Type III excitability, slope sensitivity and coincidence detection

Meng, Xiangying; Huguet, Gemma; Rinzel, John

doi:10.3934/dcds.2012.32.2729

Cited by 88 publications

(110 citation statements)

References 35 publications

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“…Spikes were evoked either by crossings of a voltage threshold (v) or by a sufficiently fast rise in the membrane voltage over time (a slope threshold, dv/dt). Note that this slope threshold was an idealization of a mechanism underlying the phasic firing we observed in MSO neurons (and some of the LSO neurons) and also has been reported in other neurons of the auditory brainstem (22,23). The voltage (or slope) threshold for spike generation was set such that the variation of the output rate of the model neuron was maximized (Fig.…”

Section: Modeling Itd and Ild Sensitivity For Resonant And Nonresonantmentioning

confidence: 85%

Subthreshold resonance properties contribute to the efficient coding of auditory spatial cues

Remme

Donato

Mikiel-Hunter

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Neurons in the medial superior olive (MSO) and lateral superior olive (LSO) of the auditory brainstem code for sound-source location in the horizontal plane, extracting interaural time differences (ITDs) from the stimulus fine structure and interaural level differences (ILDs) from the stimulus envelope. Here, we demonstrate a postsynaptic gradient in temporal processing properties across the presumed tonotopic axis; neurons in the MSO and the low-frequency limb of the LSO exhibit fast intrinsic electrical resonances and low input impedances, consistent with their processing of ITDs in the temporal fine structure. Neurons in the high-frequency limb of the LSO show low-pass electrical properties, indicating they are better suited to extracting information from the slower, modulated envelopes of sounds. Using a modeling approach, we assess ITD and ILD sensitivity of the neural filters to natural sounds, demonstrating that the transformation in temporal processing along the tonotopic axis contributes to efficient extraction of auditory spatial cues.auditory system | superior olivary nucleus | spatial listening T he auditory system analyzes sounds over different time scales to extract ecologically relevant information, including the identity and location of a sound source ( Fig. 1A; also see ref. 1). In particular, sensitivity to rapidly fluctuating signals in the temporal fine structure (TFS; the sound-pressure waveform) of sounds enables the extraction of spatial information in the form of interaural time differences (ITDs), i.e., the time difference in the arrival of the stimulus to both ears. For frequencies below about 1,500 Hz, human listeners can discriminate ITDs of just a few tens of microseconds (2-4), corresponding to a spatial resolution of about two degrees for sources located to the front. Such exquisite sensitivity relies on the ability of cochlear hair cells to generate action potentials in auditory nerve fibers that are phase-locked to the instantaneous sound-pressure waveform at each eardrum (Fig. 1A, bottom right). Phase-locking to the TFS in nerve fibers extends to at least 4 kHz in many mammalian species but starts to degrade from about 1 kHz as the result of low-pass filtering by the sensory hair cells (5). Postsynaptic specializations in subsequent stages of the ascending pathway-such as the cochlear nucleus-may improve temporal locking of action potentials to the TFS, at least for frequencies below 1 kHz (6). Phase-locked excitatory (and potentially inhibitory) inputs from each ear ("EE" input) ultimately converge on neurons in the medial superior olive (MSO) of the brainstem, where ITDs are explicitly computed (Fig. 1B).For sounds above a few kilohertz in frequency, differences in the intensity of the sound at each ear (interaural level differences, ILDs)-generated by the head "shadowing" the ear further from the source-become increasingly important as localization cues. Although phase-locking of action potentials to the TFS typically is absent in this frequency range, the spiking activity do...

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Section: Modeling Itd and Ild Sensitivity For Resonant And Nonresonantmentioning

confidence: 85%

Subthreshold resonance properties contribute to the efficient coding of auditory spatial cues

Remme

Donato

Mikiel-Hunter

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…In the auditory brain stem, low-threshold potassium current (K lt ) has the kinetics to induce resonant frequencies as high as the ones measured in NA neurons (Meng et al 2012;Svirskis 2004). Onset firing in response to a step current, the hallmark of K lt currents (Oertel 1999), was reported in only 17% of NA neurons (Fukui and Ohmori 2003), suggesting that K lt might not be expressed at sufficient levels to suppress firing in a majority of NA cells.…”

Section: Discussionmentioning

confidence: 99%

Emergence of band-pass filtering through adaptive spiking in the owl's cochlear nucleus

Fontaine

MacLeod

Lubejko

et al. 2014

Journal of Neurophysiology

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In the visual, auditory, and electrosensory modalities, stimuli are defined by first-and second-order attributes. The fast time-pressure signal of a sound, a first-order attribute, is important, for instance, in sound localization and pitch perception, while its slow amplitude-modulated envelope, a second-order attribute, can be used for sound recognition. Ascending the auditory pathway from ear to midbrain, neurons increasingly show a preference for the envelope and are most sensitive to particular envelope modulation frequencies, a tuning considered important for encoding sound identity. The level at which this tuning property emerges along the pathway varies across species, and the mechanism of how this occurs is a matter of debate. In this paper, we target the transition between auditory nerve fibers and the cochlear nucleus angularis (NA). While the owl's auditory nerve fibers simultaneously encode the fast and slow attributes of a sound, one synapse further, NA neurons encode the envelope more efficiently than the auditory nerve. Using in vivo and in vitro electrophysiology and computational analysis, we show that a single-cell mechanism inducing spike threshold adaptation can explain the difference in neural filtering between the two areas. We show that spike threshold adaptation can explain the increased selectivity to modulation frequency, as input level increases in NA. These results demonstrate that a spike generation nonlinearity can modulate the tuning to second-order stimulus features, without invoking network or synaptic mechanisms.band-pass filtering; envelope encoding; cochlear nucleus; threshold adaptation SENSORY SYSTEMS HAVE EVOLVED to efficiently represent the statistics of natural stimuli (Barlow 1961). In the auditory system, the cochlea decomposes sound into narrow frequency channels. The output of every cochlear channel can be characterized by its first-order attribute, the time-dependent pressure wave or fine-structure, and second-order attribute, the instantaneous amplitude or envelope (Attias and Schreiner

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“…When the KLT conductance is frozen, the model's resting membrane time constant is preserved, but the ability of the KLT current to rapidly repolarize the cell after an excitatory event is impaired (Day et al, 2008;Meng et al, 2012). We found that freezing the KLT dynamics slightly reduces the maximum amplitude of oscillations of the simulated neurophonic responses for all stimulus frequencies tested (compare red and black lines).…”

Section: High-frequency Oscillations: Necessity Of Fast Synaptic Kinementioning

confidence: 72%

A Model of the Medial Superior Olive Explains Spatiotemporal Features of Local Field Potentials

et al. 2014

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Local field potentials are important indicators of in vivo neural activity. Sustained, phase-locked, sound-evoked extracellular fields in the mammalian auditory brainstem, known as the auditory neurophonic, reflect the activity of neurons in the medial superior olive (MSO). We develop a biophysically based model of the neurophonic that accounts for features of in vivo extracellular recordings in the cat auditory brainstem. By making plausible idealizations regarding the spatial symmetry of MSO neurons and the temporal synchrony of their afferent inputs, we reduce the challenging problem of computing extracellular potentials in a 3D volume conductor to a onedimensional problem. We find that postsynaptic currents in bipolar MSO neuron models generate extracellular voltage responses that strikingly resemble in vivo recordings. Simulations reproduce distinctive spatiotemporal features of the in vivo neurophonic response to monaural pure tones: large oscillations (hundreds of microvolts to millivolts), broad spatial reach (millimeter scale), and a dipole-like spatial profile. We also explain how somatic inhibition and the relative timing of bilateral excitation may shape the spatial profile of the neurophonic. We observe in simulations, and find supporting evidence in in vivo data, that coincident excitatory inputs on both dendrites lead to a drastically reduced spatial reach of the neurophonic. This outcome surprises because coincident inputs are thought to evoke maximal firing rates in MSO neurons, and it reconciles previously puzzling evoked potential results in humans and animals. The success of our model, which has no axon or spike-generating sodium currents, suggests that MSO spikes do not contribute appreciably to the neurophonic.

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Type III excitability, slope sensitivity and coincidence detection

Cited by 88 publications

References 35 publications

Subthreshold resonance properties contribute to the efficient coding of auditory spatial cues

Subthreshold resonance properties contribute to the efficient coding of auditory spatial cues

Emergence of band-pass filtering through adaptive spiking in the owl's cochlear nucleus

A Model of the Medial Superior Olive Explains Spatiotemporal Features of Local Field Potentials

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