Cellular Computations Underlying Detection of Gaps in Sounds and Lateralizing Sound Sources

Oertel, Donata; Cao, Xiao-Jie; Ison, James R.; Allen, Paul D.

doi:10.1016/j.tins.2017.08.001

Cited by 14 publications

(11 citation statements)

References 107 publications

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“…The threshold for detecting brief silent gaps in noise provides a valuable analytical tool to measure temporal resolution in auditory processing (Moore, 1997). Gaps as short as 2–3 ms can be detected by humans (Penner, 1977) and rodents (Ison, 1982) and it has been suggested that to detect a 3-ms gap, auditory neurons need to encode onsets and offsets of sounds with a temporal acuity of ∼1 ms (Oertel et al, 2017). Gap-in-noise stimuli have also proven very helpful in determining the ability of the auditory system to encode sound offsets as a parameter independent of sound onsets (Pratt et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

Slow NMDA-Mediated Excitation Accelerates Offset-Response Latencies Generated via a Post-Inhibitory Rebound Mechanism

Rajaram

Kaltenbach

Fischl

et al. 2019

eNeuro

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In neural circuits, action potentials (spikes) are conventionally caused by excitatory inputs whereas inhibitory inputs reduce or modulate neuronal excitability. We previously showed that neurons in the superior paraolivary nucleus (SPN) require solely synaptic inhibition to generate their hallmark offset response, a burst of spikes at the end of a sound stimulus, via a post-inhibitory rebound mechanism. In addition SPN neurons receive excitatory inputs, but their functional significance is not yet known. Here we used mice of both sexes to demonstrate that in SPN neurons, the classical roles for excitation and inhibition are switched, with inhibitory inputs driving spike firing and excitatory inputs modulating this response. Hodgkin–Huxley modeling suggests that a slow, NMDA receptor (NMDAR)-mediated excitation would accelerate the offset response. We find corroborating evidence from in vitro and in vivo recordings that lack of excitation prolonged offset-response latencies and rendered them more variable to changing sound intensity levels. Our results reveal an unsuspected function for slow excitation in improving the timing of post-inhibitory rebound firing even when the firing itself does not depend on excitation. This shows the auditory system employs highly specialized mechanisms to encode timing-sensitive features of sound offsets which are crucial for sound-duration encoding and have profound biological importance for encoding the temporal structure of speech.

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Section: Discussionmentioning

confidence: 99%

Slow NMDA-Mediated Excitation Accelerates Offset-Response Latencies Generated via a Post-Inhibitory Rebound Mechanism

Rajaram

Kaltenbach

Fischl

et al. 2019

eNeuro

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“…In the central nervous system of vertebrates, auditory brainstem neurons are highly specialized to rapidly encode temporal acoustic information (1,2), which is critical for sound localization, escaping danger, and signal extraction from complex acoustic environments (3)(4)(5). These neurons accurately encode acoustic information by generating rapid and temporally precise action potentials (APs) for delivering and refining acoustic cues with a precision in the order of tens of microseconds (6,7).…”

Section: Introductionmentioning

confidence: 99%

“…The bushy cells in mammals participate in binaural temporally precise processing pathways and are further subdivided into three distinct subtypes: large spherical (LSBC), small spherical (SSBC), and globular bushy cells (GBC) (2,11). However, the LSBC and SSBC can be distinguished clearly by sizes in cats (12) but not in the other mammals such as guinea pigs and mice (11,13).…”

Section: Introductionmentioning

confidence: 99%

Differential contributions of voltage-gated potassium channel subunits in enhancing temporal coding in the bushy cells of the ventral cochlear nucleus

Zhang

Xie

et al. 2021

Journal of Neurophysiology

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Temporal coding precision of bushy cells in the ventral cochlear nucleus (VCN), critical for sound localization and communication, depends on the generation of rapid and temporally precise action potentials (APs). Voltage-gated potassium (Kv) channels are critically involved in this. The bushy cells in rat VCN express Kv1.1, 1.2, 1.3, 1.6, 3.1, 4.2 and 4.3 subunits. The Kv1.1 subunit contributes to the generation of a temporally precise single AP. However, the understanding of the functions of other Kv subunits expressed in the bushy cells is limited. Here, we investigated the functional diversity of Kv subunits concerning their contributions to temporal coding. We characterized the electrophysiological properties of the Kv channels with different subunits using whole-cell patch-clamp recording and pharmacological methods. The neuronal firing pattern changed from single to multiple APs only when the Kv1.1 subunit was blocked. The Kv subunits, including the Kv1.1, 1.2, 1.6 or 3.1, were involved in enhancing temporal coding by lowering membrane excitability, shortening AP latencies, reducing jitter and regulating AP kinetics. Meanwhile, all the Kv subunits contributed to rapid repolarization and sharpening peaks by narrowing half-width and accelerating fall rate, while the Kv1.1 subunit also affected the depolarization of AP. The Kv1.1, 1.2 and 1.6 subunits endowed bushy cells with a rapid time constant and a low input resistance of membrane for enhancing spike timing precision. The present results indicate that the Kv channels differentially affect intrinsic membrane properties to optimize the generation of rapid and reliable APs for temporal coding.

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“…Octopus cells are topologically arranged in frequency-ordered laminae and locally wired to bundles of ANFs. The wiring patterns' scheme constitutes their temporal receptive fields (TRFs) (Oertel et al, 2017;Spencer et al, 2018). Octopus cells latency-phase rectify space-time trajectories in their TRFs (Golding and Oertel, 2012;McGinley et al, 2012).…”

Section: Methodsmentioning

confidence: 99%

Periodicity Pitch Perception

Klefenz

Harczos

2020

Front. Neurosci.

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This study presents a computational model to reproduce the biological dynamics of "listening to music." A biologically plausible model of periodicity pitch detection is proposed and simulated. Periodicity pitch is computed across a range of the auditory spectrum. Periodicity pitch is detected from subsets of activated auditory nerve fibers (ANFs). These activate connected model octopus cells, which trigger model neurons detecting onsets and offsets; thence model interval-tuned neurons are innervated at the right interval times; and finally, a set of common interval-detecting neurons indicate pitch. Octopus cells rhythmically spike with the pitch periodicity of the sound. Batteries of interval-tuned neurons stopwatch-like measure the inter-spike intervals of the octopus cells by coding interval durations as first spike latencies (FSLs). The FSL-triggered spikes synchronously coincide through a monolayer spiking neural network at the corresponding receiver pitch neurons.

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Cellular Computations Underlying Detection of Gaps in Sounds and Lateralizing Sound Sources

Cited by 14 publications

References 107 publications

Slow NMDA-Mediated Excitation Accelerates Offset-Response Latencies Generated via a Post-Inhibitory Rebound Mechanism

Slow NMDA-Mediated Excitation Accelerates Offset-Response Latencies Generated via a Post-Inhibitory Rebound Mechanism

Differential contributions of voltage-gated potassium channel subunits in enhancing temporal coding in the bushy cells of the ventral cochlear nucleus

Periodicity Pitch Perception

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