Effects of Inhibitory Feedback in a Network Model of Avian Brain Stem

2005 ◽  
Vol 94 (1) ◽  
pp. 400-414 ◽  
Author(s):  
Vasant K. Dasika ◽  
John A. White ◽  
Laurel H. Carney ◽  
H. Steven Colburn
Keyword(s):  
Brain Stem ◽  
Network Model ◽  
Auditory Nerve ◽  
Feedback Inhibition ◽  
Interaural Time Difference ◽  
Nerve Fibers ◽  
Sound Level ◽  
Inhibitory Input ◽  
Auditory Brain Stem ◽  
Inhibitory Feedback

The avian auditory brain stem consists of a network of specialized nuclei, including nucleus laminaris (NL) and superior olivary nucleus (SON). NL cells show sensitivity to interaural time difference (ITD), a critical cue that underlies spatial hearing. SON cells provide inhibitory feedback to the rest of the network. Empirical data suggest that feedback inhibition from SON could increase the ITD sensitivity of NL across sound level. Using a bilateral network model, we assess the effects of SON feedback inhibition. Individual cells are specified as modified leaky-integrate-and-fire neurons with time constants and thresholds that vary with inhibitory input. Acoustic sound level is reflected in the discharge rates of the model auditory-nerve fibers, which innervate the network. Simulations show that with SON inhibitory feedback, ITD sensitivity is maintained in model NL cells over a threefold range in auditory-nerve discharge rate. In contrast, without SON feedback inhibition, ITD sensitivity is significantly reduced as input rates are increased. Feedback inhibition is most beneficial in maintaining ITD sensitivity at high-input rates (simulating high sound levels). With SON inhibition, ITD sensitivity is maintained for both interaurally balanced inputs (simulating an on-center sound source) and interaurally imbalanced inputs (simulating a lateralized source). Further, the empirically observed temporal build-up of SON inhibition and the presence of reciprocal inhibitory connections between the ipsi- and contralateral SON both improve ITD sensitivity. In sum, our network model shows that inhibitory feedback can substantially increase the sensitivity and dynamic range of ITD coding in the avian auditory brain stem.

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.

Effect of High Electrical Stimulus Intensities on the Auditory Nerve Using Brain Stem Response Audiometry

1987 ◽  
Vol 96 (1_suppl) ◽  
pp. 50-53 ◽  
Author(s):  
R. K. Shepherd ◽  
G. M. Clark
Keyword(s):  
Brain Stem ◽  
Speech Processing ◽  
Auditory Nerve ◽  
Electrical Stimulus ◽  
Metabolic Effects ◽  
Charge Densities ◽  
Processing Strategies ◽  
Auditory Brain Stem ◽  
High Charge Density ◽  
High Stimulus

The response of the auditory nerve to acute intracochlear electrical stimulation using charge-balanced biphasic current pulses was monitored using electrically evoked auditory brain stem responses (EABRs). Stimulation at moderate charge densities (64 μC cm−2 geom/phase; 0.8 mA, 200 μs/phase) for periods of up to 12 hours produced only minimal short-term changes in the EABR. Stimulation at a high charge density (144 μC cm−2 geom/phase; 1.8 mA, 200 μs/phase) resulted in permanent reductions in the EABR for high stimulus rates (> 200 pulses per second [pps]) or long stimulus durations (12 hours). At lower stimulus rates and durations, recovery to prestimulus levels was slow but complete. The mechanisms underlying these temporary and permanent reductions in the EABR are probably caused by neural adaptation and more long-term metabolic effects. These findings have implications for the design of speech-processing strategies using high stimulus rates.

scholarly journals Target-specific regulation of presynaptic release properties at auditory nerve terminals in the avian cochlear nucleus

2016 ◽  
Vol 115 (3) ◽  
pp. 1679-1690 ◽  
Author(s):  
J. Ahn ◽  
K. M. MacLeod
Keyword(s):  
Brain Stem ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Auditory Information ◽  
Nerve Terminals ◽  
Release Probability ◽  
Auditory Brain Stem ◽  
Presynaptic Release ◽  
Specific Regulation ◽  
Synaptic Dynamics

Short-term synaptic plasticity (STP) acts as a time- and firing rate-dependent filter that mediates the transmission of information across synapses. In the auditory brain stem, the divergent pathways that encode acoustic timing and intensity information express differential STP. To investigate what factors determine the plasticity expressed at different terminals, we tested whether presynaptic release probability differed in the auditory nerve projections to the two divisions of the avian cochlear nucleus, nucleus angularis (NA) and nucleus magnocellularis (NM). Estimates of release probability were made with an open-channel blocker of N-methyl-d-aspartate (NMDA) receptors. Activity-dependent blockade of NMDA receptor-mediated excitatory postsynaptic currents (EPSCs) with application of 20 μM (+)-MK801 maleate was more rapid in NM than in NA, indicating that release probability was significantly higher at terminals in NM. Paired-pulse ratio (PPR) was tightly correlated with the blockade rate at terminals in NA, suggesting that PPR was a reasonable proxy for relative release probability at these synapses. To test whether release probability was similar across convergent inputs onto NA neurons, PPRs of different nerve inputs onto the same postsynaptic NA target neuron were measured. The PPRs, as well as the plasticity during short trains, were tightly correlated across multiple inputs, further suggesting that release probability is coordinated at auditory nerve terminals in a target-specific manner. This highly specific regulation of STP in the auditory brain stem provides evidence that the synaptic dynamics are tuned to differentially transmit the auditory information in nerve activity into parallel ascending pathways.

scholarly journals Expression and Neurotransmitter Association of the Synaptic Calcium Sensor Synaptotagmin in the Avian Auditory Brain Stem

2021 ◽  
Author(s):  
Katrina M. MacLeod ◽  
Sangeeta Pandya
Keyword(s):  
Brain Stem ◽  
Cochlear Nucleus ◽  
Auditory Nerve ◽  
Calcium Binding ◽  
Glutamate Transporter ◽  
Calcium Sensor ◽  
Double Labeling ◽  
Excitatory Transmission ◽  
Auditory Brain Stem ◽  
Synaptotagmin 1

AbstractIn the avian auditory brain stem, acoustic timing and intensity cues are processed in separate, parallel pathways via the two division of the cochlear nucleus, nucleus angularis (NA) and nucleus magnocellularis (NM). Differences in excitatory and inhibitory synaptic properties, such as release probability and short-term plasticity, contribute to differential processing of the auditory nerve inputs. We investigated the distribution of synaptotagmin, a putative calcium sensor for exocytosis, via immunohistochemistry and double immunofluorescence in the embryonic and hatchling chick brain stem (Gallus gallus). We found that the two major isoforms, synaptotagmin 1 (Syt1) and synaptotagmin 2 (Syt2), showed differential expression. In the NM, anti-Syt2 label was strong and resembled the endbulb terminals of the auditory nerve inputs, while anti-Syt1 label was weaker and more punctate. In NA, both isoforms were intensely expressed throughout the neuropil. A third isoform, synaptotagmin 7 (Syt7), was largely absent from the cochlear nuclei. In nucleus laminaris (NL, the target nucleus of NM), anti-Syt2 and anti-Syt7 strongly labeled the dendritic lamina. These patterns were established by embryonic day 18 and persisted to postnatal day 7. Double labeling immunofluorescence showed Syt1 and Syt2 were associated with Vesicular Glutamate Transporter 2 (VGluT2), but not Vesicular GABA Transporter (VGAT), suggesting these Syt isoforms were localized to excitatory, but not inhibitory, terminals. These results suggest that Syt2 is the major calcium binding protein underlying excitatory neurotransmission in the timing pathway comprising NM and NL, while Syt2 and Syt1 regulate excitatory transmission in the parallel intensity pathway via cochlear nucleus NA.

Electrical Stimulation of the Auditory Nerve in Cats

1979 ◽  
Vol 88 (4) ◽  
pp. 533-539 ◽  
Author(s):  
F. Blair Simmons
Keyword(s):  
Electrical Stimulation ◽  
Light Microscopy ◽  
Brain Stem ◽  
Auditory Nerve ◽  
Nerve Fibers ◽  
Long Term Effects ◽  
Stimulation Of

Each of five cats (one congenitally deaf) had Pt-Ir electrodes placed in the modiolus. Some electrodes were stimulated with a 100 μamp, 0.25 msec balanced biphasic 50/sec pulse for 2 hours for a total of 20 to 40 hours each over periods of several months. Pre- and poststimulation measures of click-evoked N1 responses, averaged brain stem potentials, and impedances showed no long-term effects of damage to the nerves. Light microscopy showed very acceptable tissue tolerance and no evidence of damage caused by electrical stimulation. The deaf cat had about 10% residual nerve fibers which responded to stimulation.

scholarly journals Response Growth With Sound Level in Auditory-Nerve Fibers After Noise-Induced Hearing Loss

2004 ◽  
Vol 91 (2) ◽  
pp. 784-795 ◽  
Author(s):  
Michael G. Heinz ◽  
Eric D. Young
Keyword(s):  
Hearing Loss ◽  
Hair Cell ◽  
Auditory Nerve ◽  
Outer Hair Cell ◽  
Dynamic Range ◽  
Nerve Fibers ◽  
Sound Level ◽  
Broadband Noise ◽  
Noise Induced Hearing Loss ◽  
Rate Level

People with sensorineural hearing loss are often constrained by a reduced acoustic dynamic range associated with loudness recruitment; however, the neural correlates of loudness and recruitment are still not well understood. The growth of auditory-nerve (AN) activity with sound level was compared in normal-hearing cats and in cats with a noise-induced hearing loss to test the hypothesis that AN-fiber rate-level functions are steeper in impaired ears. Stimuli included best-frequency and fixed-frequency tones, broadband noise, and a brief speech token. Three types of impaired responses were observed. 1) Fibers with rate-level functions that were similar across all stimuli typically had broad tuning, consistent with outer-hair-cell (OHC) damage. 2) Fibers with a wide dynamic range and shallow slope above threshold often retained sharp tuning, consistent with primarily inner-hair-cell (IHC) damage. 3) Fibers with very steep rate-level functions for all stimuli had thresholds above approximately 80 dB SPL and very broad tuning, consistent with severe IHC and OHC damage. Impaired rate-level slopes were on average shallower than normal for tones, and were steeper in only limited conditions. There was less variation in rate-level slopes across stimuli in impaired fibers, presumably attributable to the lack of suppression-induced reductions in slopes for complex stimuli relative to BF-tone slopes. Sloping saturation was observed less often in impaired fibers. These results illustrate that AN fibers do not provide a simple representation of the basilar-membrane I/O function and suggest that both OHC and IHC damage can affect AN response growth.

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.

Coincidence detection by binaural neurons in the chick brain stem

1993 ◽  
Vol 69 (4) ◽  
pp. 1197-1211 ◽  
Author(s):  
A. W. Joseph ◽  
R. L. Hyson
Keyword(s):  
Action Potential ◽  
Brain Stem ◽  
Response Latency ◽  
Interstimulus Interval ◽  
Interaural Time Difference ◽  
Response Probability ◽  
Coincidence Detection ◽  
Maximal Response ◽  
Bilateral Stimulation ◽  
Auditory Brain Stem

1. Neurons in nucleus laminaris (NL) of birds are the first to receive binaural information and are presumed to play a role in encoding interaural time differences (ITDs). We studied extracellular single-unit responses of NL neurons in slices of the auditory brain stem of the chick. The afferents to NL were activated by electrical stimulation of nucleus magnocellularis (NM) or the auditory nerve. Changes in responses were measured as the delay between trains of bilateral stimuli (the simulated interaural time difference or S-ITD, n = 26) was varied and as the interstimulus interval and stimulus amplitude were varied (n = 61). 2. The probability of an action potential and the action-potential latency varied as a function of interstimulus interval. Most NL neurons showed a greater response probability and a shorter response latency to an interstimulus interval between 2.5 and 3.5 ms. The interstimulus interval that produced the minimum response latency was slightly longer than the interval that produced the maximum response probability. In contrast, NM neurons (n = 4) showed no preferred rate, instead, the probability of firing increased as the interstimulus interval increased. 3. Responses to bilateral stimulation showed that NL neurons can act as coincidence detectors. NL neurons responded most reliably when activated simultaneously by their two inputs and, at favorable S-ITDs, two subthreshold inputs combined to produce an action potential. 4. NL neurons also exhibited inhibition during bilateral stimulation. At unfavorable S-ITDs a subthreshold input combined with a suprathreshold input produced fewer action potentials than evoked by the suprathreshold input alone. 5. The latency of the bilateral response varied as a function of S-ITD. At S-ITDs near coincidence the latency of the bilateral response was shorter than the latency of either of the unilateral responses. Away from coincidence, the latency of the bilateral response was largely determined by the latency of the stronger unilateral response. When the unilateral responses were of similar strength, the earlier stimulus determined the latency of the bilateral response. 6. The range of S-ITDs producing a maximal response varied as a function of stimulus strength but was never less than approximately 300 microseconds. This is greater than the maximum possible ITD of sound calculated for the chick's head size. From these data we hypothesize that, in the chick, single units cannot uniquely encode ITDs, but rather ITDs may be coded by the proportion of maximally firing cells along an isofrequency band in NL.

Sign in / Sign up

Export Citation Format

Share Document