scholarly journals Computational Diversity in the Cochlear Nucleus Angularis of the Barn Owl

2003 ◽  
Vol 89 (4) ◽  
pp. 2313-2329 ◽  
Author(s):  
Christine Köppl ◽  
Catherine E. Carr
Keyword(s):  
Brain Stem ◽  
Cochlear Nucleus ◽  
Phase Locking ◽  
Sound Intensity ◽  
Nerve Fibers ◽  
Tuning Curves ◽  
Starting Point ◽  
Barn Owls ◽  
Different Response ◽  
Nucleus Angularis

The cochlear nucleus angularis (NA) is widely assumed to form the starting point of a brain stem pathway for processing sound intensity in birds. Details of its function are unclear, however, and its evolutionary origin and relationship to the mammalian cochlear-nucleus complex are obscure. We have carried out extracellular single-unit recordings in the NA of ketamine-anesthetized barn owls. The aim was to re-evaluate the extent of heterogeneity in NA physiology because recent studies of cellular morphology had established several distinct types. Extensive characterization, using tuning curves, phase locking, peristimulus time histograms and rate-level functions for pure tones and noise, revealed five major response types. The most common one was a primary-like pattern that was distinguished from auditory-nerve fibers by showing lower vector strengths of phase locking and/or lower spontaneous rates. Two types of chopper responses were found (chopper-transient and a rare chopper-sustained), as well as onset units. Finally, we routinely encountered a complex response type with a pronounced inhibitory component, similar to the mammalian typeIV. Evidence is presented that this range of response types is representative for birds and that earlier conflicting reports may be due to methodological differences. All five response types defined were similar to well-known types in the mammalian cochlear nucleus. This suggests convergent evolution of neurons specialized for encoding different behaviorally relevant features of the auditory stimulus. It remains to be investigated whether the different response types correlate with morphological types and whether they establish different processing streams in the auditory brain stem of birds.

Response Properties of Single Auditory Nerve Fibers in the Mouse

2005 ◽  
Vol 93 (1) ◽  
pp. 557-569 ◽  
Author(s):  
Annette M. Taberner ◽  
M. Charles Liberman
Keyword(s):  
Auditory Nerve ◽  
Dynamic Range ◽  
Phase Locking ◽  
Nerve Fibers ◽  
Cochlear Function ◽  
Response Properties ◽  
Tuning Curves ◽  
Rate Versus ◽  
Interstrain Difference ◽  
Mutant Lines

The availability of transgenic and mutant lines makes the mouse a valuable model for study of the inner ear, and a powerful window into cochlear function can be obtained by recordings from single auditory nerve (AN) fibers. This study provides the first systematic description of spontaneous and sound-evoked discharge properties of AN fibers in mouse, specifically in CBA/CaJ and C57BL/6 strains, both commonly used in auditory research. Response properties of 196 AN fibers from CBA/CaJ and 58 from C57BL/6 were analyzed, including spontaneous rates (SR), tuning curves, rate versus level functions, dynamic range, response adaptation, phase-locking, and the relation between SR and these response properties. The only significant interstrain difference was the elevation of high-frequency thresholds in C57BL/6. In general, mouse AN fibers showed similar responses to other mammals: sharpness of tuning increased with characteristic frequency, which ranged from 2.5 to 70 kHz; SRs ranged from 0 to 120 sp/s, and fibers with low SR (<1 sp/s) had higher thresholds, and wider dynamic ranges than fibers with high SR. Dynamic ranges for mouse high-SR fibers were smaller (<20 dB) than those seen in other mammals. Phase-locking was seen for tone frequencies <4 kHz. Maximum synchronization indices were lower than those in cat but similar to those found in guinea pig.

scholarly journals Spike threshold adaptation diversifies neuronal operating modes in the auditory brain stem

2019 ◽  
Vol 122 (6) ◽  
pp. 2576-2590
Author(s):  
Susan T. Lubejko ◽  
Bertrand Fontaine ◽  
Sara E. Soueidan ◽  
Katrina M. MacLeod
Keyword(s):  
Sodium Channel ◽  
Brain Stem ◽  
Cochlear Nucleus ◽  
Fine Tuning ◽  
Threshold Dynamics ◽  
Spike Threshold ◽  
Operating Modes ◽  
Auditory Brain Stem ◽  
Spike Initiation ◽  
Nucleus Angularis

Single neurons function along a spectrum of neuronal operating modes whose properties determine how the output firing activity is generated from synaptic input. The auditory brain stem contains a diversity of neurons, from pure coincidence detectors to pure integrators and those with intermediate properties. We investigated how intrinsic spike initiation mechanisms regulate neuronal operating mode in the avian cochlear nucleus. Although the neurons in one division of the avian cochlear nucleus, nucleus magnocellularis, have been studied in depth, the spike threshold dynamics of the tonically firing neurons of a second division of cochlear nucleus, nucleus angularis (NA), remained unexplained. The input-output functions of tonically firing NA neurons were interrogated with directly injected in vivo-like current stimuli during whole cell patch-clamp recordings in vitro. Increasing the amplitude of the noise fluctuations in the current stimulus enhanced the firing rates in one subset of tonically firing neurons (“differentiators”) but not another (“integrators”). We found that spike thresholds showed significantly greater adaptation and variability in the differentiator neurons. A leaky integrate-and-fire neuronal model with an adaptive spike initiation process derived from sodium channel dynamics was fit to the firing responses and could recapitulate >80% of the precise temporal firing across a range of fluctuation and mean current levels. Greater threshold adaptation explained the frequency-current curve changes due to a hyperpolarized shift in the effective adaptation voltage range and longer-lasting threshold adaptation in differentiators. The fine-tuning of the intrinsic properties of different NA neurons suggests they may have specialized roles in spectrotemporal processing. NEW & NOTEWORTHY Avian cochlear nucleus angularis (NA) neurons are responsible for encoding sound intensity for sound localization and spectrotemporal processing. An adaptive spike threshold mechanism fine-tunes a subset of repetitive-spiking neurons in NA to confer coincidence detector-like properties. A model based on sodium channel inactivation properties reproduced the activity via a hyperpolarized shift in adaptation conferring fluctuation sensitivity.

Signs of functional maturation of peripheral auditory system in discharge patterns of neurons in anteroventral cochlear nucleus of kitten

1978 ◽  
Vol 41 (6) ◽  
pp. 1557-1559 ◽  
Author(s):  
J. F. Brugge ◽  
E. Javel ◽  
L. M. Kitzes
Keyword(s):  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Discharge Rate ◽  
Phase Locking ◽  
Low Frequency ◽  
Second Phase ◽  
Extended Phase ◽  
Anteroventral Cochlear Nucleus ◽  
Peripheral Auditory System ◽  
Different Response

1. Responses to pure tones were recorded from single neurons in the anteroventral cochlear nucleus (AVCN) in kittens ranging in age from 4 to 45 days. Different response properties mature at different times after birth. 2. The shapes of response areas of AVCN neurons after the 1st postnatal week resemble those recorded in the AVCN and auditory nerve of the adult. During the 1st wk after birth the high-frequency portion of the response area is extended. Phase-locked responses to stimulus frequencies below about 600 Hz occur at this time. Phase vs. frequency measurements and shapes of response areas indicate that by the end of the 1st postnatal week the cochlear partition may be capable of supporting a traveling wave along most of its length. 3. Functional development proceeds through a second phase which lasts until the end of the 2nd or the beginning of the 3rd wk of life. During that time threshold, maximal discharge rate, and average first-spike latency achieve adult values. 4. Phase-locking to low-frequency tones, to the extent displayed by phase-sensitive neurons in the adult AVCN or auditory nerve, is achieved last, after the 3rd or 4th wk postpartum.

scholarly journals Presynaptic GABAergic receptors modulate inhibitory synaptic feedback in the avian cochlear nucleus angularis

2019 ◽  
Author(s):  
Stefanie L. Eisenbach ◽  
Sara E. Soueidan ◽  
Katrina M. MacLeod
Keyword(s):  
Brain Stem ◽  
Cochlear Nucleus ◽  
Gain Control ◽  
Short Term ◽  
Cochlear Nuclei ◽  
Inhibitory Circuitry ◽  
Inhibitory Feedback ◽  
Control Feedback ◽  
Olivary Nucleus ◽  
Nucleus Angularis

AbstractInhibition plays multiple critical roles in the neural processing of sound. In the avian auditory brain stem, the cochlear nuclei receive their principal inhibitory feedback from the superior olivary nucleus (SON) in lieu of local inhibitory circuitry. In the timing pathway, GABAergic inhibitory feedback underlies gain control to enhance sound localization. In the cochlear nucleus angularis (NA), which processes intensity information, how the inhibitory feedback is integrated is not well understood. Using whole cell patch-clamp recordings in chick brain stem slices, we investigated the effects of GABA release on the inhibitory (presumed SON) and excitatory (8th nerve) synaptic inputs onto NA neurons. Pharmacological activation of the metabotropic GABAB receptors with baclofen profoundly suppressed both evoked excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs). Baclofen similarly reduced the frequency of spontaneous IPSCs and EPSCs, but had no significant effect on the current kinetics or amplitudes, indicating a presynaptic locus of modulation. Trains of IPSCs showed substantial transient and sustained short-term synaptic facilitation. Baclofen application reduced the initial IPSC amplitude, but enhanced the relative facilitation over the train via changes in release probability. Comparable levels of GABAB receptor mediated blockade also shifted short-term synaptic plasticity of EPSCs toward less depression. Evoked (but not spontaneous) release of GABA was sufficient to suppress basal release at inhibitory synapses in slices. Overall, the modulation of excitatory and inhibitory inputs of NA neurons via GABAB receptor activation appears to parallel that in the timing pathway.New and NoteworthyAvian cochlear nucleus angularis (NA) neurons are responsible for encoding sound intensity and provide level information for gain control feedback via the superior olivary nucleus. This GABAergic inhibitory feedback was itself modulated in NA via presynaptic, metabotropic GABAB receptor mediated suppression. Excitatory transmission was modulated by the same receptors, suggesting parallel homosynaptic and heterosynaptic mechanisms in both cochlear nuclei.

Synaptic Physiology in the Cochlear Nucleus Angularis of the Chick

2005 ◽  
Vol 93 (5) ◽  
pp. 2520-2529 ◽  
Author(s):  
Katrina M. MacLeod ◽  
Catherine E. Carr
Keyword(s):  
Brain Stem ◽  
Time Constant ◽  
Auditory Nerve ◽  
Sound Intensity ◽  
Sound Recognition ◽  
Auditory Information ◽  
Decay Kinetics ◽  
Cochlear Nuclei ◽  
Auditory Brain Stem ◽  
Nucleus Angularis

Nucleus angularis (NA), one of the two cochlear nuclei in birds, is important for processing sound intensity for localization and most likely has role in sound recognition and other auditory tasks. Because the synaptic properties of auditory nerve inputs to the cochlear nuclei are fundamental to the transformation of auditory information, we studied the properties of these synapses onto NA neurons using whole cell patch-clamp recordings from auditory brain stem slices from embryonic chickens (E16–E20). We measured spontaneous excitatory postsynaptic currents (EPSCs), and evoked EPSCs and excitatory postsynaptic potentials (EPSPs) by using extracellular stimulation of the auditory nerve. These excitatory EPSCs were mediated by AMPA and N-methyl-d-aspartate (NMDA) receptors. The spontaneous EPSCs mediated by AMPA receptors had submillisecond decay kinetics (556 μs at E19), comparable with those of other auditory brain stem areas. The spontaneous EPSCs increased in amplitude and became faster with developmental age. Evoked EPSC and EPSP amplitudes were graded with stimulus intensity. The average amplitude of the EPSC evoked by minimal stimulation was twice as large as the average spontaneous EPSC amplitude (∼110 vs. ∼55 pA), suggesting that single fibers make multiple contacts onto each postsynaptic NA neuron. Because of their small size, minimal EPSPs were subthreshold, and we estimate at least three to five inputs were required to reach threshold. In contrast to the fast EPSCs, EPSPs in NA had a decay time constant of ∼12.5 ms, which was heavily influenced by the membrane time constant. Thus NA neurons spatially and temporally integrate auditory information arriving from multiple auditory nerve afferents.

Encoding of amplitude modulation in the cochlear nucleus of the cat

1994 ◽  
Vol 71 (5) ◽  
pp. 1797-1825 ◽  
Author(s):  
W. S. Rhode ◽  
S. Greenberg
Keyword(s):  
Amplitude Modulation ◽  
Carrier Frequency ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Communication Systems ◽  
Phase Locking ◽  
Nerve Fibers ◽  
Phase Lock ◽  
Spontaneous Rate ◽  
Cochlear Nuclei

1. Amplitude modulation (AM) is a pervasive property of acoustic communication systems. In the present study we investigate neural temporal mechanisms in the auditory nerve and cochlear nuclei of the pentobarbital sodium-anesthesized cat associated with the neural coding of 100% AM tones, both in quiet and in the presence of wideband, quasi-flat-spectrum noise. The AM carrier frequency was set to the neuron's characteristic frequency (CF) and the sound pressure level (SPL) of acoustic stimuli was varied over a wide dynamic range of intensities (< or = 40 dB). The temporal AM-encoding capability of auditory neurons was measured by computing the synchronization coefficient (SC) of the neural response to the signal's modulation and carrier frequency. The temporal modulation transfer function (tMTF) of a neuron was then computed by measuring the SC of the response to signals of variable fmod (50-2550 Hz). 2. Neurons in the cochlear nuclei synchronize on average more highly to the modulation frequency than fibers of comparable CF, threshold, and spontaneous rate in the auditory nerve. The disparity in performance is greatest at high SPLs and low signal-to-noise ratios. However, there is a significant degree of diversity in AM-encoding capability among neurons in both the cochlear nuclei and auditory nerve. Among auditory nerve fibers (ANFs), low- and medium-spontaneous-rate (SR) units (SR < 18 spike/s) phase-lock with greater precision than comparable high-SR units at any given frequency, particularly at moderate to high SPLs, consistent with previous studies. 3. The phase-locking capabilities of neurons in the cochlear nucleus are considerably more variable than in the auditory nerve. Moreover, the variability itself depends on two distinct measures of phase-locking performance. Most ANFs are capable of phase-locking to frequencies as high as 3–4 kHz. In the cochlear nucleus many unit types do not phase-lock to modulation frequencies > 1 kHz. As a result, phase-locking performance is measured on the basis of two parameters, maximum synchronization, irrespective of stimulus frequency, and the upper frequency limit for significant phase-locking. 4. Cochlear nucleus neurons may be divided into three distinct groups on the basis of maximum synchronization capability. In group 1 are the primary-like (PL) units of the anteroventral division, whose phase-locking capabilities are comparable with those of high-SR ANFs.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Intrinsic firing properties in the avian auditory brain stem allow both integration and encoding of temporally modulated noisy inputs in vitro

2012 ◽  
Vol 108 (10) ◽  
pp. 2794-2809 ◽  
Author(s):  
Lauren J. Kreeger ◽  
Arslaan Arshed ◽  
Katrina M. MacLeod
Keyword(s):  
Firing Rate ◽  
Cochlear Nucleus ◽  
Phase Locking ◽  
Brain Slices ◽  
Sound Intensity ◽  
Current Fluctuations ◽  
Firing Rates ◽  
Whole Cell Patch Clamp ◽  
High Degree

The intrinsic properties of tonically firing neurons in the cochlear nucleus contribute to representing average sound intensity by favoring synaptic integration across auditory nerve inputs, reducing phase locking to fine temporal acoustic structure and enhancing envelope locking. To determine whether tonically firing neurons of the avian cochlear nucleus angularis (NA) resemble ideal integrators, we investigated their firing responses to noisy current injections during whole cell patch-clamp recordings in brain slices. One subclass of neurons (36% of tonically firing neurons, mainly subtype tonic III) showed no significant changes in firing rate with noise fluctuations, acting like pure integrators. In contrast, many tonically firing neurons (>60%, mainly subtype tonic I or II) showed a robust sensitivity to noisy current fluctuations, increasing their firing rates with increased fluctuation amplitudes. For noise-sensitive tonic neurons, the firing rate vs. average current curves with noise had larger maximal firing rates, lower gains, and wider dynamic ranges compared with FI curves for current steps without noise. All NA neurons showed fluctuation-driven patterning of spikes with a high degree of temporal reliability and millisecond spike time precision. Single-spiking neurons in NA also responded to noisy currents with higher firing rates and reliable spike trains, although less precisely than nucleus magnocellularis neurons. Thus some NA neurons function as integrators by encoding average input levels over wide dynamic ranges regardless of current fluctuations, others detect the degree of coherence in the inputs, and most encode the temporal patterns contained in their inputs with a high degree of precision.

Temporal Properties of Responses to Broadband Noise in the Auditory Nerve

2004 ◽  
Vol 91 (5) ◽  
pp. 2051-2065 ◽  
Author(s):  
Dries H. G. Louage ◽  
Marcel van der Heijden ◽  
Philip X. Joris
Keyword(s):  
Fourier Analysis ◽  
Auditory Nerve ◽  
Phase Locking ◽  
Strong Dependence ◽  
Peak Height ◽  
Nerve Fibers ◽  
Broadband Noise ◽  
Temporal Information ◽  
Temporal Behavior ◽  
Locking Range

Temporal information in the responses of auditory neurons to sustained sounds has been studied mostly with periodic stimuli, using measures that are based on Fourier analysis. Less information is available on temporal aspects of responses to nonperiodic wideband sounds. We recorded responses to a reference Gaussian noise and its polarity-inverted version in the auditory nerve of barbiturate-anesthetized cats and used shuffled autocorrelograms (SACs) to quantify spike timing. Two metrics were extracted from the central peak of autocorrelograms: the peak-height and the width at halfheight. Temporal information related to stimulus fine-structure was isolated from that to envelope by subtracting or adding responses to the reference and inverted noise. Peak-height and halfwidth generally behaved as expected from the existing body of data on phase-locking to pure tones and sinusoidally amplitude-modulated tones but showed some surprises as well. Compared with synchronization to low-frequency tones, SACs reveal large differences in temporal behavior between the different classes of nerve fibers (based on spontaneous rate) as well as a strong dependence on characteristic frequency (CF) throughout the phase-locking range. SACs also reveal a larger temporal consistency (i.e., tendency to discharge at the same point in time on repeated presentation of the same stimulus) in the responses to the stochastic noise stimulus than in the responses to periodic tones. Responses at high CFs reflect envelope phase-locking and are consistent with previous reports using sinusoidal AM. We conclude that the combined use of broadband noise and SAC analysis allow a more general characterization of temporal behavior than periodic stimuli and Fourier analysis.

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)

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