scholarly journals Similarities in the Biophysical Properties of Spiral-Ganglion and Vestibular-Ganglion Neurons in Neonatal Rats

2021 ◽  
Vol 15 ◽  
Author(s):  
Radha Kalluri
Keyword(s):  
Sensory Modality ◽  
Spiral Ganglion ◽  
Input Resistance ◽  
Resting Potential ◽  
Biophysical Properties ◽  
Firing Patterns ◽  
Vestibular Ganglion ◽  
Large Current ◽  
Ganglion Neurons ◽  
Diverse Groups

The membranes of auditory and vestibular afferent neurons each contain diverse groups of ion channels that lead to heterogeneity in their intrinsic biophysical properties. Pioneering work in both auditory- and vestibular-ganglion physiology have individually examined this remarkable diversity, but there are few direct comparisons between the two ganglia. Here the firing patterns recorded by whole-cell patch-clamping in neonatal vestibular- and spiral ganglion neurons are compared. Indicative of an overall heterogeneity in ion channel composition, both ganglia exhibit qualitatively similar firing patterns ranging from sustained-spiking to transient-spiking in response to current injection. The range of resting potentials, voltage thresholds, current thresholds, input-resistances, and first-spike latencies are similarly broad in both ganglion groups. The covariance between several biophysical properties (e.g., resting potential to voltage threshold and their dependence on postnatal age) was similar between the two ganglia. Cell sizes were on average larger and more variable in VGN than in SGN. One sub-group of VGN stood out as having extra-large somata with transient-firing patterns, very low-input resistance, fast first-spike latencies, and required large current amplitudes to induce spiking. Despite these differences, the input resistance per unit area of the large-bodied transient neurons was like that of smaller-bodied transient-firing neurons in both VGN and SGN, thus appearing to be size-scaled versions of other transient-firing neurons. Our analysis reveals that although auditory and vestibular afferents serve very different functions in distinct sensory modalities, their biophysical properties are more closely related by firing pattern and cell size than by sensory modality.

scholarly journals A biophysical model examining the role of low-voltage-activated potassium currents in shaping the responses of vestibular ganglion neurons

2016 ◽  
Vol 116 (2) ◽  
pp. 503-521 ◽  
Author(s):  
Ariel E. Hight ◽  
Radha Kalluri
Keyword(s):  
Low Voltage ◽  
Potassium Currents ◽  
Synaptic Conductance ◽  
Biophysical Model ◽  
Resting Potential ◽  
Interspike Intervals ◽  
Firing Patterns ◽  
Vestibular Ganglion ◽  
Ganglion Neurons ◽  
The Impact

The vestibular nerve is characterized by two broad groups of neurons that differ in the timing of their interspike intervals; some fire at highly regular intervals, whereas others fire at highly irregular intervals. Heterogeneity in ion channel properties has been proposed as shaping these firing patterns (Highstein SM, Politoff AL. Brain Res 150: 182–187, 1978; Smith CE, Goldberg JM. Biol Cybern 54: 41–51, 1986). Kalluri et al. ( J Neurophysiol 104: 2034–2051, 2010) proposed that regularity is controlled by the density of low-voltage-activated potassium currents ( IKL). To examine the impact of IKL on spike timing regularity, we implemented a single-compartment model with three conductances known to be present in the vestibular ganglion: transient sodium ( gNa), low-voltage-activated potassium ( gKL), and high-voltage-activated potassium ( gKH). Consistent with in vitro observations, removing gKL depolarized resting potential, increased input resistance and membrane time constant, and converted current step-evoked firing patterns from transient (1 spike at current onset) to sustained (many spikes). Modeled neurons were driven with a time-varying synaptic conductance that captured the random arrival times and amplitudes of glutamate-driven synaptic events. In the presence of gKL, spiking occurred only in response to large events with fast onsets. Models without gKL exhibited greater integration by responding to the superposition of rapidly arriving events. Three synaptic conductance were modeled, each with different kinetics to represent a variety of different synaptic processes. In response to all three types of synaptic conductance, models containing gKL produced spike trains with irregular interspike intervals. Only models lacking gKL when driven by rapidly arriving small excitatory postsynaptic currents were capable of generating regular spiking.

scholarly journals Muscarinic acetylcholine receptors modulate HCN channel properties in vestibular ganglion neurons

2022 ◽  
Author(s):  
Daniel Bronson ◽  
Radha Kalluri
Keyword(s):  
Signaling Cascades ◽  
Hcn Channels ◽  
Type I ◽  
Hcn Channel ◽  
Firing Patterns ◽  
Vestibular Ganglion ◽  
Muscarinic Acetylcholine ◽  
Efferent Neurons ◽  
Ganglion Neurons ◽  
Channel Properties

Vestibular efferent neurons play an important role in shaping vestibular afferent excitability and accordingly, on the information encoded by their spike patterns. Efferent-modulation is linked to muscarinic signaling cascades that affect ion channel conductances, most notably low-voltage gated potassium channels such as KCNQ. Here we tested and found that muscarinic signaling cascades also modulate hyperpolarization-activated cyclic-nucleotide gated channels (HCN). HCN channels play a key role in controlling spike-timing regularity and a non-chemical form of transmission between type I hair cells and vestibular afferents. The impact of cholinergic efferent input on HCN channels was assessed using voltage-clamp methods, which measure currents in the disassociated cell bodies of vestibular ganglion neurons (VGN). Membrane properties in VGN were characterized before and after administration of the muscarinic acetylcholine receptor (mAChR) agonist Oxotremorine-M (Oxo-M). We found that Oxo-M shifted the voltage-activation range of HCN channels in the positive direction by 4.1 +/- 1.1 mV, which more than doubled the available current when held near rest at -60 mV (a 184 +/- 90.1% increase, n=19). This effect was not blocked by pre-treating the cells with a KCNQ channel blocker, linopirdine, which suggests that this effect is not dependent on KCNQ currents. We also found that HCN channel properties in the baseline condition and sensitivity to mAChR activation depended on cell size and firing patterns. Large-bodied neurons with onset firing patterns had the most depolarized activation range and least sensitivity to mAChR activation. Together, our results highlight the complex and dynamic regulation of HCN channels in VGN.

scholarly journals Endogenous Firing Patterns of Murine Spiral Ganglion Neurons

1997 ◽  
Vol 77 (3) ◽  
pp. 1294-1305 ◽  
Author(s):  
Zun-Li Mo ◽  
Robin L. Davis
Keyword(s):  
Action Potential ◽  
Spiral Ganglion ◽  
Constant Current ◽  
Inward Rectification ◽  
Spiral Ganglion Neurons ◽  
Patch Clamp Technique ◽  
Firing Patterns ◽  
Spike Amplitude ◽  
Ganglion Neurons

Mo, Zun-Li and Robin L. Davis. Endogenous firing patterns of murine spiral ganglion neurons. J. Neurophysiol. 77: 1294–1305, 1997. Current-clamp recordings with the use of the whole cell configuration of the patch-clamp technique were made from postnatal mouse spiral ganglion neurons in vitro. Cultures contained neurons that displayed monopolar, bipolar, and pseudomonopolar morphologies. Additionally, a class of neurons having exceptionally large somata was observed. Frequency histograms of the maximum number of action potentials fired from 240-ms step depolarizations showed that neurons could be classified as either slowly adapting or rapidly adapting. Most neurons (85%) were in the rapidly adapting category (58 of 68 recordings). Measurements of elementary properties were used to define the endogenous firing characteristics of both neuron classes. Action potential number varied with step and holding potential, spike amplitude decayed during prolonged depolarizations, and spike frequency adaptation was observed in both rapidly and slowly adapting neurons. The apparent input resistance, spike amplitude decrement, and instantaneous firing frequency differed significantly between rapidly and slowly adapting neurons. Inward rectification was evaluated in response to hyperpolarizing constant current injections. Present in both electrophysiological classes, its magnitude was graded from neuron to neuron, reflecting differences in number, type, and/or voltage dependence of the underlying channels. These data suggest that spiral ganglion neurons possess intrinsic firing properties that regulate action potential number and timing, features that may be crucial to signal coding in the auditory periphery.

Molecular identity, ontogeny, and cAMP modulation of the hyperpolarization-activated current in vestibular ganglion neurons

2012 ◽  
Vol 108 (8) ◽  
pp. 2264-2275 ◽  
Author(s):  
Angélica Almanza ◽  
Enoch Luis ◽  
Francisco Mercado ◽  
Rosario Vega ◽  
Enrique Soto
Keyword(s):  
Current Density ◽  
Small Cells ◽  
Resting Potential ◽  
Afferent Neuron ◽  
Intracellular Camp ◽  
Rt Pcr ◽  
Patch Clamp Technique ◽  
Vestibular Ganglion ◽  
Hyperpolarization Activated Current ◽  
Ganglion Neurons

Properties, developmental regulation, and cAMP modulation of the hyperpolarization-activated current ( Ih) were investigated by the whole cell patch-clamp technique in vestibular ganglion neurons of the rat at two postnatal stages (P7–10 and P25–28). In addition, by RT-PCR and immunohistochemistry the identity and distribution of hyperpolarization-activated and cyclic nucleotide-gated channel (HCN) isoforms that generate Ih were investigated. Ih current density was larger in P25–28 than P7–10 rats, increasing 410% for small cells (<30 pF) and 200% for larger cells (>30 pF). The half-maximum activation voltage ( V1/2) of Ih was −102 mV in P7–10 rats and in P25–28 rats shifted 7 mV toward positive voltages. At both ages, intracellular cAMP increased Ih current density, decreased its activation time constant (τ), and resulted in a rightward shift of V1/2 by 9 mV. Perfusion of 8-BrcAMP increased Ih amplitude and speed up its activation kinetics. Ih was blocked by Cs+, zatebradine, and ZD7288. As expected, these drugs also reduced the voltage sag caused with hyperpolarizing pulses and prevented the postpulse action potential generation without changes in the resting potential. RT-PCR analysis showed that HCN1 and HCN2 subunits were predominantly amplified in vestibular ganglia and end organs and HCN3 and HCN4 to a lesser extent. Immunohistochemistry showed that the four HCN subunits were differentially expressed (HCN1 > HCN2 > HCN3 ≥ HCN4) in ganglion slices and in cultured neurons at both P7–10 and P25–28 stages. Developmental changes shifted V1/2 of Ih closer to the resting membrane potential, increasing its functional role. Modulation of Ih by cAMP-mediated signaling pathway constitutes a potentially relevant control mechanism for the modulation of afferent neuron discharge.

scholarly journals Functional contributions of HCN channels in the primary auditory neurons of the mouse inner ear

2013 ◽  
Vol 142 (3) ◽  
pp. 207-223 ◽  
Author(s):  
Ye-Hyun Kim ◽  
Jeffrey R. Holt
Keyword(s):  
Signal Transmission ◽  
Spiral Ganglion ◽  
Auditory Brainstem ◽  
Spike Timing ◽  
Membrane Properties ◽  
Auditory Brainstem Responses ◽  
Resting Potential ◽  
Hcn Channels ◽  
Adult Mice ◽  
Ganglion Neurons

The hyperpolarization-activated current, Ih, is carried by members of the Hcn channel family and contributes to resting potential and firing properties in excitable cells of various systems, including the auditory system. Ih has been identified in spiral ganglion neurons (SGNs); however, its molecular correlates and their functional contributions have not been well characterized. To investigate the molecular composition of the channels that carry Ih in SGNs, we examined Hcn mRNA harvested from spiral ganglia of neonatal and adult mice using quantitative RT-PCR. The data indicate expression of Hcn1, Hcn2, and Hcn4 subunits in SGNs, with Hcn1 being the most highly expressed at both stages. To investigate the functional contributions of HCN subunits, we used the whole-cell, tight-seal technique to record from wild-type SGNs and those deficient in Hcn1, Hcn2, or both. We found that HCN1 is the most prominent subunit contributing to Ih in SGNs. Deletion of Hcn1 resulted in reduced conductance (Gh), slower activation kinetics (τfast), and hyperpolarized half-activation (V1/2) potentials. We demonstrate that Ih contributes to SGN function with depolarized resting potentials, depolarized sag and rebound potentials, accelerated rebound spikes after hyperpolarization, and minimized jitter in spike latency for small depolarizing stimuli. Auditory brainstem responses of Hcn1-deficient mice showed longer latencies, suggesting that HCN1-mediated Ih is critical for synchronized spike timing in SGNs. Together, our data indicate that Ih contributes to SGN membrane properties and plays a role in temporal aspects of signal transmission between the cochlea and the brain, which are critical for normal auditory function.

Otopathologic Abnormalities in CHARGE Syndrome

2021 ◽  
pp. 019459982110089
Author(s):  
Rafael da Costa Monsanto ◽  
Renata Malimpensa Knoll ◽  
Norma de Oliveira Penido ◽  
Grace Song ◽  
Felipe Santos ◽  
...  
Keyword(s):  
Facial Nerve ◽  
Middle Ear ◽  
Spiral Ganglion ◽  
Internal Auditory Canal ◽  
Semicircular Canals ◽  
Charge Syndrome ◽  
University Of Minnesota ◽  
Bony Canal ◽  
Ganglion Neurons ◽  
Temporal Bones

Objective To perform an otopathologic analysis of temporal bones (TBs) with CHARGE syndrome. Study Design Otopathologic study of human TB specimens. Setting Otopathology laboratories. Methods From the otopathology laboratories at the University of Minnesota and Massachusetts Eye and Ear Infirmary, we selected TBs from donors with CHARGE syndrome. These TBs were serially sectioned at a thickness of 20 µm, and every 10th section was stained with hematoxylin and eosin. We performed otopathologic analyses of the external ear, middle ear (middle ear cleft, mucosal lining, ossicles, mastoid, and facial nerve), and inner ear (cochlea, vestibule, internal auditory canal, and cochlear and vestibular nerves). The gathered data were statistically analyzed. Results Our study included 12 TBs from 6 donors. We found a high prevalence of abnormalities affecting the ears. The most frequent findings were stapes malformation (100%), aberrant course of the facial nerve (100%) with narrow facial recess (50%), sclerotic and hypodeveloped mastoids (50%), cochlear (100%) and vestibular (83.3%) hypoplasia with aplasia of the semicircular canals, hypoplasia and aplasia of the cochlear (66.6%) and vestibular (91.6%) nerves, and narrowing of the bony canal of the cochlear nerve (66.6%). The number of spiral ganglion and Scarpa’s ganglion neurons were decreased in all specimens (versus normative data). Conclusions In our study, CHARGE syndrome was associated with multiple TB abnormalities that may severely affect audiovestibular function and rehabilitation.

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