Voltage-Sensitive Conductances of Bushy Cells of the Mammalian Ventral Cochlear Nucleus

2007 ◽  
Vol 97 (6) ◽  
pp. 3961-3975 ◽  
Author(s):  
Xiao-Jie Cao ◽  
Shalini Shatadal ◽  
Donata Oertel
Keyword(s):  
Cochlear Nucleus ◽  
Low Voltage ◽  
Nerve Fibers ◽  
Superior Olivary Complex ◽  
Voltage Sensitivity ◽  
Sound Sources ◽  
Temporal Precision ◽  
Ventral Cochlear Nucleus ◽  
Cation Conductance ◽  
Bushy Cells

Bushy cells in the ventral cochlear nucleus convey firing of auditory nerve fibers to neurons in the superior olivary complex that compare the timing and intensity of sounds at the two ears and enable animals to localize sound sources in the horizontal plane. Three voltage-sensitive conductances allow bushy cells to convey acoustic information with submillisecond temporal precision. All bushy cells have a low-voltage-activated, α-dendrotoxin (α-DTX)-sensitive K+ conductance ( gKL) that was activated by depolarization past −70 mV, was half-activated at −39.0 ± 1.7 (SE) mV, and inactivated ∼60% over 5 s. Maximal gKL varied between 40 and 150 nS (mean: 80.8 ± 16.7 nS). An α-DTX-insensitive, tetraethylammonium (TEA)-sensitive, K+ conductance ( gKH) was activated at voltages positive to −40 mV, was half-activated at −18.1 ± 3.8 mV, and inactivated by 90% over 5 s. Maximal gKH varied between 35 and 80 nS (mean: 58.2 ± 6.5 nS). A ZD7288-sensitive, mixed cation conductance ( gh) was activated by hyperpolarization greater than −60 mV and half-activated at −83.1 ± 1.1 mV. Maximum gh ranged between 14.5 and 56.6 nS (mean: 30.0 ± 5.5 nS). 8-Br-cAMP shifted the voltage sensitivity of gh positively. Changes in temperature stably altered the steady-state magnitude of Ih. Both gKL and gKH contribute to repolarizing action potentials and to sharpening synaptic potentials. Those cells with the largest gh and the largest gKL fired least at the onset of a depolarization, required the fastest depolarizations to fire, and tended to be located nearest the nerve root.

Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons

1990 ◽  
Vol 63 (5) ◽  
pp. 1169-1190 ◽  
Author(s):  
G. A. Spirou ◽  
W. E. Brownell ◽  
M. Zidanic
Keyword(s):  
Cochlear Nucleus ◽  
Small Diameter ◽  
Nerve Fibers ◽  
Superior Olivary Complex ◽  
Ventral Cochlear Nucleus ◽  
Medial Nucleus ◽  
Large Branch ◽  
Pass Through ◽  
Trapezoid Body ◽  
Bushy Cells

1. Recordings were made from single nerve fibers in barbiturate-anesthetized cats in the midline trapezoid body, a location that permits selective sampling of efferent cells of the ventral cochlear nucleus. Single units were localized to either the dorsal or ventral components of the trapezoid body. The fibers were physiologically classified on the basis of their peristimulus time histograms (PSTH) and receptive-field properties. In addition, low characteristic frequency (CF) units were probed for rapid rate and phase shifts with increases in intensity. The projection patterns of some fibers were traced by iontophoresing horseradish peroxidase (HRP) into their axons. 2. HRP-labeled fibers most likely originated from globular bushy cells of the ventral cochlear nucleus in that they sent a large branch into the contralateral medial nucleus of the trapezoid body which terminated in a calyceal ending and an ipsilateral branch into the lateral nucleus of the trapezoid body. A thin branch, usually starting from the large branch, wound its way through the medial nucleus of the trapezoid body to its termination in the ventral nucleus of the trapezoid body. Additional branches from the parent axon could pass through medial periolivary groups throughout the rostrocaudal extent of the superior olivary complex. The parent fiber was traced as far as the ventral lateral lemniscus where it faded before reaching its termination. 3. The majority of units were recorded in the ventral component of the trapezoid body. Although the ventral component is comprised of both large and small diameter fibers, our sample was biased to the larger diameter fibers representing the activity of axons originating from globular bushy cells in the ventral cochlear nucleus. Ventral component units were not tonotopically arrayed and had CFs that spanned the audible range for cats. HRP labeling of ventral component axons revealed that the section of the axon traveling through the midline shifted its dorsal-ventral location. This pattern was compatible with the lack of tonotopy found in the ventral component. Recordings were also made from the dorsal component of the trapezoid body, which contained medium diameter axons. These axons originated from spherical bushy cells in the ventral cochlear nucleus. Dorsal component units were tonotopically arrayed and had CFs less than 7 kHz. 4. Cells were characterized by their PSTH at CF. Primary-like and phase-locked units constituted most of the dorsal component units.(ABSTRACT TRUNCATED AT 400 WORDS)

Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: implications of a computational model

1993 ◽  
Vol 70 (6) ◽  
pp. 2562-2583 ◽  
Author(s):  
J. S. Rothman ◽  
E. D. Young ◽  
P. B. Manis
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Full Range ◽  
Nerve Fibers ◽  
Membrane Properties ◽  
Delayed Rectifier ◽  
Current Clamp ◽  
Synaptic Inputs ◽  
Ventral Cochlear Nucleus ◽  
Bushy Cells

1. Convergence of auditory nerve (AN) fibers onto bushy cells of the ventral cochlear nucleus (VCN) was investigated with a model that describes the electrical membrane properties of these cells. The model consists of a single compartment, representing the soma, and includes three voltage-sensitive ion channels (fast sodium, delayed-rectifier-like potassium, and low-threshold potassium). These three channels have characteristics derived from voltage clamp data of VCN bushy cells. The model also contains a leakage channel, membrane capacitance, and synaptic inputs. The model accurately reproduces the membrane rectification seen in current clamp studies of bushy cells, as well as their unique current clamp responses. 2. In this study, the number and synaptic strength of excitatory AN inputs to the model were varied to investigate the relationship between input convergence parameters and response characteristics. From 1 to 20 excitatory synaptic inputs were applied through channels in parallel with the voltage-gated channels. Each synapse was driven by an independent AN spike train; spike arrivals produced brief (approximately 0.5 ms) conductance increases. The number (NS) and conductance (AE) of these inputs were systematically varied. The input spike trains were generated as a renewal point process that accurately models characteristics of AN fibers (refractoriness, adaptation, onset latency, irregularity of discharge, and phase locking). Adaptation characteristics of both high and low spontaneous rate (SR) AN fibers were simulated. 3. As NS and AE vary over the ranges 1–20 and 3–80 nS, respectively, the full range of response types seen in VCN bushy cells are produced by the model, with AN inputs typical of high-SR AN fibers. These include primarylike (PL), primarylike-with-notch (Pri-N), and onset-L (On-L). In addition, Onset responses, whose association with bushy cells in uncertain, and “dip” responses, which are not seen in the VCN, are produced. Dip responses occur with large NS and/or AE, and are due to depolarization block. When the AN inputs have the adaptation characteristics of low-SR AN fibers, PL--but not Pri-N or On-L responses--are produced. This suggests that neurons showing Pri-N and On-L responses must receive high-SR AN inputs. 4. The regularity of discharge of the model is compared with that of VCN bushy cells, using a measure derived from the mean and standard deviation of interspike intervals. Regularity is an important constraint on the model because the regularity of VCN bushy cells is the same as that of their AN inputs.(ABSTRACT TRUNCATED AT 400 WORDS)

Temperature Affects Voltage-Sensitive Conductances Differentially in Octopus Cells of the Mammalian Cochlear Nucleus

2005 ◽  
Vol 94 (1) ◽  
pp. 821-832 ◽  
Author(s):  
Xiao-Jie Cao ◽  
Donata Oertel
Keyword(s):  
Cochlear Nucleus ◽  
Action Potentials ◽  
Low Voltage ◽  
Voltage Sensitivity ◽  
Physiological Variable ◽  
Cation Conductance ◽  
Electrophysiological Measurements ◽  
Measured Time ◽  
Lower Temperature ◽  
Kinetics Of

Temperature is an important physiological variable the influence of which on macroscopic electrophysiological measurements in slices is not well documented. We show that each of three voltage-sensitive conductances of octopus cells of the mammalian ventral cochlear nucleus (VCN) is affected differently by changes in temperature. As expected, the kinetics of the currents were faster at higher than at lower temperature. Where they could be measured, time constants of activation, deactivation, and inactivation had Q10 values between 1.8 and 4.6. The magnitude of the peak conductances was differentially affected by temperature. While the peak magnitude of the high-voltage-activated K+ conductance, gKH, was unaffected by changes in temperature, the peak of the low-voltage-activated K+ conductance, gKL, was reduced by half when the temperature was lowered from 33 to 23°C ( Q10 = 2). Changing the temperature changed the kinetics and the magnitude of the hyperpolarization-activated mixed cation conductance, gh, but the changes in magnitude were transient. The voltage sensitivity of the three conductances was unaffected by temperature. The action of temperature on these conductances is reflected in the resting potentials and in the shapes of action potentials.

Octopus Cells of the Mammalian Ventral Cochlear Nucleus Sense the Rate of Depolarization

2002 ◽  
Vol 87 (5) ◽  
pp. 2262-2270 ◽  
Author(s):  
Michael J. Ferragamo ◽  
Donata Oertel
Keyword(s):  
Synaptic Input ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Action Potentials ◽  
Dynamic Properties ◽  
Nerve Fibers ◽  
Temporal Precision ◽  
Ventral Cochlear Nucleus ◽  
Threshold Rate ◽  
Auditory Nerve Fibers

Whole cell patch recordings in slices show that the probability of firing of action potentials in octopus cells of the ventral cochlear nucleus depends on the dynamic properties of depolarization. Octopus cells fired only when the rate of rise of a depolarization exceeded a threshold value that varied between 5 and 15 mV/ms among cells. The threshold rate of rise was independent of whether depolarizations were evoked synaptically or by the intracellular injection of current. Previous work showed that octopus cells are contacted by many auditory nerve fibers, each providing less than 1-mV depolarization. Summation of synaptic input from multiple fibers is required for an octopus cell to reach threshold. In firing only when synaptic depolarization exceeds a threshold rate, octopus cells fire selectively when synaptic input is sufficiently large and synchronized for the small, brief unitary excitatory postsynaptic potentials (EPSPs) to sum to produce a rapidly rising depolarization. The sensitivity to rate of depolarization is governed by a low-threshold, α-dendrotoxin-sensitive potassium conductance ( g KL). This conductance also shapes the peaks of action potentials, contributing to the precision in their timing. Firing in neighboring T stellate cells depends much less strongly on the rate of rise. They lack strong α-dendrotoxin-sensitive conductances. Octopus cells appear to be specialized to detect synchronization in the activation of groups of auditory nerve fibers, a common pattern in responses to natural sounds, and convey its occurrence with temporal precision.

Encoding timing and intensity in the ventral cochlear nucleus of the cat

1986 ◽  
Vol 56 (2) ◽  
pp. 261-286 ◽  
Author(s):  
W. S. Rhode ◽  
P. H. Smith
Keyword(s):  
Firing Rate ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Cell Types ◽  
Nerve Fibers ◽  
Frequency Selectivity ◽  
Firing Rates ◽  
Ventral Cochlear Nucleus ◽  
Auditory Nerve Fibers ◽  
Different Cell Types

Physiological response properties of neurons in the ventral cochlear nucleus have a variety of features that are substantially different from the stereotypical auditory nerve responses that serve as the principal source of activation for these neurons. These emergent features are the result of the varying distribution of auditory nerve inputs on the soma and dendrites of the various cell types within the nucleus; the intrinsic membrane characteristics of the various cell types causing different responses to the same input in different cell types; and secondary excitatory and inhibitory inputs to different cell types. Well-isolated units were recorded with high-impedance glass microelectrodes, both intracellularly and extracellularly. Units were characterized by their temporal response to short tones, rate vs. intensity relation, and response areas. The principal response patterns were onset, chopper, and primary-like. Onset units are characterized by a well-timed first spike in response to tones at the characteristic frequency. For frequencies less than 1 kHz, onset units can entrain to the stimulus frequency with greater precision than their auditory nerve inputs. This implies that onset units receive converging inputs from a number of auditory nerve fibers. Onset units are divided into three subcategories, OC, OL, and OI. OC units have extraordinarily wide dynamic ranges and low-frequency selectivity. Some are capable of sustaining firing rates of 800 spikes/s at high intensities. They have the smallest standard deviation and coefficient of variation of the first spike latency of any cells in the cochlear nuclei. OC units are candidates for encoding intensity. OI and OL units differ from OC units in that they have dynamic ranges and frequency selectivity ranges much like those of auditory nerve fibers. They differ from one another in their steady-state firing rates; OI units fire mainly at the onset of a tone. OI units also differ from OL units in that they prefer frequency sweeps in the low to high direction. Primary-like-with-notch (PLN) units also respond to tones with a well-timed first spike. They differ from onset cells in that the onset peak is not always as precise as the spontaneous rate is higher. A comparison of spontaneous firing rate and saturation firing rate of PLN units with auditory nerve fibers suggest that PLN units receive one to four auditory nerve fiber inputs. Chopper units fire in a sustained regular manner when they are excited by sound.(ABSTRACT TRUNCATED AT 400 WORDS)

Differential Expression of Three Distinct Potassium Currents in the Ventral Cochlear Nucleus

2003 ◽  
Vol 89 (6) ◽  
pp. 3070-3082 ◽  
Author(s):  
Jason S. Rothman ◽  
Paul B. Manis
Keyword(s):  
Differential Expression ◽  
Cochlear Nucleus ◽  
Nerve Fibers ◽  
Delayed Rectifier ◽  
High Threshold ◽  
Type I ◽  
Acoustic Environment ◽  
Ventral Cochlear Nucleus ◽  
Wide Range ◽  
Slope Factor

In the ventral cochlear nucleus (VCN), neurons transform information from auditory nerve fibers into a set of parallel ascending pathways, each emphasizing different aspects of the acoustic environment. Previous studies have shown that VCN neurons differ in their intrinsic electrical properties, including the K+ currents they express. In this study, we examine these K+ currents in more detail using whole cell voltage-clamp techniques on isolated VCN cells from adult guinea pigs at 22°C. Our results show a differential expression of three distinct K+ currents. Whereas some VCN cells express only a high-threshold delayed-rectifier-like current ( IHT), others express IHT in combination with a fast inactivating current ( IA) and/or a slow-inactivating low-threshold current ( ILT). IHT, ILT, and IA, were partially blocked by 1 mM 4-aminopyridine. In contrast, only ILT was blocked by 10–100 nM dendrotoxin-I. A surprising finding was the wide range of levels of ILT, suggesting ILT is expressed as a continuum across cell types rather than modally in a particular cell type. IA, on the other hand, appears to be expressed only in cells that show little or no ILT, the Type I cells. Boltzmann analysis shows IHT activates with 164 ± 12 (SE) nS peak conductance, -14.3 ± 0.7 mV half-activation, and 7.0 ± 0.5 mV slope factor. Similar analysis shows ILT activates with 171 ± 22 nS peak conductance, -47.4 ± 1.0 mV half-activation, and 5.8 ± 0.3 mV slope factor.

scholarly journals The magnitudes of hyperpolarization-activated and low-voltage-activated potassium currents co-vary in neurons of the ventral cochlear nucleus

2011 ◽  
Vol 106 (2) ◽  
pp. 630-640 ◽  
Author(s):  
Xiao-Jie Cao ◽  
Donata Oertel
Keyword(s):  
Cochlear Nucleus ◽  
Low Voltage ◽  
Resting Potential ◽  
Wild Type ◽  
Α Subunit ◽  
Time Constants ◽  
Ventral Cochlear Nucleus ◽  
Icr Mice ◽  
Neuronal Types ◽  
Type Strains

In the ventral cochlear nucleus (VCN), neurons have hyperpolarization-activated conductances, which in some cells are enormous, that contribute to the ability of neurons to convey acoustic information in the timing of their firing by decreasing the input resistance and speeding-up voltage changes. Comparisons of the electrophysiological properties of neurons in the VCN of mutant mice that lack the hyperpolarization-activated cyclic nucleotide-gated channel α subunit 1 (HCN1−/−) ( Nolan et al. 2003 ) with wild-type controls (HCN1+/+) and with outbred ICR mice reveal that octopus, T stellate, and bushy cells maintain their electrophysiological distinctions in all strains. Hyperpolarization-activated (Ih) currents were smaller and slower, input resistances were higher, and membrane time constants were longer in HCN1−/− than in HCN1+/+ in octopus, bushy, and T stellate cells. There were significant differences in the average magnitudes of Ih, input resistances, and time constants between HCN1+/+ and ICR mice, but the resting potentials did not differ between strains. Ih is opposed by a low-voltage-activated potassium (IKL) current in bushy and octopus cells, whose magnitudes varied widely between neuronal types and between strains. The magnitudes of Ih and IKL were correlated across neuronal types and across mouse strains. Furthermore, these currents balanced one another at the resting potential in individual cells. The magnitude of Ih and IKL is linked in bushy and octopus cells and varies not only between HCN1−/− and HCN1+/+ but also between “wild-type” strains of mice, raising the question to what extent the wild-type strains reflect normal mice.

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