Potassium currents and excitability in second‐order auditory and vestibular neurons

Peusner, Kenna D.; Gamkrelidze, Georgi; Giaume, Christian

doi:10.1002/(sici)1097-4547(19980901)53:5<511::aid-jnr1>3.3.co;2-8

Cited by 7 publications

(8 citation statements)

References 55 publications

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“…Generally, calcium-dependent potassium currents contribute to the repolarizing phase of the action potential and to control the repetitive discharge of spikes. The calcium-dependent potassium currents of the vestibular nuclear neurons are known to underlie the afterhyperpolarization of action potential (12,13). In the present study, the depth of afterhyperpolarization was decreased by nitric oxide liberating agents and L-arginine, which coincides with the results of Park and Jeong (5).…”

supporting

confidence: 91%

Nitric Oxide Modulation of the Spontaneous Firing of Rat Medial Vestibular Nuclear Neurons

et al. 2004

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Abstract. Modulation of the spontaneous activity of rat medial vestibular nuclear neurons by nitric oxide was investigated using the whole-cell patch-clamp technique. The spike frequency was increased by sodium nitroprusside (SNP), a nitric oxide liberating agent, and it was also increased by another nitric oxide liberating agent, sodium-nitroso-N-acetylpenicillamine. LArginine, the substrate of nitric oxide synthase, increased the firing of the neurons. The increased SNP-induced firing was inhibited by 1H-[1,2,4]oxadiazolo[4,3-a]quinozalin-1-one (ODQ), a specific inhibitor of guanylate cyclase. These results suggest that nitric oxide increases the neuronal excitability of the neurons by a cGMP-dependent mechanism.Keywords: nitric oxide, medial vestibular nucleus, action potential Nitric oxide synthesized from L-arginine by nitric oxide synthase functions as a neurotransmitter in the central nervous system through the activation of guanylate cyclase, cycloxygenase, and protein kinase C (1). It mediates actions of glutamate and is involved in lasting changes of neuronal activity such as long-term suppression and long-term potentiation (2). Evidences suggest that nitric oxide is also involved in neuronal development, apoptosis, memory, control of cerebral blood flow, and hyperalgesia (3).The medial vestibular nucleus (MVN) is the largest one among the vestibular nuclei and known to play important roles not only in normal vestibular information processing but also in vestibular compensation (4). Previous studies have shown that nitric oxide has effects on potassium currents that regulate cellular excitability, especially in neuronal cells. Park and Jeong reported that nitric oxide inhibits potassium currents of the rat MVN neuron by increasing intracellular cGMP (5). However, little is known about direct effects of nitric oxide on the neuronal excitability of the vestibular nuclear neurons. In the present study, we performed a whole-cell patch-clamp under the current clamp mode to investigate the direct action of nitric oxide on the spontaneous activity of acutely isolated rat MVN neurons.Institutional Committee of Laboratory Animal Care and Use approved the experimental protocol. Coronal slices of the brain stem of Sprague-Dawley rats aged 14 to 17 days were prepared as described previously for rats (6). Briefly, the animals were anesthetized with ether and decapitated. The brain stem was rapidly removed into ice-cold artificial cerebrospinal fluid. The coronal slices (400-m m-thick) of the brain stem were made with a sliding microtome (Vibroslice; WPI, Sarasota FL, USA). These slices were incubated in artificial cerebrospinal fluid well saturated with 95% O 2 / 5% CO 2 at room temperature for 1 h. The slices were treated with pronase (0.2 mg/ ml) for 40 -60 min and subsequently exposed to thermolysin (0.2 mg / ml) for 10 min at 32°C. After this enzyme digestion, the portion of MVN neuron was removed by micropunching and gently agitated. The dissociated neurons were transferred into a recording chamber mounted on ...

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confidence: 91%

Nitric Oxide Modulation of the Spontaneous Firing of Rat Medial Vestibular Nuclear Neurons

et al. 2004

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“…Increasing numbers of K channels in rat MVN neurons, unlike the ganglion neurons, can lead to more sustained spiking. In maturing chick tangential neurons, in contrast, Peusner et al (1998) observed downregulation of LV K ϩ currents and more sustained spike patterns, observations that are consistent with the role of LV channels in rat primary afferent neurons, but following the opposite developmental trend.…”

Section: Development Of Firing Patternssupporting

confidence: 76%

Ion Channels Set Spike Timing Regularity of Mammalian Vestibular Afferent Neurons

Kalluri

Xue

Eatock

2010

Journal of Neurophysiology

166

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Kalluri R, Xue J, Eatock RA. Ion channels set spike timing regularity of mammalian vestibular afferent neurons. J Neurophysiol 104: 2034-2051, 2010. First published July 21, 2010 doi:10.1152/jn.00396.2010. In the mammalian vestibular nerve, some afferents have highly irregular interspike intervals and others have highly regular intervals. To investigate whether spike timing is determined by the afferents' ion channels, we studied spiking activity in their cell bodies, isolated from the vestibular ganglia of young rats. Whole cell recordings were made with the perforated-patch method. As previously reported, depolarizing current steps revealed distinct firing patterns. Transient neurons fired one or two onset spikes, independent of current level. Sustained neurons were more heterogeneous, firing either trains of spikes or a spike followed by large voltage oscillations. We show that the firing pattern categories are robust, occurring at different temperatures and ages, both in mice and in rats. A difference in average resting potential did not cause the difference in firing patterns, but contributed to differences in afterhyperpolarizations. A low-voltage-activated potassium current (I LV ) was previously implicated in the transient firing pattern. We show that I LV grew from the first to second postnatal week and by the second week comprised Kv1 and Kv7 (KCNQ) components. Blocking I LV converted step-evoked firing patterns from transient to sustained. Separated from their normal synaptic inputs, the neurons did not spike spontaneously. To test whether the firing-pattern categories might correspond to afferent populations of different regularity, we injected simulated excitatory postsynaptic currents at pseudorandom intervals. Sustained neurons responded to a given pattern of input with more regular firing than did transient neurons. Pharmacological block of I LV made firing more regular. Thus ion channel differences that produce transient and sustained firing patterns in response to depolarizing current steps can also produce irregular and regular spike timing.

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“…With similar findings, earlier works also divided vestibular neurons into these two categories (Serafin et al, 1991;Johnston et al, 1994;Him & Dutia, 2001;Beraneck et al, 2003). In vestibular neurons, the combination of electrophysiological and pharmacological studies has distinguished different potassium and calcium conductances shaping the falling and AHP phases of the action potential (reviewed in Darlington et al, 1995;Peusner et al, 1998;Straka et al, 2005). Whether such conductances are also underlying I A and I B Mns of the rat oculomotor nucleus is not known.…”

Section: Type I Mnsmentioning

confidence: 85%

Phasic and tonic firing properties in rat oculomotor nucleus motoneurons, studied in vitro

Nieto-González¹,

Carrascal²,

Nuñez-Abades³

et al. 2007

Eur J of Neuroscience

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Alert-chronic studies show that ocular motoneurons (Mns) exhibit a phasic and tonic firing correlated with eye saccade-velocity and position (fixation), respectively. Differences in the phasic and tonic firing among Mns depend on synaptic inputs and/or the intrinsic membrane properties. We have used in vitro slice preparation to investigate the contribution of membrane properties to firing properties of Wistar rat oculomotor nucleus Mns. We recorded different discharge patterns and focused on Mns with sustained discharge (type I) because they were the most abundant, and their firing pattern resembles that reported in alert preparations. Various differences divided these Mns into types I(A) and I(B); the afterhyperpolarization (AHP) phase of the spike was monophasic in I(A) and biphasic in I(B); I(A) Mns showed tonic or phasic-tonic firing depending on the current intensity, while I(B) Mns showed phasic-tonic discharge; the phasic firing was higher in I(B) than in I(A) Mns; I(A) Mns fired in a narrower range than did I(B) Mns; and I(A) Mns showed lower maximum frequency than did I(B) Mns. In conclusion, I(A) and I(B) Mns show different phasic firing properties and dynamic range, supported by intrinsic membrane properties. We suggest that I(A) and I(B) Mns innervate fast-twitch muscle fibres with different contraction speeds, and could contribute to generating a fine phasic signal for a graded muscle contraction. Finally, we have demonstrated an inverse relationship between Mn thresholds and tonic firing gain, concluding that intrinsic membrane properties could not support the covariation between tonic firing gain and recruitment thresholds reported in alert studies.

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Potassium currents and excitability in second‐order auditory and vestibular neurons

Cited by 7 publications

References 55 publications

Nitric Oxide Modulation of the Spontaneous Firing of Rat Medial Vestibular Nuclear Neurons

Nitric Oxide Modulation of the Spontaneous Firing of Rat Medial Vestibular Nuclear Neurons

Ion Channels Set Spike Timing Regularity of Mammalian Vestibular Afferent Neurons

Phasic and tonic firing properties in rat oculomotor nucleus motoneurons, studied in vitro

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