findings clarify the electrophysiological properties of excitatory and inhibitory neurons in the MVN, and the information about the preferential membrane properties may be useful for identifying GABAergic and glutamatergic MVN neurons electrophysiologically.

scholarly journals Oscillatory and Intrinsic Membrane Properties of Guinea Pig Nucleus Prepositus Hypoglossi Neurons In Vitro

2006 ◽  
Vol 96 (1) ◽  
pp. 175-196 ◽  
Author(s):  
Erwin Idoux ◽  
Mauro Serafin ◽  
Patrice Fort ◽  
Pierre-Paul Vidal ◽  
Mathieu Beraneck ◽  
...  
Keyword(s):  
Vestibular Nucleus ◽  
Discharge Rate ◽  
Oscillatory Behavior ◽  
Membrane Properties ◽  
Medial Vestibular Nucleus ◽  
Relative Role ◽  
Type D ◽  
Highly Nonlinear ◽  
Prepositus Hypoglossi

Numerous models of the oculomotor neuronal integrator located in the prepositus hypoglossi nucleus (PHN) involve both highly tuned recurrent networks and intrinsic neuronal properties; however, there is little experimental evidence for the relative role of these two mechanisms. The experiments reported here show that all PHN neurons (PHNn) show marked phasic behavior, which is highly oscillatory in ∼25% of the population. The behavior of this subset of PHNn, referred to as type D PHNn, is clearly different from that of the medial vestibular nucleus neurons, which transmit the bulk of head velocity-related sensory vestibular inputs without integrating them. We have investigated the firing and biophysical properties of PHNn and developed data-based realistic neuronal models to quantitatively illustrate that their active conductances can produce the oscillatory behavior. Although some individual type D PHNn are able to show some features of mathematical integration, the lack of robustness of this behavior strongly suggests that additional network interactions, likely involving all types of PHNn, are essential for the neuronal integrator. Furthermore, the relationship between the impulse activity and membrane potential of type D PHNn is highly nonlinear and frequency-dependent, even for relatively small-amplitude responses. These results suggest that some of the synaptic input to type D PHNn is likely to evoke oscillatory responses that will be nonlinearly amplified as the spike discharge rate increases. It would appear that the PHNn have specific intrinsic properties that, in conjunction with network interconnections, enhance the persistent neural activity needed for their function.

Anticipation in the Rodent Head Direction System Can Be Explained by an Interaction of Head Movements and Vestibular Firing Properties

2007 ◽  
Vol 98 (4) ◽  
pp. 1883-1897 ◽  
Author(s):  
Matthijs A. A. van der Meer ◽  
James J. Knierim ◽  
D. Yoganarasimha ◽  
Emma R. Wood ◽  
Mark C. W. van Rossum
Keyword(s):  
Vestibular Nucleus ◽  
Passive Movement ◽  
Head Movements ◽  
Medial Vestibular Nucleus ◽  
Electrophysiological Recording ◽  
Head Direction ◽  
Movement Data ◽  
Behavioral Variables ◽  
Firing Properties ◽  
Functional Circuitry

The rodent head-direction (HD) system, which codes for the animal's head direction in the horizontal plane, is thought to be critically involved in spatial navigation. Electrophysiological recording studies have shown that HD cells can anticipate the animal's HD by up to 75–80 ms. The origin of this anticipation is poorly understood. In this modeling study, we provide a novel explanation for HD anticipation that relies on the firing properties of neurons afferent to the HD system. By incorporating spike rate adaptation and postinhibitory rebound as observed in medial vestibular nucleus neurons, our model produces realistic anticipation on a large corpus of rat movement data. In addition, HD anticipation varies between recording sessions of the same cell, between active and passive movement, and between different studies. Such differences do not appear to be correlated with behavioral variables and cannot be accounted for using earlier models. In the present model, anticipation depends on the power spectrum of the head movements. By direct comparison with recording data, we show that the model explains 60–80% of the observed anticipation variability. We conclude that HD afferent dynamics and the statistics of rat head movements are important in generating HD anticipation. This result contributes to understanding the functional circuitry of the HD system and has methodological implications for studies of HD anticipation.

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