Interaural Time Difference Processing in the Mammalian Medial Superior Olive: The Role of Glycinergic Inhibition

Neurons in the medial superior olive (MSO) are tuned to the interaural time difference (ITD) of sound arriving at the two ears. MSO neurons evoke a strongest response at their best delay (BD), at which the internal delay between bilateral inputs to MSO matches the external ITD. We performed extracellular recordings in the superior olivary complex of the anesthetized gerbil and found a majority of single units localized to the MSO to exhibit BDs that shifted with tone frequency. The relation of best interaural phase difference to tone frequency revealed nonlinearities in some MSO units and others with linear relations with characteristic phase between 0.4 and 0.6 cycles. The latter is usually associated with the interaction of ipsilateral excitation and contralateral inhibition, as in the lateral superior olive, yet all MSO units exhibited evidence of bilateral excitation. Interaural cochlear delays and phase-locked contralateral inhibition are two mechanisms of internal delay that have been suggested to create frequency-dependent delays. Best interaural phase-frequency relations were compared with a cross-correlation model of MSO that incorporated interaural cochlear delays and an additional frequency-independent delay component. The model with interaural cochlear delay fit phase-frequency relations exhibiting frequency-dependent delays with precision. Another model of MSO incorporating inhibition based on realistic biophysical parameters could not reproduce observed frequency-dependent delays.

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The role of interaural time difference and fundamental frequency difference in the identification of concurrent vowel pairs

The Journal of the Acoustical Society of America ◽

10.1121/1.402811 ◽

1992 ◽

Vol 91 (6) ◽

pp. 3579-3581 ◽

Cited By ~ 26

Author(s):

Trevor M. Shackleton ◽

Ray Meddis

Keyword(s):

Fundamental Frequency ◽

Interaural Time Difference ◽

Time Difference ◽

Frequency Difference

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Auditory brainstem models: adapting cochlear nuclei improve spatial encoding by the medial superior olive in reverberation

10.1101/694356 ◽

2019 ◽

Author(s):

Andrew Brughera ◽

Jason Mikiel-Hunter ◽

Mathias Dietz ◽

David McAlpine

Keyword(s):

Spatial Information ◽

Interaural Time Difference ◽

Auditory Pathway ◽

Auditory Brainstem ◽

Coincidence Detection ◽

Type Model ◽

Medial Superior Olive ◽

Sound Energy ◽

Superior Olive ◽

Cochlear Nuclei

AbstractListeners perceive sound-energy as originating from the direction of its source, even as direct sound is followed milliseconds later by reflected sound from multiple different directions. Early-arriving sound is emphasised in the ascending auditory pathway, including the medial superior olive (MSO) where binaural neurons encode the interaural time difference (ITD) cue for spatial location. Behaviourally, weighting of ITD conveyed during rising sound-energy is stronger at 600 Hz, a frequency with higher reverberant energy, than at 200 Hz where reverberant energy is lower. Here we computationally explore the combined effectiveness of adaptation before ITD-encoding, and excitatory binaural coincidence detection within MSO neurons, in emphasising ITD conveyed in early-arriving sound. With excitatory inputs from adapting model spherical bushy cells (SBCs) of the bilateral cochlear nuclei, a Hodgkin-Huxley-type model MSO neuron reproduces the frequency-dependent emphasis of rising vs. peak sound-energy in ITD-encoding. Maintaining the adaptation in model SBCs, and adjusting membrane speed in model MSO neurons, hemispheric populations of model SBCs and MSO neurons, with simplified membranes for computational efficiency, also reproduce the stronger weighting of ITD information conveyed during rising sound-energy at 600 Hz compared to 200 Hz. This hemispheric model further demonstrates a link between strong weighting of spatial information during rising sound-energy, and correct unambiguous lateralisation of reverberant speech.

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

Journal of Neurophysiology ◽

10.1152/jn.1985.53.1.89 ◽

1985 ◽

Vol 53 (1) ◽

pp. 89-109 ◽

Cited By ~ 79

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)

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Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset

The Journal of Physiology ◽

10.1113/jphysiol.2005.094763 ◽

2005 ◽

Vol 568 (2) ◽

pp. 497-512 ◽

Cited By ~ 86

Author(s):

Anna K. Magnusson ◽

Christoph Kapfer ◽

Benedikt Grothe ◽

Ursula Koch

Keyword(s):

Medial Superior Olive ◽

Superior Olive ◽

Glycinergic Inhibition

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Estimated Cochlear Delays in Low Best-Frequency Neurons in the Barn Owl Cannot Explain Coding of Interaural Time Difference

Journal of Neurophysiology ◽

10.1152/jn.00501.2010 ◽

2010 ◽

Vol 104 (4) ◽

pp. 1946-1954 ◽

Cited By ~ 6

Author(s):

Martin Singheiser ◽

Brian J. Fischer ◽

Hermann Wagner

Keyword(s):

Interaural Time Difference ◽

Low Frequency ◽

Barn Owl ◽

Time Difference ◽

Central Nucleus ◽

Response Functions ◽

Frequency Range ◽

Response Peak ◽

Cochlear Delays

The functional role of the low-frequency range (<3 kHz) in barn owl hearing is not well understood. Here, it was tested whether cochlear delays could explain the representation of interaural time difference (ITD) in this frequency range. Recordings were obtained from neurons in the core of the central nucleus of the inferior colliculus. The response of these neurons varied with the ITD of the stimulus. The response peak shared by all neurons in a dorsoventral penetration was called the array-specific ITD and served as criterion for the representation of a given ITD in a neuron. Array-specific ITDs were widely distributed. Isolevel frequency response functions obtained with binaural, contralateral, and ispilateral stimulation exhibited a clear response peak and the accompanying frequency was called the best frequency. The data were tested with respect to predictions of a model, the stereausis model, assuming cochlear delays as source for the best ITD of a neuron. According to this model, different cochlear delays determined by mismatches between the ipsilateral and contralateral best frequencies are the source for the ITD in a binaural neuron. The mismatch should depend on the best frequency and the best ITD. The predictions of the stereausis model were not fulfilled in the low best-frequency neurons analyzed here. It is concluded that cochlear delays are not responsible for the representation of best ITD in the barn owl.

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