Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells

1994 ◽  
Vol 71 (3) ◽  
pp. 914-930 ◽  
Author(s):  
S. Zhang ◽  
D. Oertel
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Nerve Fibers ◽  
Dorsal Cochlear Nucleus ◽  
Resting Potential ◽  
Temporal Association ◽  
Common Source ◽  
Excitatory Postsynaptic Potential ◽  
Current Voltage ◽  
Synaptic Responses

1. Intracellular recordings were made from 21 anatomically identified fusiform cells in the dorsal cochlear nucleus (DCN) of mice in slices. The aim of the experiments was to dissect the synaptic responses to shocks of the auditory nerve to correlate functional characteristics with the different classes of synaptic inputs. 2. When depolarized from rest (-57 +/- 5 mV) with current pulses, fusiform cells fired regular, overshooting action potentials that were followed by two undershoots. The frequency of firing increased with the strength of injected current by between 100 and 300 spikes/s/nA. The current-voltage relationship rectified between 10 and 15 mV below the resting potential. The slopes of current-voltage relationships of fusiform cells in the range between the resting potential and 10 mV hyperpolarization indicated an average input resistance of 86 +/- 37 M omega. 3. In each of the labeled fusiform cells frequent, spontaneous inhibitory postsynaptic potentials (IPSPs) were recorded singly or in bursts. Some, but not all, IPSPs were preceded by a slowly rising excitatory postsynaptic potential (EPSP). The temporal association of spontaneous EPSPs and IPSPs suggests that they are driven by a common source, possibly granule cells. 4. Shocks to the auditory nerve evoked synaptic responses consisting of early (1 to approximately 10 ms) and late (approximately 10 to 100 ms) components. 6,7-Dinitroquinoxaline-2,3-dione (DNQX) at 20 to 40 microM eliminated all detectable excitation and all late IPSPs. Late bursts of IPSPs, therefore, are mediated through a polysynaptic pathway that includes a DNQX-sensitive stage. Strong shocks to the nerve root elicited single monosynaptic IPSPs, indicating that inhibitory interneurons have processes close to the auditory nerve. Strychnine at 0.5 microM eliminated all detectable inhibition. 6. Cuts through the posteroventral cochlear nucleus (PVCN), which severed the descending branches of auditory nerve fibers, eliminated early EPSPs and IPSPs leaving late, slowly rising EPSPs and bursts of IPSPs in responses to shocks of the auditory nerve. Late, slowly rising EPSPs and bursts of IPSPs, as well as monosynaptic IPSPs, could also be evoked by stimulating the anteroventral cochlear nucleus (AVCN). 7. Focal applications of glutamate evoked excitation and inhibition from many parts of a slice, with patterns varying among cells, indicating that fusiform cells receive inputs through several groups of interneurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Tuberculoventral cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices

1993 ◽  
Vol 69 (5) ◽  
pp. 1409-1421 ◽  
Author(s):  
S. Zhang ◽  
D. Oertel
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Stellate Cells ◽  
Nerve Fibers ◽  
Dorsal Cochlear Nucleus ◽  
Resting Potential ◽  
Intracellular Recordings ◽  
Cochlear Nuclei ◽  
Auditory Nerve Fibers ◽  
Narrow Bands

1. Intracellular recordings were made from six tuberculoventral cells (also called vertical or corn cells) whose identity was confirmed by labeling with biocytin, with the aim of understanding their projection patterns and how their synaptic inputs and their intrinsic electrical properties shape their responses to activation of auditory nerve fibers. 2. The cell bodies, dendrites, and local axonal terminals of all six tuberculoventral cells lay in narrow bands, 70-100 microns wide and parallel to the path of auditory nerve fibers, in the dorsal cochlear nucleus (DCN). Terminals in the ventral cochlear nucleus (VCN) also lay in narrow bands, parallel to the path of auditory nerve fibers in either or both the anteroventral and posteroventral cochlear nuclei. 3. When depolarized with current, tuberculoventral cells fired regularly. The peaks of action potentials were usually overshooting and were followed by two afterhyperpolarizations, resembling other cells of the DCN. Unlike some other cells in the DCN, however, neither of the afterhyperpolarizations resulted in an undershoot of the resting potential in the presence of depolarizing currents stronger than 0.3 nA. The second afterhyperpolarization was more variable than the first. 4. Shocks to the auditory nerve evoked monosynaptic as well as polysynaptic excitation and weak polysynaptic inhibition. These results show that, in addition to receiving excitation directly through auditory nerve fibers, tuberculoventral cells also receive excitation through interneurons. 5. To locate the interneurons in the cochlear nuclei whose activation affects a tuberculoventral cell monosynaptically or polysynaptically, glutamate was applied focally to various loci in the VCN while responses were recorded in a target tuberculoventral cell that was subsequently labeled. Excitation of this tuberculoventral cell arose from a rostrocaudal band in the VCN. 6. The results are consistent with tuberculoventral cells receiving excitatory synaptic input from auditory nerve fibers and from T stellate cells in the VCN. They could be inhibited by D stellate cells in the VCN.

Synaptic Inputs to Stellate Cells in the Ventral Cochlear Nucleus

1998 ◽  
Vol 79 (1) ◽  
pp. 51-63 ◽  
Author(s):  
Michael J. Ferragamo ◽  
Nace L. Golding ◽  
Donata Oertel
Keyword(s):  
Receptor Antagonist ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Stellate Cells ◽  
Nerve Fibers ◽  
Synaptic Inputs ◽  
Ventral Cochlear Nucleus ◽  
Cochlear Nuclei ◽  
Potential Source ◽  
Synaptic Responses

Ferragamo, Michael J., Nace L Golding, and Donata Oertel. Synaptic inputs to stellate cells in the ventral cochlear nucleus. J. Neurophysiol. 79: 51–63, 1998. Auditory information is carried from the cochlear nuclei to the inferior colliculi through six parallel ascending pathways, one of which is through stellate cells of the ventral cochlear nuclei (VCN) through the trapezoid body. To characterize and identify the synaptic influences on T stellate cells, intracellular recordings were made from anatomically identified stellate cells in parasagittal slices of murine cochlear nuclei. Shocks to the auditory nerve consistently evoked five types of synaptic responses in T stellate cells, which reflect sources intrinsic to the cochlear nuclear complex. 1) Monosynaptic excitatory postsynaptic potentials (EPSPs) that were blocked by 6,7-dinitroquinoxaline-2,3-dione (DNQX), an antagonist of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors, probably reflected activation by auditory nerve fibers. Electrophysiological estimates indicate that about five auditory nerve fibers converge on one T stellate cell. 2) Disynaptic, glycinergic inhibitory postsynaptic potentials (IPSPs) arise through inhibitory interneurons in the VCN or in the dorsal cochlear nucleus (DCN). 3) Slow depolarizations, the source of which has not been identified, that lasted between 0.2 and 1 s and were blocked by dl-2-amino-5-phosphonovaleric acid (APV), the N-methyl-d-aspartate (NMDA) receptor antagonist. 4) Rapid, late glutamatergic EPSPs are polysynaptic and may arise from other T stellate cells. 5) Trains of late glycinergic IPSPs after single or repetitive shocks match the responses of D stellate cells, showing that D stellate cells are one source of glycinergic inhibition to T stellate cells. The source of late, polysynaptic EPSPs and IPSPs was assessed electrophysiologically and pharmacologically. Late synaptic responses in T stellate cells were enhanced by repetitive stimulation, indicating that the interneurons from which they arose should fire trains of action potentials in responses to trains of shocks. Late EPSPs and late IPSPs were blocked by APV and enhanced by the removal of Mg2+, indicating that the interneurons were driven at least in part through NMDA receptors. Bicuculline, a γ-aminobutyric acid-A (GABAA) receptor antagonist, enhanced the late PSPs, indicating that GABAergic inhibition suppresses both the glycinergic interneurons responsible for the trains of IPSPs in T-stellate cells and the interneuron responsible for late EPSPs in T stellate cells. The glycinergic interneurons that mediate the series of IPSPs are intrinsic to the ventral cochlear nucleus because long series of IPSPs were recorded from T stellate cells in slices in which the DCN was removed. These experiments indicate that T stellate cells are a potential source of late EPSPs and that D stellate cells are a potential source for trains of late IPSPs.

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)

Frequency Tuning and Spontaneous Activity in the Auditory Nerve and Cochlear Nucleus Magnocellularis of the Barn Owl Tyto alba

1997 ◽  
Vol 77 (1) ◽  
pp. 364-377 ◽  
Author(s):  
Christine Köppl
Keyword(s):  
Response Latency ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Frequency Tuning ◽  
Barn Owl ◽  
Nerve Fibers ◽  
Spontaneous Discharge ◽  
Tyto Alba ◽  
Nucleus Magnocellularis ◽  
Auditory Nerve Fibers

Köppl, Christine. Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. J. Neurophysiol. 77: 364–377, 1997. Single-unit recordings were obtained from the brain stem of the barn owl at the level of entrance of the auditory nerve. Auditory nerve and nucleus magnocellularis units were distinguished by physiological criteria, with the use of the response latency to clicks, the spontaneous discharge rate, and the pattern of characteristic frequencies encountered along an electrode track. The response latency to click stimulation decreased in a logarithmic fashion with increasing characteristic frequency for both auditory nerve and nucleus magnocellularis units. The average difference between these populations was 0.4–0.55 ms. The most sensitive thresholds were ∼0 dB SPL and varied little between 0.5 and 9 kHz. Frequency-threshold curves showed the simple V shape that is typical for birds, with no indication of a low-frequency tail. Frequency selectivity increased in a gradual, power-law fashion with increasing characteristic frequency. There was no reflection of the unusual and greatly expanded mapping of higher frequencies on the basilar papilla of the owl. This observation is contrary to the equal-distance hypothesis that relates frequency selectivity to the spatial respresentation in the cochlea. On the basis of spontaneous rates and/or sensitivity there was no evidence for distinct subpopulations of auditory nerve fibers, such as the well-known type I afferent response classes in mammals. On the whole, barn owl auditory nerve physiology conformed entirely to the typical patterns seen in other bird species. The only exception was a remarkably small spread of thresholds at any one frequency, this being only 10–15 dB in individual owls. Average spontaneous rate was 72.2 spikes/s in the auditory nerve and 219.4 spikes/s for nucleus magnocellularis. This large difference, together with the known properties of endbulb-of-Held synapses, suggests a convergence of ∼2–4 auditory nerve fibers onto one nucleus magnocellularis neuron. Some auditory nerve fibers as well as nucleus magnocellularis units showed a quasiperiodic spontaneous discharge with preferred intervals in the time-interval histogram. This phenomenon was observed at frequencies as high as 4.7 kHz.

Vertical Cell Responses to Sound in Cat Dorsal Cochlear Nucleus

1999 ◽  
Vol 82 (2) ◽  
pp. 1019-1032 ◽  
Author(s):  
William S. Rhode
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Molecular Layer ◽  
Broadband Noise ◽  
Dorsal Cochlear Nucleus ◽  
Type Ii ◽  
Fusiform Cell ◽  
Sound Sources ◽  
Tuning Curves ◽  
Axonal Arbors

The dorsal cochlear nucleus receives input from the auditory nerve and relays acoustic information to the inferior colliculus. Its principal cells receive two systems of inputs. One system through the molecular layer carries multimodal information that is processed through a neuronal circuit that resembles the cerebellum. A second system through the deep layer carries primary auditory nerve input, some of which is relayed through interneurons. The present study reveals the morphology of individual interneurons and their local axonal arbors and how these inhibitory interneurons respond to sound. Vertical cells lie beneath the fusiform cell layer. Their dendritic and axonal arbors are limited to an isofrequency lamina. They give rise to pericellular nests around the base of fusiform cells and their proximal basal dendrites. These cells exhibit an onset-graded response to short tones and have response features defined as type II. They have tuning curves that are closed contours (0 shaped), thresholds ∼27 dB SPL, spontaneous firing rates of ∼0 spikes/s, and they respond weakly or not at all to broadband noise, as described for type II units. Their responses are nonmonotonic functions of intensity with peak responses between 30 and 60 dB SPL. They also show a preference for the high-to-low direction of a frequency sweep. It has been suggested that these circuits may be involved in the processing of spectral cues for the localization of sound sources.

R446 – Rostral Cochlear Nucleus Changes After Cochlear Ablation

2008 ◽  
Vol 139 (2_suppl) ◽  
pp. P194-P194 ◽  
Author(s):  
Kyle Robinson ◽  
Donald A Godfrey ◽  
Matthew A. Godfrey
Keyword(s):  
Auditory Processing ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
High Performance ◽  
Nerve Fibers ◽  
Average Concentration ◽  
Gamma Aminobutyric Acid ◽  
Freeze Dried ◽  
Concentration Changes ◽  
Temporal Bones

Problem Identification of neurotransmitter concentration changes occurring in the rostral anterior ventral cochlear nucleus (AVCN) following transection of the auditory nerve within the cochlea. Methods Chinchillas with cochlear ablations, as well as sham-lesioned chinchillas, were euthanized at times ranging from 3 to 84 days post ablation. Both temporal bones and brains were saved. Temporal bones were fixed, embedded in paraffin and sectioned to document the completeness of the cochlear lesion. Brain portions containing the cochlear nuclei were frozen-sectioned, and sections were freeze dried. Freeze-dried sections were microdissected into samples of AVCN for high performance liquid chromatography (HPLC) assay of 12 amino acid concentrations. Results The average concentration of glutamate, the most likely neurotransmitter of auditory nerve fibers, declined in the lesioned-side rostral AVCN by about 25% at 15 days. This decrease was maintained through 31 days post ablation and became bilateral at 83 days. There was no decrease in the adjacent granular region. Larger lesioned-side decreases, approaching 50%, were found more caudally in the AVCN at 31 days post ablation. The average concentration of the inhibitory neurotransmitter gamma-aminobutyric acid (GABA) decreased bilaterally by 15–25% at 3 through 15 days post ablation. Conclusion The degeneration of the central portion of the auditory nerve following mechanical ablation of the cochlea is accompanied by decreases of glutamate concentration on the lesioned side but bilateral decreases of GABA in the rostral part of the AVCN. These decreases were smaller than those reported previously for the posteroventral cochlear nucleus (PVCN). However, changes more caudally in AVCN approach those found in PVCN. Significance Our results are consistent with other evidence that damage to the cochlea leads to neurotransmitter changes in the central auditory system. The smaller changes in AVCN than in PVCN may correlate with different types of auditory processing in these two regions. Support The American Tinnitus Association and the University of Toledo Foundation.

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)

Frequency extent of two-tone facilitation in onset units in the ventral cochlear nucleus

1996 ◽  
Vol 75 (1) ◽  
pp. 380-395 ◽  
Author(s):  
D. Jiang ◽  
A. R. Palmer ◽  
I. M. Winter
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Low Frequency ◽  
Nerve Fibers ◽  
Inhibitory Input ◽  
Ventral Cochlear Nucleus ◽  
Narrow Region ◽  
Morphological Studies ◽  
Wide Range ◽  
Auditory Nerve Fibers

1. The frequency threshold curves (FTCs) of 91 single units in the cochlear nucleus of the anesthetized guinea pig were measured using a conventional single-tone paradigm and a two-tone paradigm designed to elucidate the frequency extent of two-tone facilitation in onset units (On). Units were classified according to existing classification schemes into primary-like (n = 3), chopper (n = 23), and three onset groups: OnI (n = 12), OnC (n = 29), and OnL (n = 24). Histological reconstructions show onset units to be widely distributed within the ventral cochlear nucleus in a manner generally consistent with its tonotopic organization. 2. The FTCs of onset units differed in their minimum thresholds, the steepness of their high- and low-frequency cutoffs, and their sharpness of tuning as quantified by the quality factor at 10 dB (Q10dB) above best frequency (BF) threshold values. There was considerable overlap in the sharpness of tuning between onset units and auditory nerve fibers, as indicated by the distribution of Q10dB values in the octave around 10 kHz: onset units had Q10dB values of 3.56 +/- 1.38 (SD), compared with 6.3 +/- 2.48 for auditory nerve fibers. The tuning of chopper units was similar to that of auditory nerve fibers (5.52 +/- 1.46). 3. Seventy-five percent of onset units showed some degree of facilitation (a threshold reduction) when their FTCs were measured in the presence of BF tones 4 dB below BF threshold. The frequency extent of such facilitation was variable, with a maximum of 6 octaves around the BF. In extreme cases facilitation could be measured when the BF tone was as low as 30 dB below BF threshold. 4. In 17% of onset units, suppressive effects were evident, as shown by noncontiguous frequency regions of facilitation. These suppressive effects might be a reflection either of suppression in the auditory nerve input or of a direct inhibitory input to the onset units. The strength of this effect suggests that inhibition is a likely explanation, consistent with the finding in previous morphological studies of profuse synapses with pleomorphic vesicles on multipolar cells. 5. FTCs of chopper and primary-like units measured in the presence of BF tones showed little facilitation. The facilitation that was observed in chopper units was confined to a narrow region around BF and disappeared when the facilitatory tone was lowered to 4 dB below BF threshold. 6. These data support the hypothesis that onset units, but not chopper or primary-like units, receive excitatory inputs from auditory nerve fibers with a wide range of BFs. However, the frequency range of facilitation and the magnitude of the threshold facilitation varied from unit to unit, suggesting that the off-BF inputs from auditory nerve fibers are not evenly distributed or equally effective in all units.

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