Intrinsic membrane properties of central vestibular neurons in rodents (original) (raw)
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Intrinsic membrane properties of vertebrate vestibular neurons: Function, development and plasticity
Progress in Neurobiology, 2005
Central vestibular neurons play an important role in the processing of body motion-related multisensory signals and their transformation into motor commands for gaze and posture control. Over recent years, medial vestibular nucleus (MVN) neurons and to a lesser extent other vestibular neurons have been extensively studied in vivo and in vitro, in a range of species. These studies have begun to reveal how their intrinsic electrophysiological properties may relate to their response patterns, discharge dynamics and computational capabilities. In vitro studies indicate that MVN neurons are of two major subtypes (A and B), which differ in their spike shape and after-hyperpolarizations. This reflects differences in particular K + conductances present in the two subtypes, which also affect their response dynamics with type A cells having relatively lowfrequency dynamics (resembling ''tonic'' MVN cells in vivo) and type B cells having relatively high-frequency dynamics (resembling ''kinetic'' cells in vivo). The presence of more than one functional subtype of vestibular neuron seems to be a ubiquitous feature since vestibular neurons in the chick and frog also subdivide into populations with different, analogous electrophysiological properties. The ratio of type A to type B neurons appears to be plastic, and may be determined by the signal processing requirements of the vestibular system, which are species-variant. The membrane properties and discharge pattern of type A and type B MVN neurons develop largely post-natally, through the expression of the underlying ion channel conductances. The membrane properties of MVN neurons show rapid and long-lasting plastic changes after deafferentation (unilateral labyrinthectomy), which may serve to maintain their level of activity and excitability after the loss of afferent inputs.
The Journal of Physiology, 2007
The effect of the lack of vestibular input on the membrane properties of central vestibular neurons was studied by using a strain of transgenic, vestibular-deficient mutant KCNE1 −/− mice where the hair cells of the inner ear degenerate just after birth. Despite the absence of sensory vestibular input, their central vestibular pathways are intact. Juvenile and adult homozygous mutant have a normal resting posture, but show a constant head bobbing behaviour and display the shaker/waltzer phenotype characterized by rapid bilateral circling during locomotion. In juvenile mice, the KCNE1 mutation was associated with a strong decrease in the expression of the calcium-binding proteins calbindin, calretinin and parvalbumin within the medial vestibular nucleus (MVN) and important modifications of the membrane properties of MVN neurons. In adult mice, however, there was almost no difference between the membrane properties of MVN neurons of homozygous and control or heterozygous mutant mice, which have normal inner ear hair cells and show no behavioural symptoms. The expression levels of calbindin and calretinin were lower in adult homozygous mutant animals, but the amount of calcium-binding proteins expressed in the MVN was much greater than in juvenile mice. These data demonstrate that suppression of sensory vestibular inputs during a 'sensitive period' around birth can generate the circling/waltzing behaviour, but that this behaviour is not due to persistent abnormalities of the membrane properties of central vestibular neurons. Altogether, maturation of the membrane properties of central vestibular neurons is delayed, but not impaired by the absence of sensory vestibular information.
Intrinsic membrane properties and plasticity in medial vestibular nucleus neurones
2002
In vivo electrophysiological properties of MVN neurones 13 1.1.4 In vitro electrophysiological properties of MVN neurones 16 1.2 Pharmacology of the MVN 17 1.3 Vestibular Compensation 1.3.1 Behavioural component of vestibular compensation 1.3.2 Neuronal component of vestibular compensation 1.3.3 Mechanisms of vestibular compensation 1.4 Aims of the Thesis Chapter 2. Intrinsic membrane properties of rat MVN neurones and their role in vestibular compensation 2.1 Introduction 2.2 Materials and Methods 2.3 Results 2.3.1 Intrinsic membrane properties and spike firing characteristics of MVN neurones in normal rats 2.3.2 Intrinsic membrane properties and spike firing characteristics of MVN neurones after the UL 2.4 Discussion Chapter 3. Tonic activity and GABAergic inhibition in aged rat MVN neurones 3.1 Introduction 3.2 Materials and Methods 3.3 Results 3.4 Discussion Conclusions and future work References
Perinatal development of central vestibular neurons in mice
Frontiers in Neuroscience, 2022
Central circuitry of the vestibular nuclei integrates sensory inputs in the adaptive control of motor behaviors such as posture, locomotion, and gaze stabilization. Thus far, such circuits have been mostly examined at mature stages, whereas their emergence and early development have remained poorly described. Here, we focused on the perinatal period of murine development, from embryonic day E14.5 to post-natal day P5, to investigate the ontogeny of two functionally distinct vestibular neuronal groups, neurons projecting to the spinal cord via the lateral vestibulospinal tract (LVST) and commissural neurons of the medial vestibular nucleus that cross the midline to the contralateral nucleus. Using transgenic mice and retrograde labeling, we found that network-constitutive GABAergic and glycinergic neurons are already established in the two vestibular groups at embryonic stages. Although incapable of repetitive firing at E14.5, neurons of both groups can generate spike trains from E15.5 onward and diverge into previously established A or B subtypes according to the absence (A) or presence (B) of a two-stage spike after hyperpolarization. Investigation of several voltagedependent membrane properties indicated that solely LVST neurons undergo significant maturational changes in their electrophysiological characteristics during perinatal development. The proportions of A vs B subtypes also evolve in both groups, with type A neurons remaining predominant at all stages, and type B commissural neurons appearing only post-natally. Together, our results indicate that vestibular neurons acquire their distinct morpho-functional identities after E14.5 and that the early maturation of membrane properties does not emerge uniformly in the different functional subpopulations of vestibulo-motor pathways.
Vestibular Critical Period, Maturation of Central Vestibular Neurons, and Locomotor Control
Annals of the New York Academy of Sciences, 2009
Mutant mice are a good model to study to what extent the postnatal activity of sensory afferents is necessary for the maturation of central neurons. In particular, the question arises whether the signals carried by the first-order vestibular neurons, which encode information on the head movement of pups, are necessary for the maturation of second-order vestibular neurons. To address that question, juvenile and adult transgenic, vestibular-deficient mutants where a null mutation of the KCNE1 potassiumchannel gene leads to degeneration of all hair cells of the inner ear just after birth were studied. These KCNE1 −/− mutants are deaf and show quasi-constant head bobbing and a permanent shaker/waltzer phenotype. This behavior is not due to persistent abnormalities of the membrane properties of central vestibular neurons, because their maturation is delayed but not impaired by the absence of sensory vestibular information. On the other hand, the data shed light on how the membrane properties of vestibular neurons might be modified according to functional requirements or following lesions. The expression levels of the protein calretinin that regulates the intracellular free-calcium concentration in central vestibular neurons could play a major role both in intact animals and following labyrinthectomy. By comparing the KCNE1 −/− mutant mice to other vestibular-deficient animals, it was concluded that the suppression of vestibular inputs during a "critical period" of postnatal development can induce a permanent circling behavior, but that this phenotype is not always due to congenital vestibular deficiency.
Properties of neurons from the rat medial vestibular nucleus in microexplant culture
Neuroscience Letters, 2003
This study is a first step in an attempt to identify the factors which determine and maintain the electrophysiological phenotype(s) of mature neurons of the medial vestibular nucleus (MVN). We cultured MVN microexplants obtained from slices of the brainstem of newborn rats, using a hollow punching needle. The electrophysiological maturation of the neurons was followed by analyzing their responses to 1 s steps of current of increasing amplitude. The maximal number of spikes that was generated in response to such stimuli increased dramatically over time in vitro. However, even after 28 days in vitro, it did not exceed about 60 spikes/s. At this stage of culture, the input -output properties of the spike generator of the MVN neurons were similar to those observed in brainstem slices of newborn rats, but clearly inferior to those of adult neurons which can generate sustained firing up to 150-200 spikes/s. q
PLoS ONE, 2014
The functional role of efferent innervation of the vestibular end-organs in the inner ear remains elusive. This study provides the first physiological characterization of the cholinergic vestibular efferent (VE) neurons in the brainstem by utilizing a transgenic mouse model, expressing eGFP under a choline-acetyltransferase (ChAT)-locus spanning promoter in combination with targeted patch clamp recordings. The intrinsic electrical properties of the eGFP-positive VE neurons were compared to the properties of the lateral olivocochlear (LOC) brainstem neurons, which gives rise to efferent innervation of the cochlea. Both VE and the LOC neurons were marked by their negative resting membrane potential ,2 75 mV and their passive responses in the hyperpolarizing range. In contrast, the response properties of VE and LOC neurons differed significantly in the depolarizing range. When injected with positive currents, VE neurons fired action potentials faithfully to the onset of depolarization followed by sparse firing with long inter-spike intervals. This response gave rise to a low response gain. The LOC neurons, conversely, responded with a characteristic delayed tonic firing upon depolarizing stimuli, giving rise to higher response gain than the VE neurons. Depolarization triggered large TEA insensitive outward currents with fast inactivation kinetics, indicating A-type potassium currents, in both the inner ear-projecting neuronal types. Immunohistochemistry confirmed expression of Kv4.3 and 4.2 ion channel subunits in both the VE and LOC neurons. The difference in spiking responses to depolarization is related to a two-fold impact of these transient outward currents on somatic integration in the LOC neurons compared to in VE neurons. It is speculated that the physiological properties of the VE neurons might be compatible with a wide-spread control over motion and gravity sensation in the inner ear, providing likewise feed-back amplification of abrupt and strong phasic signals from the semi-circular canals and of tonic signals from the gravito-sensitive macular organs.
Journal of Neurophysiology, 2003
Static and dynamic membrane properties of lateral vestibular nucleus neurons in guinea pig brain stem slices. . 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.
Medial vestibular nucleus in the guinea-pig
Experimental Brain Research, 1991
Intracellular recordings were obtained from medial vestibular nuclei neurones (MVNn) in guinea-pig brainstem slices. Two main distinct neuronal classes were encountered. Type A MVNn (32.3 %) were characterized by a broad action potential followed by a deep single afterhyperpolarization, a transient A-like rectification, and a single range of firing in response to current injection. Type B MVNn (47.1%), in contrast, were distinguished by the presence of a thin action potential followed first by a fast and then by a delayed and slower afterhyperpolarization. In addition, they displayed a secondary range of firing in their response to current injection. A majority of B MVNn also had either subthreshold plateau potentials or low threshold spike bursts or a combination thereof. A third, non-homogeneous class of cells, could not be fitted into either one of the two main classes (20.6%, type C MVNn).
European Journal of Neuroscience, 1994
Vestibular compensation is an attractive model for investigations of cellular mechanisms underlying post-lesional plasticity in the adult central nervous system. Immediately after hemilabyrinthectomy, the spontaneous activity in the deafferented second-order vestibular neurons falls to zero, resulting in a strong asymmetry between the resting discharge of the vestibular complexes on the lesioned and intact sides. This asymmetry most probably causes the static and dynamic vestibular deficits observed in the acute stage. After ∼50 h, the deafferented vestibular neurons recover a quasi-normal resting activity which is thought to be the key of the compensation of the static vestibular syndromes. However, the molecular mechanisms underlying this recovery are unknown. In this study, we investigate possible changes in the distribution of glutamatergic N-methyl-d-aspartate (NMDA) and glutamate metabotropic receptors and of glutamate decarboxylase 67k (GAD 67k) mRNAs in the deafferented vestibular neurons induced by the labyrinthine lesion. Specific radioactive oligonucleotides were used to probe sections of rat vestibular nuclei according to in situ hybridization methods. Animals were killed at different times (5 h, 3 days and 3 weeks) following the lesion. Signal was detected by means of film or emulsion autoradiography. In the normal animals, several brainstem regions including the medial, lateral, inferior and superior vestibular nuclei were densely labelled by the antisense oligonucleotide NMDAR1 probe. However, the vestibular nuclei were not labelled by the glutamate metabotropic oligonucleotide antisense probe (mGluR 1). The GAD 67k antisense oligonucleotide probe labelled numerous small- to medium-sized central vestibular neurons but not the larger cell bodies in the lateral vestibular nucleus. This agrees with previous studies. In the hemilabyrinthectomized rats, no asymmetry could be detected, at either the autoradiographic or cellular levels, between the two medial vestibular nuclei whatever the probe used and whatever the delay following the lesion. However, for the NMDAR1 probe, the mean density of silver grains in both the deafferented and intact medial vestibular neurons was 20% lower 5 h after the lesion. Three days and 3 weeks later, the intensity of labelling over all cells was the same as in the control group. Further studies are necessary to confirm the relatively weak modification of the NMDAR1 mRNAs expression and to exclude a change of GAD 65 and of other NMDA subunit mRNAs during the vestibular compensation process.