Maturation of firing pattern in chick vestibular nucleus neurons

Abstract

The principal cells of the chick tangential nucleus are vestibular nucleus neurons participating in the vestibuloocular and vestibulocollic reflexes. In birds and mammals, spontaneous and stimulusevoked firing of action potentials is essential for vestibular nucleus neurons to generate mature vestibular reflex activity. The emergence of spike-firing pattern and the underlying ion channels were studied in morphologically-identified principal cells using whole-cell patch-clamp recordings from brain slices of late-term embryos (embryonic day 16) and hatchling chickens (hatching day 1 and hatching day 5). Spontaneous spike activity emerged around the perinatal period, since at embryonic day 16 none of the principal cells generated spontaneous action potentials. However, at hatching day 1, 50% of the cells fired spontaneously (range, 3 to 32 spikes/s), which depended on synaptic transmission in most cells. By hatching day 5, 80% of the principal cells could fire action potentials spontaneously (range, 5 to 80 spikes/s), and this activity was independent of synaptic transmission and showed faster kinetics than at hatching day 1. Repetitive firing in response to depolarizing pulses appeared in the principal cells starting around embryonic day 16, when < 20% of the neurons fired repetitively. However, almost 90% of the principal cells exhibited repetitive firing on depolarization at hatching day 1, and 100% by hatching day 5. From embryonic day 16 to hatching day 5, the gain for evoked spike firing increased almost 10-fold. At hatching day 5, a persistent sodium channel was essential for the generation of spontaneous spike activity, while a small conductance, calciumdependent potassium current modulated both the spontaneous and evoked spike firing activity. Altogether, these in vitro studies showed that during the perinatal period, the principal cells switched from displaying no spontaneous spike activity at resting membrane potential and generating one spike on depolarization to the tonic firing of spontaneous and evoked action potentials. Keywordsintrinsic membrane properties; spike activity; brain sliceThe vestibuloocular (VOR) and optokinetic (OKR) reflexes are involved in stabilizing visual gaze during head movements, whereas the vestibulocollic (VCR) reflex stabilizes the head position in space. To perform these functions, the VOR generates compensatory eye movements in a direction opposite to the head movements, while the OKR produces eye movements in the same direction as the image motion, and the VCR stimulates the muscles of the neck to support the head during movements. Defined as the eye speed divided by head speed, the VOR gain is an important property, which is subject to change during different types of movements. For example, during natural head rotations, the gain of compensatory eye movements is larger than 1, but when there is image motion during head turning, the gain is smaller than 1. Thus, the VOR is an adaptive response, rather than an automatic reflex (for . E-mail address: anakdp@gwumc....

Developmental increase in hyperpolarization-activated current regulates intrinsic firing properties in rat vestibular ganglion cells

“…On the other hand, tonic type VGCs increased from 10% to 30% during the same period. These results are consistent with our previous study (Iwasaki et al, 2008), and similar developmental changes in the firing patterns have been reported in chick vestibular nucleus neurons (Shao et al, 2006). We previously examined developmental changes in the expression of Kv1 potassium channels in VGCs from developing rats by using immunohistochemistry, Western blotting and quantitative real-time RT-PCR, and showed that downregulation of the Kv1.6 protein and mRNA has an association with the maturation of excitable properties of primary vestibular neurons (Iwasaki et al, 2012).…”

Critical Roles of Voltage-Dependent Sodium Channels in the Process of Synaptogenesis During the Postnatal Cortical Development of Rats

“…Taken together, these aspects indicate that the alterations in the Na ? channel observed in our study may enhance the excitability of mature neurons during postnatal development, which would be in agreement with the observation that action potentials could be frequently elicited in more mature neurons, whereas abortive regenerative events or no action potentials were most frequently observed in immature ones (Holter et al 2007;Shao et al 2006).…”

Plasticity of spontaneous excitatory and inhibitory synaptic activity in morphologically defined vestibular nuclei neurons during early vestibular compensation

“…No significant difference was detected in either sEPSC or sIPSC frequency for spontaneous spike firing or silent principal cells from the same experimental group, suggesting that the ability of the principal cells to generate spontaneous spike activity was not related to the frequency of these spontaneous events. This conclusion is supported by finding that on exposure to a cocktail of excitatory and inhibitory neurotransmitter antagonists, principal cells in H5 controls do not change their spontaneous spike firing rates (Shao et al 2006).…”