Mechanisms of Onset Responses in Octopus Cells of the Cochlear Nucleus: Implications of a Model

1997 ◽  
Vol 78 (2) ◽  
pp. 872-883 ◽  
Author(s):  
Yidao Cai ◽  
Edward J. Walsh ◽  
JoAnn McGee

Cai, Yidao, Edward J. Walsh, and JoAnn McGee. Mechanisms of onset responses in octopus cells of the cochlear nucleus: implications of a model. J. Neurophysiol. 78: 872–883, 1997. The octopus cells of the posteroventral cochlear nucleus receive inputs from auditory-nerve fibers and form one of the major ascending auditory pathways. They respond to acoustic and electrical stimulation transiently and are believed to carry temporal information in the precise timing of their action potentials. The mechanism whereby onset responses are generated is not clear. Proposals aimed at elucidating the mechanism range from neural circuitry and/or inhibition, “depolarization block” (or inactivation of Na+ channels), and the involvement of a 4-aminopyridine (4-AP)–sensitive, low-threshold channel (KLT). In the present study, we used a compartment model to investigate possible mechanisms. The model cell contains a soma, an axon, and four passive dendrites. Four kinds of ionic channels were included in the soma compartment: the Hodgkin-Huxley–like Na+ and K+ channels, a 4-AP–sensitive, low-threshold channel, KLT, and a Cs+-sensitive, hyperpolarization-activated inward rectifier, I h . DC currents and half-wave–rectified sinewaves were used as stimuli. Our results showed that an onset response can be generated in the absence of neuronal circuitry of any form, thus suggesting that the onset response in octopus cells is regulated intrinsically. Among the many factors involved, low-input impedance, partly contributed by I h , appears to be essential to the basic onset response pattern; also, the KLT conductance plays a major role, whereas the inactivation of Na+ channels probably plays only a secondary role. The dynamics of I h also can modify the response pattern, but due to its slow kinetics, its role is probably limited to longer-term regulation under the conditions simulated in this study.

1986 ◽  
Vol 56 (2) ◽  
pp. 287-307 ◽  
Author(s):  
W. S. Rhode ◽  
P. H. Smith

Results reported here support the conclusion that an individual neuron in the dorsal cochlear nucleus (DCN) can exhibit pauser, buildup, and chopper patterns in response to tone pips. Fusiform cells have been previously identified as the principal cell exhibiting these patterns. Fusiform cells can also exhibit an onset response followed by suppression of spontaneous activity at their characteristic frequency (CF). Off CF only suppression is seen. These neurons are characterized by a restricted excitatory region near threshold. All these cells can exhibit nonmonotonic rate curves, narrow excitatory regions, and inhibitory sidebands. Nonmonotonicity occurred in 34% of pausers, 52% of buildup, 89% of onsets with a graded response, and 50% overall in the DCN cells. Chopper units occur as often as the other types combined in the DCN. Only 14% show nonmonotonic rate curves. Those with high-spontaneous activity also show inhibitory sidebands. Cells with a predominant buildup pattern occur most frequently in the fusiform cell layer, whereas pausers occur throughout the DCN below the molecular layer. Intracellular potentials often reflect the average response pattern. Sharply delimited response areas indicate that these cells may be useful for performing a spectral analysis. These cells show almost no phase locking suggesting that temporal encoding is an unlikely function. It is suggested that the effects of anesthetic on the function of the DCN is not as marked as previously indicated.


2001 ◽  
Vol 86 (5) ◽  
pp. 2299-2311 ◽  
Author(s):  
Ramazan Bal ◽  
Donata Oertel

Octopus cells in the posteroventral cochlear nucleus (PVCN) of mammals are biophysically specialized to detect coincident firing in the population of auditory nerve fibers that provide their synaptic input and to convey its occurrence with temporal precision. The precision in the timing of action potentials depends on the low input resistance (∼6 MΩ) of octopus cells at the resting potential that makes voltage changes rapid (τ ∼ 200 μs). It is the activation of voltage-dependent conductances that endows octopus cells with low input resistances and prevents repetitive firing in response to depolarization. These conductances have been examined under whole cell voltage clamp. The present study reveals the properties of two conductances that mediate currents whose reversal at or near the equilibrium potential for K+ over a wide range of extracellular K+ concentrations identifies them as K+ currents. One rapidly inactivating conductance, g KL, had a threshold of activation at −70 mV, rose steeply as a function of depolarization with half-maximal activation at −45 ± 6 mV (mean ± SD), and was fully activated at 0 mV. The low-threshold K+ current ( I KL) was largely blocked by α-dendrotoxin (α-DTX) and partially blocked by DTX-K and tityustoxin, indicating that this current was mediated through potassium channels of the Kv1 (also known as shakeror KCNA) family. The maximum low-threshold K+conductance ( g KL) was large, 514 ± 135 nS. Blocking I KL with α-DTX revealed a second K+ current with a higher threshold ( I KH) that was largely blocked by 20 mM tetraethylammonium (TEA). The more slowly inactivating conductance, g KH, had a threshold for activation at −40 mV, reached half-maximal activation at −16 ± 5 mV, and was fully activated at +30 mV. The maximum high-threshold conductance, g KH, was on average 116 ± 27 nS. The present experiments show that it is not the biophysical and pharmacological properties but the magnitude of the K+ conductances that make octopus cells unusual. At the resting potential, −62 mV, g KLcontributes ∼42 nS to the resting conductance and mediates a resting K+ current of 1 nA. The resting outward K+ current is balanced by an inward current through the hyperpolarization-activated conductance, g h, that has been described previously.


1975 ◽  
Vol 38 (2) ◽  
pp. 418-429 ◽  
Author(s):  
L. M. Aitkin ◽  
J. Boyd

The responses of 146 cerebellar neurons to tone stimuli were studied in 29 cats anesthetized with chloralose-urethan and in 7 decerebrate preparations. Units were classified as onset or sustained firing. Onset spikes occurred on stimulation of either ear and showed binaural facilitation, while sustained discharges were frequently only excited by monaural stimulation. The latent periods of sustained discharges appeared to be shorter than those of onset responses, and sustained discharges were also more sharply tuned than the onset units. Evidence was presented suggesting that onset responses reflected input from the inferior colliculus and sustained responses, the cochlear nucleus. The sterotyped facilitatory behavior of onset units suggested that a maximal discharge might occur if sounds were of equal intensity at each ear; 26 neurons were examined with variable interaural time or intensity differences and 10 of these exhibited maximal firing when the interaural time and intensity difference was zero--i.e., if the sound was located directly in front of the head.


1986 ◽  
Vol 56 (2) ◽  
pp. 261-286 ◽  
Author(s):  
W. S. Rhode ◽  
P. H. Smith

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)


1997 ◽  
Vol 77 (1) ◽  
pp. 364-377 ◽  
Author(s):  
Christine Köppl

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.


2003 ◽  
Vol 89 (6) ◽  
pp. 3070-3082 ◽  
Author(s):  
Jason S. Rothman ◽  
Paul B. Manis

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.


2020 ◽  
Vol 21 (17) ◽  
pp. 6221 ◽  
Author(s):  
Ramón Cobo ◽  
Jorge García-Piqueras ◽  
Yolanda García-Mesa ◽  
Jorge Feito ◽  
Olivia García-Suárez ◽  
...  

The vertebrate skin contains sensory corpuscles that are receptors for different qualities of mechanosensitivity like light brush, touch, pressure, stretch or vibration. These specialized sensory organs are linked anatomically and functionally to mechanosensory neurons, which function as low-threshold mechanoreceptors connected to peripheral skin through Aβ nerve fibers. Furthermore, low-threshold mechanoreceptors associated with Aδ and C nerve fibers have been identified in hairy skin. The process of mechanotransduction requires the conversion of a mechanical stimulus into electrical signals (action potentials) through the activation of mechanosensible ion channels present both in the axon and the periaxonal cells of sensory corpuscles (i.e., Schwann-, endoneurial- and perineurial-related cells). Most of those putative ion channels belong to the degenerin/epithelial sodium channel (especially the family of acid-sensing ion channels), the transient receptor potential channel superfamilies, and the Piezo family. This review updates the current data about the occurrence and distribution of putative mechanosensitive ion channels in cutaneous mechanoreceptors including primary sensory neurons and sensory corpuscles.


2009 ◽  
Vol 102 (5) ◽  
pp. 2627-2637 ◽  
Author(s):  
Lioudmila Pliss ◽  
Hua Yang ◽  
Matthew A. Xu-Friedman

Many synapses contain both AMPA receptors (AMPAR) and N-methyl-d-aspartate receptors (NMDAR), but their different roles in synaptic computation are not clear. We address this issue at the auditory nerve fiber synapse (called the endbulb of Held), which is formed on bushy cells of the cochlear nucleus. The endbulb refines and relays precise temporal information to nuclei responsible for sound localization. The endbulb has a number of specializations that aid precise timing, including AMPAR-mediated excitatory postsynaptic currents (EPSCs) with fast kinetics. Voltage-clamp experiments in mouse brain slices revealed that slow NMDAR EPSCs are maintained at mature endbulbs, contributing a peak conductance of around 10% of the AMPAR-mediated EPSC. During repetitive synaptic activity, AMPAR EPSCs depressed and NMDAR EPSCs summated, thereby increasing the relative importance of NMDARs. This could impact temporal precision of bushy cells because of the slow kinetics of NMDARs. We tested this by blocking NMDARs and quantifying bushy cell spike timing in current clamp when single endbulbs were activated. These experiments showed that NMDARs contribute to an increased probability of firing, shorter latency, and reduced jitter. Dynamic-clamp experiments confirmed this effect and showed it was dose-dependent. Bushy cells can receive inputs from multiple endbulbs. When we applied multiple synaptic inputs in dynamic clamp, NMDARs had less impact on spike timing. NMDAR conductances much higher than mature levels could disrupt spiking, which may explain its downregulation during development. Thus mature NMDAR expression can support the conveying of precise temporal information at the endbulb, depending on the stimulus conditions.


1976 ◽  
Vol 39 (1) ◽  
pp. 179-194 ◽  
Author(s):  
R. Britt ◽  
A. Starr

Responses of 99 cochlear nucleus cells and 24 cochlear nerve fibers were studied with FM signals; 14 cochlear nerve fibers and 57 cochlear nucleus cells were studied at four rates of modulation and several signal intensities. Classification of FM response patterns as symmetrical, asymmetrical, or unidirectional was based on the calculation of a symmetry factor (S), which compared the number of discharges evoked by the ascending and by the descending phases of the FM sweep. Certain FM response patterns could not adequately be described by the symmetry factor along and variables of modulation rate and signal intensity had significant influence. A correspondence was found between the four response classes evoked by a steady-frequency tone burst (primarylike, buildup, onset, and pause) and the FM response pattern. Cochlear nerve fibers showed symmetrical response patterns to FM stimulation. Primarylike units were similar to eighth nerve fibers and generally showed symmetrical FM responses. Occasional eighth nerve fibers and primarylike cells developed asymmetry at the fastest rate of modulation (50 sps). Buildup units showed a variety of response patterns to FM signals. Onset units generally showed asymmetrical response patterns with the greater response occurring to the ascending than to the descending phase of the FM sweep. Pause units showed a characteristic inhibition of activity at 5 sps (rate-dependent inhibition). Of the 57 cochlear nuclear cells studied in response to FM signals, 16 were symmetrical, another 16 were symmetrical except at the fastest modulation rate, 12 were asymmetrical, 3 were unidirectional, and 10 showed complex responses to certain signal rates or intensities. It is clear the the cat cochlear with its complex cytoarchitecture is involved in the recoding of acoustic information. Some units in cochlear nucleus demonstrate differential responses to the direction and to the rate of frequency movement. Other cochlear nucleus cells respond as eighth nerve fibers and may serve as simple "relays" in transmitting information from the cochlea to higher auditory centers.


Sign in / Sign up

Export Citation Format

Share Document