scholarly journals Small dendritic synapses enhance temporal coding in a model of cochlear nucleus bushy cells

2021 ◽  
Author(s):  
Elisabeth Koert ◽  
Thomas Kuenzel
Keyword(s):  
Membrane Potential ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Stimulus Frequency ◽  
Dendritic Tree ◽  
Temporal Coding ◽  
Functional Explanation ◽  
Model Parameters ◽  
Temporal Precision ◽  
Bushy Cells

Spherical bushy cells (SBCs) in the the anteroventral cochlear nucleus receive a single or very few powerful axosomatic inputs from the auditory nerve. However, SBCs are also contacted by small regular bouton synapses of the auditory nerve, located in their dendritic tree. The function of these small inputs is unknown. It was speculated that the interaction of axosomatic inputs with small dendritic inputs improved temporal precision, but direct evidence for this is missing. In a compartment model of spherical bushy cells with a stylized or realistic 3D-representation of the bushy dendrite we thus explored this proposal. Phase-locked dendritic inputs caused both tonic depolarization and a modulation of the model SBC membrane potential at the frequency of the stimulus. For plausible model parameters dendritic inputs were subthreshold. Instead, the tonic depolarization increased the excitability of the SBC model and the modulation of the membrane potential caused a phase-dependent increase in the efficacy of the main axosomatic input. This improved rate, entrainment and temporal precision of output action potentials. However, these effects showed differential dependency on the stimulus frequency. A careful exploration of morphological and biophysical parameters of the bushy dendrite suggested a functional explanation for the peculiar shape of the bushy dendrite. Our model for the first time directly implied a role for the small excitatory dendritic inputs in auditory processing: they modulate the efficacy of the main input and are thus a plausible mechanism for the improvement of temporal precision and fidelity in these central auditory neurons.

scholarly journals Small dendritic synapses enhance temporal coding in a model of cochlear nucleus bushy cells

2020 ◽  
Author(s):  
Elisabeth Koert ◽  
Thomas Kuenzel
Keyword(s):  
Membrane Potential ◽  
Cochlear Nucleus ◽  
Temporal Coding ◽  
Fine Tuning ◽  
Model Parameters ◽  
Biophysical Parameters ◽  
Temporal Precision ◽  
Main Input ◽  
The Impact ◽  
Bushy Cells

AbstractSpherical bushy cells (SBC) in the the anteroventral cochlear nucleus can improve the temporal precision of the auditory nerve spiking activity despite receiving sometimes only a single suprathreshold axosomatic input. The interaction with small dendritic inputs could provide a possible explanation for this phenomenon. In a compartment model of spherical bushy cells with a stylized or realistic three-dimensional representation of the bushy dendrite we explored this proposal. Phase-locked dendritic inputs caused both a tonic depolarization and a modulation of the SBC membrane potential at the frequency of the stimulus but for plausible model parameters do not cause output action potentials (AP). The tonic depolarization increased the excitability of the SBC model. The modulation of the membrane potential caused a phase-dependent increase in the efficacy of the main axosomatic input to cause output AP. These effects increased the rate and the temporal precision of output AP. Rate was mainly increased for stimulus frequencies at and below the characteristic frequency of the main input. Precision mostly increased for higher frequencies above about 1 kHz. Dendritic morphological parameters, biophysical parameters of the dendrite and the synaptic inputs and tonotopic parameters of the inputs all affected the impact of dendritic synapses. This suggested the possibility of fine tuning of the effect the dendritic inputs have for different coding demands or input frequency ranges. Excitatory dendritic inputs modulate the processing of the main input and are thus a plausible mechanism for the improvement of temporal precision in spherical bushy cells.

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)

Regularity analysis in a compartmental model of chopper units in the anteroventral cochlear nucleus

1991 ◽  
Vol 65 (3) ◽  
pp. 606-629 ◽  
Author(s):  
M. I. Banks ◽  
M. B. Sachs
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Compartmental Model ◽  
Dendritic Tree ◽  
Stellate Cells ◽  
Physiological Data ◽  
Response Patterns ◽  
Anteroventral Cochlear Nucleus

1. We investigate the discharge patterns of chopper units in the anteroventral cochlear nucleus (AVCN) by developing an equivalent cylinder compartmental model of AVCN stellate cells, which are the sources of the chopper response pattern. The model consists of a passive dendritic tree connected to somatic and axonal compartments with voltage-sensitive channels. Synaptic inputs to the model are simulated auditory nerve fiber responses to best-frequency tones. 2. We adjust the anatomic and electrical parameters of the model to agree with available intracellular data from stellate cells in the AVCN of the mouse and the cat and compare the response of the model to injected current with responses recorded in vitro. The model shows approximately linear current-voltage characteristics for small hyperpolarizing currents. The model's input resistance and the time course of its response to hyperpolarizing current applied at the soma are comparable with those measured from stellate cells in vitro. In response to sustained depolarizing current, the model fires repetitively with nearly perfect regularity, a property also observed in vitro. 3. Auditory nerve inputs to the cell are modeled as deadtime-modified Poisson processes with a multiexponential adaptation in the Poisson rate. We are able to adjust the number, rate, and location of excitatory and inhibitory inputs to the model and succeed in simulating chopper response patterns seen in vivo. 4. Chopper units exhibit a variety of regularity and adaptation patterns in response to tone stimuli. Physiological data from brain slice experiments and experiments in vivo imply that this heterogeneity is primarily due to differences in input configurations. By systematically varying the number and position of excitatory and inhibitory inputs, we can simulate a range of chopper response patterns. 5. We quantify the regularity of the model's response using the coefficient of variation (CV) of the interspike interval. We find that the CV decreases, i.e., the regularity increases, as the number of converging inputs or their distance from the soma increases. The regularity of the output is more sensitive to the number of converging inputs than to their location on the dendritic tree. The statistics of the first spike latency (FSL) are also sensitive to the configuration of excitatory inputs. The mean and minimum FSL are more sensitive to the electrotonic distance of the inputs from the soma than to the number of inputs, whereas the standard deviation of the FSL is highly dependent on the number of converging inputs and is nearly independent of their location.(ABSTRACT TRUNCATED AT 400 WORDS)

The Functional Role of Excitatory and Inhibitory Interactions in Chopper Cells of the Anteroventral Cochlear Nucleus

1994 ◽  
Vol 6 (6) ◽  
pp. 1127-1140 ◽  
Author(s):  
Ying-Cheng Lai ◽  
Raimond L. Winslow ◽  
Murray B. Sachs
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Dendritic Tree ◽  
Nerve Fibers ◽  
High Threshold ◽  
Spontaneous Rate ◽  
Anteroventral Cochlear Nucleus ◽  
Rate Versus ◽  
High Stimulus ◽  
Auditory Nerve Fibers

Chopper cells in the anteroventral cochlear nucleus of the cat maintain a robust rate-place representation of vowel spectra over a broad range of stimulus levels. This representation resembles that of low threshold, high spontaneous rate primary auditory nerve fibers at low stimulus levels, and that of high threshold, low spontaneous rate auditory-nerve fibers at high stimulus levels. This has led to the hypothesis that chopper cells in the anteroventral cochlear nucleus selectively process inputs from different spontaneous rate populations of primary auditory-nerve fibers at different stimulus levels. We present a computational model, making use of shunting inhibition, for how this level dependent processing may be performed within the chopper cell dendritic tree. We show that this model (1) implements level-dependent selective processing, (2) reproduces detailed features of real chopper cell post-stimulus-time histograms, and (3) reproduces nonmonotonic rate versus level functions in response to single tones measured.

Differential contributions of voltage-gated potassium channel subunits in enhancing temporal coding in the bushy cells of the ventral cochlear nucleus

2021 ◽  
Author(s):  
Mingyu Fu ◽  
Lu Zhang ◽  
Xiao Xie ◽  
Ningqian Wang ◽  
Zhongju Xiao
Keyword(s):  
Cochlear Nucleus ◽  
Spike Timing ◽  
Temporal Coding ◽  
Membrane Properties ◽  
Membrane Excitability ◽  
Patch Clamp Recording ◽  
Voltage Gated ◽  
Ventral Cochlear Nucleus ◽  
Kv Channels ◽  
Bushy Cells

Temporal coding precision of bushy cells in the ventral cochlear nucleus (VCN), critical for sound localization and communication, depends on the generation of rapid and temporally precise action potentials (APs). Voltage-gated potassium (Kv) channels are critically involved in this. The bushy cells in rat VCN express Kv1.1, 1.2, 1.3, 1.6, 3.1, 4.2 and 4.3 subunits. The Kv1.1 subunit contributes to the generation of a temporally precise single AP. However, the understanding of the functions of other Kv subunits expressed in the bushy cells is limited. Here, we investigated the functional diversity of Kv subunits concerning their contributions to temporal coding. We characterized the electrophysiological properties of the Kv channels with different subunits using whole-cell patch-clamp recording and pharmacological methods. The neuronal firing pattern changed from single to multiple APs only when the Kv1.1 subunit was blocked. The Kv subunits, including the Kv1.1, 1.2, 1.6 or 3.1, were involved in enhancing temporal coding by lowering membrane excitability, shortening AP latencies, reducing jitter and regulating AP kinetics. Meanwhile, all the Kv subunits contributed to rapid repolarization and sharpening peaks by narrowing half-width and accelerating fall rate, while the Kv1.1 subunit also affected the depolarization of AP. The Kv1.1, 1.2 and 1.6 subunits endowed bushy cells with a rapid time constant and a low input resistance of membrane for enhancing spike timing precision. The present results indicate that the Kv channels differentially affect intrinsic membrane properties to optimize the generation of rapid and reliable APs for temporal coding.

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.

scholarly journals Synaptic transmission between end bulbs of Held and bushy cells in the cochlear nucleus of mice with a mutation in Otoferlin

2014 ◽  
Vol 112 (12) ◽  
pp. 3173-3188 ◽  
Author(s):  
Samantha Wright ◽  
Youngdeok Hwang ◽  
Donata Oertel
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Calcium Binding ◽  
Otoacoustic Emissions ◽  
Nerve Fibers ◽  
Mutant Mice ◽  
Synaptic Current ◽  
Cross Sectional ◽  
Distortion Product ◽  
Bushy Cells

Mice that carry a mutation in a calcium binding domain of Otoferlin, the putative calcium sensor at hair cell synapses, have normal distortion product otoacoustic emissions (DPOAEs), but auditory brain stem responses (ABRs) are absent. In mutant mice mechanotransduction is normal but transmission of acoustic information to the auditory pathway is blocked even before the onset of hearing. The cross-sectional area of the auditory nerve of mutant mice is reduced by 54%, and the volume of ventral cochlear nuclei is reduced by 46% relative to hearing control mice. While the tonotopic organization was not detectably changed in mutant mice, the axons to end bulbs of Held and the end bulbs themselves were smaller. In mutant mice bushy cells in the anteroventral cochlear nucleus (aVCN) have the electrophysiological hallmarks of control cells. Spontaneous miniature excitatory postsynaptic currents (EPSCs) occur with similar frequencies and have similar shapes in deaf as in hearing animals, but they are 24% larger in deaf mice. Bushy cells in deaf mutant mice are contacted by ∼2.6 auditory nerve fibers compared with ∼2.0 in hearing control mice. Furthermore, each fiber delivers more synaptic current, on average 4.8 nA compared with 3.4 nA, in deaf versus hearing control mice. The quantal content of evoked EPSCs is not different between mutant and control mice; the increase in synaptic current delivered in mutant mice is accounted for by the increased response to the size of the quanta. Although responses to shocks presented at long intervals are larger in mutant mice, they depress more rapidly than in hearing control mice.

scholarly journals Temporal Coding of Periodicity Pitch in the Auditory System: An Overview

1999 ◽  
Vol 6 (4) ◽  
pp. 147-172 ◽  
Author(s):  
Peter Cariani
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Sensory Information ◽  
Nerve Fibers ◽  
Temporal Coding ◽  
Single Type ◽  
Time Of Arrival ◽  
Type I ◽  
Pitch Frequency ◽  
Auditory Nerve Fibers

This paper outlines a taxonomy of neural pulse codes and reviews neurophysiological evidence for interspike interval-based representations for pitch and timbre in the auditory nerve and cochlear nucleus. Neural pulse codes can be divided into channel-based codes, temporal-pattern codes, and time-of-arrival codes. Timings of discharges in auditory nerve fibers reflect the time structure of acoustic waveforms, such that the interspike intervals that are produced precisely convey information concerning stimulus periodicities. Population-wide inter-spike interval distributions are constructed by summing together intervals from the observed responses of many single Type I auditory nerve fibers. Features in such distributions correspond closely with pitches that are heard by human listeners. The most common all-order interval present in the auditory nerve array almost invariably corresponds to the pitch frequency, whereas the relative fraction of pitchrelated intervals amongst all others qualitatively corresponds to the strength of the pitch. Consequently, many diverse aspects of pitch perception are explained in terms of such temporal representations. Similar stimulus-driven temporal discharge patterns are observed in major neuronal populations of the cochlear nucleus. Population-interval distributions constitute an alternative time-domain strategy for representing sensory information that complements spatially organized sensory maps. Similar autocorrelation-like representations are possible in other sensory systems, in which neural discharges are time-locked to stimulus waveforms.

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