Binaural interaction in the lateral superior olive: time difference sensitivity studied in mouse brain slice

1992 ◽  
Vol 68 (4) ◽  
pp. 1151-1159 ◽  
Author(s):  
S. H. Wu ◽  
J. B. Kelly
Keyword(s):  
Brain Slice ◽  
Response Probability ◽  
Interpulse Interval ◽  
Superior Olivary Complex ◽  
Lead Times ◽  
Complete Suppression ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Trapezoid Body ◽  
Stimulation Of

1. The sensitivity of lateral superior olive (LSO) neurons to interaural time differences was examined in an in vitro brain slice preparation. Brain slices, 400-500 microns, were taken through the superior olivary complex of C57 BL/6J mice and were maintained in an oxygenated saline solution for single-unit recording. Both extracellular and intracellular recordings were made with glass pipettes filled with 4 M potassium acetate. Responses were elicited by applying current pulses to the trapezoid body through bipolar stimulating electrodes located ipsilateral or contralateral to the olivary complex. Binaural interactions were studied by manipulating the timing and intensity of paired ipsilateral and contralateral pulses. 2. In extracellular recordings, stimulation of the ipsilateral trapezoid body usually elicited a single action potential, whereas stimulation of the contralateral trapezoid body failed to produce a spike response. Bilateral stimulation resulted in the complete suppression of the evoked spike, indicating the presence of a contralateral inhibitory effect. The degree of inhibition depended on the interpulse interval between ipsilateral and contralateral stimulation. With sufficiently large ipsilateral lead times, the probability of eliciting an extracellular spike was 1.0. As the interpulse interval was gradually shifted to reduce the ipsilateral lead time, the response probability precipitously dropped to 0.0. Most neurons could be completely suppressed by simultaneous stimulation. The dynamic range, defined as the range of interpulse intervals over which response probability changed from 0.9 to 0.1, was between 125 and 225 microseconds for most cells tested. 3. With increasing contralateral lead times, the extracellularly recorded spike was eventually released from inhibition.(ABSTRACT TRUNCATED AT 250 WORDS)

scholarly journals GABA is a modulator, rather than a classical transmitter, in the medial nucleus of the trapezoid body–lateral superior olive sound localization circuit

2019 ◽  
Vol 597 (8) ◽  
pp. 2269-2295 ◽  
Author(s):  
Alexander U. Fischer ◽  
Nicolas I. C. Müller ◽  
Thomas Deller ◽  
Domenico Del Turco ◽  
Jonas O. Fisch ◽  
...  
Keyword(s):  
Sound Localization ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Medial Nucleus ◽  
Trapezoid Body

scholarly journals GABAB and Trk Receptor Signaling Mediates Long-Lasting Inhibitory Synaptic Depression

2001 ◽  
Vol 86 (1) ◽  
pp. 536-540 ◽  
Author(s):  
Vibhakar C. Kotak ◽  
Christopher DiMattina ◽  
Dan H. Sanes
Keyword(s):  
Synaptic Depression ◽  
Inhibitory Synapses ◽  
Receptor Signaling ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Medial Nucleus ◽  
Dependent Form ◽  
Early Expression ◽  
Neurotrophin Signaling ◽  
Trapezoid Body

In many areas of the nervous system, excitatory and inhibitory synapses are reconfigured during early development. We have previously described the anatomical refinement of an inhibitory projection from the medial nucleus of the trapezoid body to the lateral superior olive in the developing gerbil auditory brain stem. Furthermore, these inhibitory synapses display an age-dependent form of long-lasting depression when activated at a low rate, suggesting that this process could support inhibitory synaptic refinement. Since the inhibitory synapses release both glycine and GABA during maturation, we tested whether GABAB receptor signaling could initiate the decrease in synaptic strength. When whole cell recordings were made from lateral superior olive neurons in a brain slice preparation, the long-lasting depression of medial nucleus of the trapezoid body–evoked inhibitory potentials was eliminated by the GABABreceptor antagonist, SCH-50911. In addition, inhibitory potentials could be depressed by repeated exposure to the GABAB receptor agonist, baclofen. Since GABAB receptor signaling may not account entirely for inhibitory synaptic depression, we examined the influence of neurotrophin signaling pathways located in the developing superior olive. Bath application of brain-derived neurotrophic factor or neurotrophin-3 depressed evoked inhibitory potentials, and use-dependent depression was blocked by the tyrosine kinase antagonist, K-252a. We suggest that early expression of GABAergic and neurotrophin signaling mediates inhibitory synaptic plasticity, and this mechanism may support the anatomical refinement of inhibitory connections.

Lateral Superior Olive

2019 ◽  
pp. 328-394 ◽  
Author(s):  
Eckhard Friauf ◽  
Elisa G. Krächan ◽  
Nicolas I.C. Müller
Keyword(s):  
Neural Plasticity ◽  
Auditory Processing ◽  
Sound Intensity ◽  
Inhibitory Synapses ◽  
Superior Olivary Complex ◽  
Central Auditory Processing ◽  
Spatial Cues ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Interaural Level Differences

Auditory neurons in the mammalian brainstem are involved in several basic computation processes essential for survival; for example, sound localization. Differences in sound intensity between the two ears, so-called interaural level differences (ILDs), provide important spatial cues for localizing sound in the horizontal plane, particularly for animals with high-frequency hearing. The earliest center of ILD detection is the lateral superior olive (LSO), a prominent component of the superior olivary complex (SOC) in the medulla oblongata. LSO neurons receive input from both ears of excitatory and inhibitory nature and perform a subtraction-like process. The LSO has become a model system for studies addressing inhibitory synapses, map formation, and neural plasticity. This review aims to provide an overview of several facets of the LSO, focusing on its functional and anatomical organization, including development and plasticity. Understanding this important ILD detector is fundamental in multiple ways—among others, to analyze central auditory processing disorders and central presbyacusis.

Interaural Level Difference Processing in the Lateral Superior Olive and the Inferior Colliculus

2004 ◽  
Vol 92 (1) ◽  
pp. 289-301 ◽  
Author(s):  
Thomas J. Park ◽  
Achim Klug ◽  
Michael Holinstat ◽  
Benedikt Grothe
Keyword(s):  
Inferior Colliculus ◽  
Population Analysis ◽  
Single Cells ◽  
Central Nucleus ◽  
Interaural Level Difference ◽  
Population Activity ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Synaptic Level ◽  
Stimulation Of

Interaural level differences (ILDs) provide salient cues for localizing high-frequency sounds in space, and populations of neurons that are sensitive to ILDs are found at almost every synaptic level from brain stem to cortex. These cells are predominantly excited by stimulation of one ear and predominantly inhibited by stimulation of the other ear, such that the magnitude of their response is determined in large part by the intensities at the 2 ears. However, in many cases ILD sensitivity is also influenced by overall intensity, which challenges the idea of unambiguous ILD coding. We investigated whether ambiguity is reduced from one synaptic level to another for 2 centers in the so-called ILD processing pathway. We recorded from single cells in the free-tailed bat lateral superior olive (LSO), the first station where ILDs are coded, and the central nucleus of the inferior colliculus (ICC), which receives a strong projection from the LSO, as well as convergent projections from many other auditory centers. We assessed effects of overall intensity by comparing ILD functions generated with different fixed intensities to the excitatory ear. LSO cells were characterized by functions that shifted in a systematic manner with increasing intensity to the excitatory ear. In contrast, significantly more ICC cells had functions that were stable across overall sound intensity, indicating that hierarchical transformations increase stability. Furthermore, a population analysis based on proportion of active cells indicated that stability in the ICC was greatly enhanced when overall population activity was considered.

The Brain Stem Evoked Response and Medial Nucleus of the Trapezoid Body

1994 ◽  
Vol 110 (1) ◽  
pp. 84-92 ◽  
Author(s):  
Chiyeko Tsuchitani
Keyword(s):  
Brain Stem ◽  
Action Potentials ◽  
Stimulus Onset ◽  
Evoked Response ◽  
Superior Olivary Complex ◽  
Lateral Superior Olive ◽  
Medial Nucleus ◽  
Brain Stem Evoked Response ◽  
The Brain ◽  
Trapezoid Body

Single-unit responses of cat superior olivary complex neurons to acoustic stimuli were examined to determine whether the units' action potentials were sufficiently synchronized to contribute to the brain stem evoked response. The medial nucleus of the trapezoid body and lateral superior olive are two major nuclei within the cat superior olivary complex. The first-spike discharge latencies of medial nucleus of the trapezoid body and lateral superior olivary neurons to monaural presentations of tone burst stimuli were measured as a function of stimulus level. Evidence is provided to support the hypotheses that in cat the medial nucleus of the trapezoid body may contribute directly to the monaural brain stem evoked response by producing action potentials synchronized to stimulus onset and may also contribute indirectly to the brain stem evoked response binaural difference wave bc by inhibiting the lateral superior olive unit excitatory responses synchronized to stimulus onset.

Glycine and GABA influence binaural processing in the inferior colliculus of the mustache bat

1995 ◽  
Vol 74 (4) ◽  
pp. 1701-1713 ◽  
Author(s):  
A. Klug ◽  
T. J. Park ◽  
G. D. Pollak
Keyword(s):  
Receptor Antagonist ◽  
Inferior Colliculus ◽  
Spike Count ◽  
Gabaergic Inhibition ◽  
Lateral Superior Olive ◽  
Superior Olive ◽  
Contralateral Ear ◽  
Glycinergic Inhibition ◽  
Ipsilateral Stimulation ◽  
Stimulation Of

1. The mammalian inferior colliculus contains large populations of binaural cells that are excited by stimulation of the contralateral ear and are inhibited by stimulation of the ipsilateral ear, and are called excitatory/inhibitory (EI) cells. Neurons with EI properties are initially created in the lateral superior olive (LSO), which, in turn, sends strong bilateral projections to the inferior colliculus. The questions that we address in this report are 1) whether the inhibition evoked by stimulation of the ipsilateral ear occurs at the inferior colliculus or whether it occurs in a lower nucleus, presumably the LSO; and 2) if the ipsilaterally evoked inhibition occurs at the inferior colliculus, is the inhibition a consequence of glycinergic innervation or is it a consequence of GABAergic innervation. To study these questions, we recorded from 61 EI neurons in the inferior colliculus of the mustache bat before and during the iontophoretic application of the glycine receptor antagonist, strychnine. We also tested the effects of the gamma-aminobutyric acid-A (GABAA) receptor antagonist, bicuculline, on 38 of the 61 neurons that were tested with strychnine. The main finding is that glycinergic or GABAergic inhibition, or both, contribute to the ipsilaterally evoked inhibition in approximately 50% of the EI neurons in the inferior colliculus. 2. Strychnine and bicuculline had different effects on the magnitude of the spike counts evoked by stimulation of the contralateral (excitatory) ear. On average, strychnine caused the maximum spike count evoked by contralateral stimulation to increase by only 23%. The relatively small effects of strychnine on response magnitude are in marked contrast to the effects of bicuculline, which usually caused much larger increases in spike counts. For example, although strychnine caused spike counts to more than double in approximately 25% of the collicular neurons, bicuculline caused a doubling of the spike count in approximately 60% of the cells. 3. The inhibitory influences of ipsilateral stimulation were evaluated by driving the neurons with a fixed intensity at the contralateral ear and then documenting the reductions in spike counts due to the presentation of progressively higher intensities at the ipsilateral ear. In 64% of the neurons sampled, blocking glycinergic inhibition with strychnine had little or no effect on the ipsilaterally evoked inhibition. These cells remained as strongly inhibited during the application of strychnine as they did before its application. In addition, the ipsilateral intensity that produced complete or nearly complete spike suppression in the predrug condition was also unchanged by strychnine. 4. In 36% of the neurons, strychnine markedly reduced the degree of ipsilaterally evoked spike suppression. In five of these neurons, there was a complete elimination of the ipsilateral inhibition: these neurons were transformed from strongly inhibited EI neurons into monaural neurons. 5. The influence of both strychnine and bicuculline was tested sequentially in 38 neurons. In about one-half of these cells, (53%, 20/38) the ipsilaterally evoked inhibition was unaffected by either drug. In 10 other units (26%), both drugs substantially reduced or eliminated the ipsilaterally evoked inhibition. In most of these cells, both bicuculline and strychnine reduced the ipsilaterally evoked inhibition to a similar degree. In the remaining eight cells studied with both drugs (21%), the ipsilaterally evoked inhibition was reduced or eliminated by one of the drugs, but not by both. 6. These results show that both glycinergic and GABAergic projections influence the ipsilaterally evoked inhibition in about one-half of the EI neurons in the inferior colliculus. The glycinergic inhibition elicited by ipsilateral stimulation is most likely due to projections from the ipsilateral lateral superior olive, whereas the GABAergic inhibition evoked by ipsilateral stimulation is most likely caused b

Functional organization of lateral cell groups of cat superior olivary complex

1977 ◽  
Vol 40 (2) ◽  
pp. 296-318 ◽  
Author(s):  
C. Tsuchitani
Keyword(s):  
Superior Olivary Complex ◽  
Maximum Output ◽  
Medial Superior Olive ◽  
Superior Olive ◽  
Response Characteristics ◽  
Cell Groups ◽  
Discharge Patterns ◽  
Intensity Functions ◽  
Contralateral Stimulus ◽  
Stimulation Of

1. Single-unit discharges to auditory stimuli were recorded extracellularly from superior olivary complex (SOC) units located lateral to the medial superior olive. Stimuli consisted of monaurally or binaurally presented tone bursts. The response measures obtained were effective ear, nature of effect, stimulus-frequency representation, maximum output, latency of response, and temporal pattern of tone burst-elicited discharges. Electrolytic marks were made at the unit studied or at the end of the electrode tract and in the medial superior olive. Following each experiment the locations of the units studied were determined histologically. An atlas of the laterally located SOC cell groups was developed to permit classification of units on the basis of localization within cell groups. Units were also classified according to the effects of stimulating the two ears. 2. All SOC units located lateral to the medial superior olive were excited by stimulation of the ipsilateral ear. Stimulation of the contralateral ear either excited, inhibited, had no effect, or had a potentiating effect on the discharges elicited by stimulating the ipsilateral ear. 3. Most lateral superior olivary (LSO) units were inhibited by contralateral stimulation, were narrowly tuned, produced low to high levels of maximum output, had short latencies, and produced regular discharge patterns characterized by chopper PST histograms with narrow initial peaks. 4. Most units within the caudal margins of the LSO (pLSO) were not affected or were inhibited by a contralateral stimulus; many were broadly tuned and exhibited intensity functions with large dynamic range and low slope. These units also had long latencies and produced chopper PST histograms with wide initial peaks. 5. Most units located dorsal to the LSO (DPO and DLPO) were not affected by the contralateral stimulus, were narrowly tuned, produced moderate levels of maximum discharge, had long latencies, and produced chopper PST histograms with wide initial peaks. 6. Units located ventral to the LSO appeared to have response characteristics related to unit location. Most units below the ventral hilum of the LSO (VLPO) were inhibited by the contralateral stimulus and many were broadly tuned VLPO units produced wide or poorly defined narrow-chopper discharge patterns and intensity functions with high maximum output. Most units located ventral to the lateral loop of the LSO (LNTB) were not affected by the contralateral stimulus and had response characteristics that may be related to the rostrocaudal location of the unit. 7. The cell groups located dorsal and ventral to the LSO were tonotopically organized with low-frequency-sensitive units located laterally and high-frequency-sensitive units located medially. The units located along the caudal margins of the LSO had a tonotopic organization similar to that of the LSO.

The inhibition of cat lateral superior olive unit excitatory responses to binaural tone bursts. II. The sustained discharges

1988 ◽  
Vol 59 (1) ◽  
pp. 184-211 ◽  
Author(s):  
C. Tsuchitani
Keyword(s):  
Unit Activity ◽  
Statistical Properties ◽  
Serial Dependence ◽  
Control Stimulus ◽  
Interspike Intervals ◽  
Lateral Superior Olive ◽  
Comparable Rate ◽  
Superior Olive ◽  
Contralateral Ear ◽  
Stimulation Of

1. Preliminary to extending a point process model of lateral superior olive (LSO) unit activity to describe the units' binaural responses, the statistical properties of their discharges to binaural tone bursts were studied. The hypothesis that stimulation of the contralateral ear results in the simple reduction of the ipsilateral input was also examined. Single-unit activity was recorded extracellularly from the LSO of the anesthetized cat. The sustained discharges to characteristic frequency (CF) tone bursts presented simultaneously to the two ears were examined to determine whether the fine temporal (statistical) properties of these discharges differed from those of the discharges elicited by stimulating the ipsilateral ear alone. 2. The major effect of simultaneously stimulating the contralateral ear was the inhibition (i.e., the reduction in the mean discharge rate) of the sustained discharges to the ipsilateral control stimulus. The temporal pattern of discharges to the ipsilateral stimulus was also affected by stimulation of the contralateral ear. The discharges to binaural stimulation were more irregular in pattern: they often produced bimodal or multimodal interval histograms where unimodal interval histograms had been produced by the discharges to the ipsilateral control stimulus alone. The hazard function, an estimate of the unit recovery function, also often differed in form for the binaural and monaural discharges. 3. The binaural discharges could be distinguished from an ipsilaterally elicited discharge of comparable mean rate: there was a greater incidence of “short” interspike intervals in the binaural discharge. These short interspike intervals occurred most frequently in the discharges to the ipsilateral control stimulus alone and infrequently in the discharges to an ipsilateral stimulus that produced a mean rate similar to that of the binaural discharge. Thus the dead time estimates derived from the binaural discharges were more similar to the estimates derived from the ipsilateral control discharges than to those derived from the comparable-rate ipsilaterally elicited discharges. 4. Although the measures of the recovery properties of LSO unit discharges differed under monaural and binaural stimulus conditions, the serial dependence observed between successive interspike intervals in the binaurally elicited discharges was similar to that in the ipsilaterally elicited discharges. The conditional mean function, an estimate of the serial dependence or unit shifting function, did not differ greatly in form for the monaural and binaural discharges.(ABSTRACT TRUNCATED AT 400 WORDS)

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