Medial Superior Olivary Neurons Receive Surprisingly Few Excitatory and Inhibitory Inputs with Balanced Strength and Short-Term Dynamics

Couchman, Kiri; Grothe, Benedikt; Felmy, Felix

doi:10.1523/jneurosci.1760-10.2010

Cited by 108 publications

(143 citation statements)

References 49 publications

(107 reference statements)

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“…Using both anatomical and functional data, Couchman et al (2010) estimated that the total excitatory synaptic strength in gerbil MSO neurons (the sum of the synaptic conductances for all inputs) is 180-200 nS. This value is comparable to the 200 nS total synaptic strength used in the "fast" MSO model that gave good ITD sensitivity at 1000 Hz (Fig.…”

Section: Relation To Other Models and Limitations Of The Modelmentioning

confidence: 72%

Modeling Binaural Responses in the Auditory Brainstem to Electric Stimulation of the Auditory Nerve

Chung

Delgutte

Colburn

2014

JARO

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Bilateral cochlear implants (CIs) provide improvements in sound localization and speech perception in noise over unilateral CIs. However, the benefits arise mainly from the perception of interaural level differences, while bilateral CI listeners' sensitivity to interaural time difference (ITD) is poorer than normal. To help understand this limitation, a set of ITD-sensitive neural models was developed to study binaural responses to electric stimulation. Our working hypothesis was that central auditory processing is normal with bilateral CIs so that the abnormality in the response to electric stimulation at the level of the auditory nerve fibers (ANFs) is the source of the limited ITD sensitivity. A descriptive model of ANF response to both acoustic and electric stimulation was implemented and used to drive a simplified biophysical model of neurons in the medial superior olive (MSO). The model's ITD sensitivity was found to depend strongly on the specific configurations of membrane and synaptic parameters for different stimulation rates. Specifically, stronger excitatory synaptic inputs and faster membrane responses were required for the model neurons to be ITD-sensitive at high stimulation rates, whereas weaker excitatory synaptic input and slower membrane responses were necessary at low stimulation rates, for both electric and acoustic stimulation. This finding raises the possibility of frequency-dependent differences in neural mechanisms of binaural processing; limitations in ITD sensitivity with bilateral CIs may be due to a mismatch between stimulation rate and cell parameters in ITD-sensitive neurons.

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Section: Relation To Other Models and Limitations Of The Modelmentioning

confidence: 72%

Modeling Binaural Responses in the Auditory Brainstem to Electric Stimulation of the Auditory Nerve

Chung

Delgutte

Colburn

2014

JARO

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“…Synaptic input was modeled as the convergence of 32 independent excitatory fibers from each side and 32 contralateral inhibitory fibers, with each fiber firing in a time-varying Poisson-like manner at ϳ160 spikes/s for 2 s, and phase-locked to an input frequency f, with a vector strength R ϭ 0.9. The number of excitatory and inhibitory fibers was larger than the estimated minimum number necessary to evoke an action potential in MSO (Couchman et al 2010); however, a larger number may be necessary to maintain sustained activity given the substantial short-term synaptic depression in MSO (Couchman et al 2010). Phase-locking was achieved by choosing a synaptic event time in a given tone period as a Gaussian random number centered on zero with SD ϭ sqrt(Ϫ2logR)/(2f) (Mardia and Jupp 2000).…”

Section: Methodsmentioning

confidence: 90%

Frequency-dependent interaural delays in the medial superior olive: implications for interaural cochlear delays

Day

Semple

2011

Journal of Neurophysiology

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Day ML, Semple MN. Frequency-dependent interaural delays in the medial superior olive: implications for interaural cochlear delays. J Neurophysiol 106: 1985-1999. First published July 20, 2011 doi:10.1152/jn.00131.2011.-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 phasefrequency 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. interaural time delay; interaural time difference; sound localization; gerbil; superior olivary complex HUMANS AND MANY OTHER ANIMALS localize sound in the horizontal plane using interaural sound cues. In humans, the interaural time difference (ITD)-the difference of arrival time of sound to the two ears-is the dominant cue to localize sound azimuth whenever low-frequency information is available (Wightman and Kistler 1992). The medial superior olive (MSO) is considered the primary site along the auditory pathway to encode ITDs in its neuron's firing patterns (Yin 2002), as it receives input bilaterally from monaural brain stem nuclei [the anteroventral cochlear nuclei (AVCN)] and yields spike rate responses that are tuned to the ITD of sound (Goldberg and Brown 1969;Yin and Chan 1990).As initially proposed by Jeffress (1948), the excitatory inputs onto the ITD processor phase-lock to pure tones (e.g., Joris et al. 1994a) and elicit a tuned rate response to ITD in the MSO via coincidence detection (Goldberg and Brown 1969). While the basic construction of ITD sensitivity is clear, there has been much debate over the mechanisms of internal delay that determine which ITD elicits the greatest rate response, i.e., the best delay (BD) (Joris and Yin

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“…Synapses with high P r , small RRPs, and strong STD appear well-suited for coding ITDs (Kuba et al, 2002;Cook et al, 2003;Yang and Xu-Friedman, 2009;Couchman et al, 2010), whereas synapses with low P r , large RRPs, and STF followed by slow depression are better tuned for coding ILDs (MacLeod et al, 2007;Yang and Xu-Friedman, 2009). Thus, it is tempting to speculate that calyces with simple morphologies filter timing information, those with complex morphologies filter intensity information, and those with intermediate morphologies filter a combination of both.…”

Section: Role In Sound Localizationmentioning

confidence: 99%

Morphological and Functional Continuum Underlying Heterogeneity in the Spiking Fidelity at the Calyx of Held SynapseIn Vitro

Grande¹,

Wang²

2011

J. Neurosci.

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Reliable neuronal spiking is critical for a myriad of computations performed by neural circuits. This is particularly evident for sound localization cues in the auditory brainstem circuits that detect timing and intensity differences of sounds arriving at two ears. The calyx of Held-principal neuron synapse in the medial nucleus of the trapezoid body (MNTB) in this circuit is traditionally viewed as a reliable relay, which converts contralateral excitatory inputs to inhibitory outputs to ipsilateral superior olive neurons that code interaural timing and intensity differences. However, recent studies demonstrated large variability in the incidence of postsynaptic spike failures at this synapse, challenging the view that this synapse is a fail-safe relay. Using combined imaging and paired recordings in mature (P16 -P19) mouse brainstem slices, we show that spike failure rates of MNTB neurons are strongly correlated with differences in gross morphology of the calyx terminal and quantal properties under standard in vitro-and in vivo-like conditions. MNTB neurons innervated by calyces with simple morphologies (mainly digits) express strong short-term synaptic depression and a high incidence of spike failures after high-frequency stimulation. Conversely, MNTB neurons innervated by structurally complex calyces (digits and numerous bouton-like swellings) exhibit initial facilitation followed by slow depression and very few spike failures. Our results indicate that the calyx of Held-MNTB synapse is likely organized as a structural and functional continuum, in that correlated heterogeneities in calyx morphology and short-term plasticity serve as a filter for regulating the inhibition delivered to superior olive neurons during sound localization.

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Medial Superior Olivary Neurons Receive Surprisingly Few Excitatory and Inhibitory Inputs with Balanced Strength and Short-Term Dynamics

Cited by 108 publications

References 49 publications

Modeling Binaural Responses in the Auditory Brainstem to Electric Stimulation of the Auditory Nerve

Modeling Binaural Responses in the Auditory Brainstem to Electric Stimulation of the Auditory Nerve

Frequency-dependent interaural delays in the medial superior olive: implications for interaural cochlear delays

Morphological and Functional Continuum Underlying Heterogeneity in the Spiking Fidelity at the Calyx of Held SynapseIn Vitro

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