scholarly journals Stochastic Model Explains the Role of Excitation and Inhibition in Binaural Sound Localization in Mammals

2011 ◽  
pp. 573-583 ◽  
Author(s):  
M. DRAPAL ◽  
P. MARSALEK
Keyword(s):  
Sound Localization ◽  
Arrival Time ◽  
Neural Circuit ◽  
Low Frequency ◽  
Spike Timing ◽  
Inhibitory Input ◽  
Medial Superior Olive ◽  
Interaural Time Differences ◽  
Stochastic Description

Interaural time differences (ITDs), the differences of arrival time of the sound at the two ears, provide a major cue for low-frequency sound localization in the horizontal plane. The first nucleus involved in the computation of ITDs is the medial superior olive (MSO). We have modeled the neural circuit of the MSO using a stochastic description of spike timing. The inputs to the circuit are stochastic spike trains with a spike timing distribution described by a given probability density function (beta density). The outputs of the circuit reproduce the empirical firing rates found in experiment in response to the varying ITD. The outputs of the computational model are calculated numerically and these numerical simulations are also supported by analytical calculations. We formulate a simple hypothesis concerning how sound localization works in mammals. According to this hypothesis, there is no array of delay lines as in the Jeffress’ model, but the inhibitory input is shifted in time as a whole. This is consistent with experimental observations in mammals.

scholarly journals Inhibition in the balance: binaurally coupled inhibitory feedback in sound localization circuitry

2011 ◽  
Vol 106 (1) ◽  
pp. 4-14 ◽  
Author(s):  
R. Michael Burger ◽  
Iwao Fukui ◽  
Harunori Ohmori ◽  
Edwin W. Rubel
Keyword(s):  
Sound Localization ◽  
Arrival Time ◽  
Dynamic Range ◽  
Low Frequency ◽  
Neural Circuitry ◽  
Significant Progress ◽  
Interaural Time Differences ◽  
Inhibitory Function ◽  
Inhibitory Feedback ◽  
Auditory Systems

Interaural time differences (ITDs) are the primary cue animals, including humans, use to localize low-frequency sounds. In vertebrate auditory systems, dedicated ITD processing neural circuitry performs an exacting task, the discrimination of microsecond differences in stimulus arrival time at the two ears by coincidence-detecting neurons. These neurons modulate responses over their entire dynamic range to sounds differing in ITD by mere hundreds of microseconds. The well-understood function of this circuitry in birds has provided a fruitful system to investigate how inhibition contributes to neural computation at the synaptic, cellular, and systems level. Our recent studies in the chicken have made significant progress in bringing together many of these findings to provide a cohesive picture of inhibitory function.

Sound localization with microsecond precision in mammals: what is it we do not understand?

e-Neuroforum ◽  
2015 ◽  
Vol 21 (1) ◽  
Author(s):  
C. Leibold ◽  
B. Grothe
Keyword(s):  
Present State ◽  
Sound Localization ◽  
Theoretical Models ◽  
Delay Lines ◽  
Topographic Map ◽  
Medial Superior Olive ◽  
Interaural Time Differences ◽  
Coincidence Detector ◽  
Model Predictions

AbstractThe Jeffress model for the computation and encoding of interaural time differences (ITDs) is one of the most widely known theoretical models of a neuronal microcircuit. In archosaurs (birds and reptiles), several features envisioned by Jeffress in 1948 seem to be implemented, like a topographic map of space and axonal delay lines. In mammals, however, most of the model predictions could not be verified or have been disproved. This led to an ongoing competition of alternative models and hypothesis, which is not settled by far. Particularly the role of the feed-forward inhibitory inputs to the binaural coincidence detector neurons in the medial superior olive (MSO) remains a matter of debate. In this paper, we review the present state of the field and indicate what in our opinion are the most important gaps in understanding of the mammalian circuitry. Approaching these issues requires integrating all levels of neuroscience from cellular biophysics to behavior and even evolution.

scholarly journals Differences in chloride gradients allow for three distinct types of synaptic modulation by endocannabinoids

2016 ◽  
Vol 116 (2) ◽  
pp. 619-628 ◽  
Author(s):  
Yanqing Wang ◽  
Brian D. Burrell
Keyword(s):  
Neural Circuit ◽  
Critical Role ◽  
Low Frequency ◽  
Inhibitory Synapses ◽  
Primary Role ◽  
Synaptic Modulation ◽  
Hirudo Verbana ◽  
Frequency Stimulation ◽  
Circuit Output

Endocannabinoids can elicit persistent depression of excitatory and inhibitory synapses, reducing or enhancing (disinhibiting) neural circuit output, respectively. In this study, we examined whether differences in Cl−gradients can regulate which synapses undergo endocannabinoid-mediated synaptic depression vs. disinhibition using the well-characterized central nervous system (CNS) of the medicinal leech, Hirudo verbana. Exogenous application of endocannabinoids or capsaicin elicits potentiation of pressure (P) cell synapses and depression of both polymodal (Npoly) and mechanical (Nmech) nociceptive synapses. In P synapses, blocking Cl−export prevented endocannabinoid-mediated potentiation, consistent with a disinhibition process that has been indicated by previous experiments. In Nmechneurons, which are depolarized by GABA due to an elevated Cl−equilibrium potentials (ECl), endocannabinoid-mediated depression was prevented by blocking Cl−import, indicating that this decrease in synaptic signaling was due to depression of excitatory GABAergic input (disexcitation). Npolyneurons are also depolarized by GABA, but endocannabinoids elicit depression in these synapses directly and were only weakly affected by disruption of Cl−import. Consequently, the primary role of elevated EClmay be to protect Npolysynapses from disinhibition. All forms of endocannabinoid-mediated plasticity required activation of transient potential receptor vanilloid (TRPV) channels. Endocannabinoid/TRPV-dependent synaptic plasticity could also be elicited by distinct patterns of afferent stimulation with low-frequency stimulation (LFS) eliciting endocannabinoid-mediated depression of Npolysynapses and high-frequency stimulus (HFS) eliciting endocannabinoid-mediated potentiation of P synapses and depression of Nmechsynapses. These findings demonstrate a critical role of differences in Cl−gradients between neurons in determining the sign, potentiation vs. depression, of synaptic modulation under normal physiological conditions.

Role of GABAergic Inhibition in the Coding of Interaural Time Differences of Low-Frequency Sounds in the Inferior Colliculus

2005 ◽  
Vol 93 (6) ◽  
pp. 3390-3400 ◽  
Author(s):  
W. R. D’Angelo ◽  
S. J. Sterbing ◽  
E.-M. Ostapoff ◽  
S. Kuwada
Keyword(s):  
Inferior Colliculus ◽  
Signal To Noise Ratio ◽  
Interaural Time Difference ◽  
Low Frequency ◽  
Gabaergic Inhibition ◽  
Interaural Time Differences ◽  
Gaba Antagonists ◽  
Inhibitory Transmitter ◽  
Almost All

A major cue for the localization of sound in space is the interaural time difference (ITD). We examined the role of inhibition in the shaping of ITD responses in the inferior colliculus (IC) by iontophoretically ejecting γ-aminobutyric acid (GABA) antagonists and GABA itself using a multibarrel pipette. The GABA antagonists block inhibition, whereas the applied GABA provides a constant level of inhibition. The effects on ITD responses were evaluated before, during and after the application of the drugs. If GABA-mediated inhibition is involved in shaping ITD tuning in IC neurons, then applying additional amounts of this inhibitory transmitter should alter ITD tuning. Indeed, for almost all neurons tested, applying GABA reduced the firing rate and consequently sharpened ITD tuning. Conversely, blocking GABA-mediated inhibition increased the activity of IC neurons, often reduced the signal-to-noise ratio and often broadened ITD tuning. Blocking GABA could also alter the shape of the ITD function and shift its peak suggesting that the role of inhibition is multifaceted. These effects indicate that GABAergic inhibition at the level of the IC is important for ITD coding.

scholarly journals Impact of cercal air currents on singing motor pattern generation in the cricket (Gryllus bimaculatus DeGeer)

2015 ◽  
Vol 114 (5) ◽  
pp. 2649-2660 ◽  
Author(s):  
Pedro F. Jacob ◽  
Berthold Hedwig
Keyword(s):  
Motor Pattern ◽  
Low Frequency ◽  
Inhibitory Response ◽  
Pattern Generation ◽  
Inhibitory Input ◽  
Cercal System ◽  
Singing Activity ◽  
Sensory Activity ◽  
Motor Pattern Generation

The cercal system of crickets detects low-frequency air currents produced by approaching predators and self-generated air currents during singing, which may provide sensory feedback to the singing motor network. We analyzed the effect of cercal stimulation on singing motor pattern generation to reveal the response of a singing interneuron to predator-like signals and to elucidate the possible role of self-generated air currents during singing. In fictive singing males, we recorded an interneuron of the singing network while applying air currents to the cerci; additionally, we analyzed the effect of abolishing the cercal system in freely singing males. In fictively singing crickets, the effect of short air stimuli is either to terminate prematurely or to lengthen the interchirp interval, depending on their phase in the chirp cycle. Within our stimulation paradigm, air stimuli of different velocities and durations always elicited an inhibitory postsynaptic potential in the singing interneuron. Current injection in the singing interneuron elicited singing motor activity, even during the air current-evoked inhibitory input from the cercal pathway. The disruptive effects of air stimuli on the fictive singing pattern and the inhibitory response of the singing interneuron point toward the cercal system being involved in initiating avoidance responses in singing crickets, according to the established role of cerci in a predator escape pathway. After abolishing the activity of the cercal system, the timing of natural singing activity was not significantly altered. Our study provides no evidence that self-generated cercal sensory activity has a feedback function for singing motor pattern generation.

Interaural time and intensity coding in superior olivary complex and inferior colliculus of the echolocating bat Molossus ater

1985 ◽  
Vol 53 (1) ◽  
pp. 89-109 ◽  
Author(s):  
G. Harnischfeger ◽  
G. Neuweiler ◽  
P. Schlegel
Keyword(s):  
Inferior Colliculus ◽  
Stimulus Frequency ◽  
Stimulus Onset ◽  
Time Difference ◽  
Superior Olivary Complex ◽  
Inhibitory Input ◽  
Medial Superior Olive ◽  
Transient Time ◽  
Interaural Time Differences ◽  
Superior Olive

Single-unit responses to tonal stimulation with interaural disparities were recorded in the nuclei of the superior olivary complex (SOC) and the central nucleus of the inferior colliculus (ICC) of the echolocating bat, Molossus ater. Seventy-six units were recorded from the ICC and 74 from the SOC; of the SOC units, 31 were histologically verified in the medial superior olive (MSO), 10 in the lateral superior olive (LSO), and 33 in unidentified areas of the SOC. Best frequencies (BFs) of the units ranged from 10.3 to 89.6 kHz, and Q10 dB values ranged from 2 to 70 dB. Most ICC neurons responded phasically to stimulus onset and were either inhibitory/excitatory [I/E; (53)] or excitatory/excitatory [E/E; (21)] units. In the MSO, 23 units responded tonically and 7 phasically on, 18 were E/E or E/OF (facilitatory for other input) units, and 11 were I/E neurons. All LSO neurons responded in a "chopper" fashion, and the binaural neurons were E/I units. In E/E units the excitatory response to binaural stimulation was frequently larger than the sum of the monaurally evoked responses. Many neurons with E/I or I/E inputs had very steep binaural impulse-count functions and were sensitive to small interaural intensity differences. Twenty-eight units (24%) responded with a change in firing rate of at least 20% to interaural time differences of +/- 500 microseconds. Within this sample, 11 units (8 from ICC, 2 from MSO, and 1 from SOC) were sensitive to interaural time differences of only +/- 50 microseconds. Of these 11 units, 10 were I/E units responding phasically only to stimulus onset and were also sensitive to intensity differences (delta I), being suppressed completely by the inhibitory input over a delta I range of 20 dB or less. Of 117 units tested in the ICC and SOC nuclei, 86 units (76%) were not sensitive to interaural time disparities within +/- 500 microseconds. Because the BFs of these units sensitive to interaural transient time differences (delta t) ranged between 18 and 90 kHz, responses were elicited by pure tones, and responses did not change periodically with the period equal to that of the stimulus frequency, we conclude that the neurons reacted to interaural differences of stimulus-onset time (transient time difference) but not to phase differences (ongoing time difference). Sensitivity to interaural time differences was also correlated with interaural intensity differences.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Predicting binaural responses from monaural responses in the gerbil medial superior olive

2016 ◽  
Vol 115 (6) ◽  
pp. 2950-2963 ◽  
Author(s):  
Andrius Plauška ◽  
J. Gerard Borst ◽  
Marcel van der Heijden
Keyword(s):  
Amplitude Ratio ◽  
Low Frequency ◽  
Linear Representation ◽  
Coincidence Detection ◽  
Mongolian Gerbils ◽  
Medial Superior Olive ◽  
Interaural Time Differences ◽  
Arrival Times ◽  
Superior Olive ◽  
Successful Prediction

Accurate sound source localization of low-frequency sounds in the horizontal plane depends critically on the comparison of arrival times at both ears. A specialized brainstem circuit containing the principal neurons of the medial superior olive (MSO) is dedicated to this comparison. MSO neurons are innervated by segregated inputs from both ears. The coincident arrival of excitatory inputs from both ears is thought to trigger action potentials, with differences in internal delays creating a unique sensitivity to interaural time differences (ITDs) for each cell. How the inputs from both ears are integrated by the MSO neurons is still debated. Using juxtacellular recordings, we tested to what extent MSO neurons from anesthetized Mongolian gerbils function as simple cross-correlators of their bilateral inputs. From the measured subthreshold responses to monaural wideband stimuli we predicted the rate-ITD functions obtained from the same MSO neuron, which have a damped oscillatory shape. The rate of the oscillations and the position of the peaks and troughs were accurately predicted. The amplitude ratio between dominant and secondary peaks of the rate-ITD function, captured in the width of its envelope, was not always exactly reproduced. This minor imperfection pointed to the methodological limitation of using a linear representation of the monaural inputs, which disregards any temporal sharpening occurring in the cochlear nucleus. The successful prediction of the major aspects of rate-ITD curves supports a simple scheme in which the ITD sensitivity of MSO neurons is realized by the coincidence detection of excitatory monaural inputs.

scholarly journals Physiology and anatomy of neurons in the medial superior olive of the mouse

2016 ◽  
Vol 116 (6) ◽  
pp. 2676-2688 ◽  
Author(s):  
Matthew J. Fischl ◽  
R. Michael Burger ◽  
Myriam Schmidt-Pauly ◽  
Olga Alexandrova ◽  
James L. Sinclair ◽  
...  
Keyword(s):  
Sound Localization ◽  
Molecular Mechanisms ◽  
Low Frequency ◽  
Acoustic Stimulation ◽  
Medial Superior Olive ◽  
Temporal Acuity ◽  
Low Frequencies ◽  
Superior Olive

In mammals with good low-frequency hearing, the medial superior olive (MSO) computes sound location by comparing differences in the arrival time of a sound at each ear, called interaural time disparities (ITDs). Low-frequency sounds are not reflected by the head, and therefore level differences and spectral cues are minimal or absent, leaving ITDs as the only cue for sound localization. Although mammals with high-frequency hearing and small heads (e.g., bats, mice) barely experience ITDs, the MSO is still present in these animals. Yet, aside from studies in specialized bats, in which the MSO appears to serve functions other than ITD processing, it has not been studied in small mammals that do not hear low frequencies. Here we describe neurons in the mouse brain stem that share prominent anatomical, morphological, and physiological properties with the MSO in species known to use ITDs for sound localization. However, these neurons also deviate in some important aspects from the typical MSO, including a less refined arrangement of cell bodies, dendrites, and synaptic inputs. In vitro, the vast majority of neurons exhibited a single, onset action potential in response to suprathreshold depolarization. This spiking pattern is typical of MSO neurons in other species and is generated from a complement of Kv1, Kv3, and IH currents. In vivo, mouse MSO neurons show bilateral excitatory and inhibitory tuning as well as an improvement in temporal acuity of spiking during bilateral acoustic stimulation. The combination of classical MSO features like those observed in gerbils with more unique features similar to those observed in bats and opossums make the mouse MSO an interesting model for exploiting genetic tools to test hypotheses about the molecular mechanisms and evolution of ITD processing.

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