Glycinergic inhibition tunes coincidence detection in the auditory brainstem

Myoga, Michael H.; Lehnert, Simon; Leibold, Christian; Felmy, Felix; Grothe, Benedikt

doi:10.1038/ncomms4790

Cited by 90 publications

(104 citation statements)

References 59 publications

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“…Studies of the FFR binaural interaction component indicate that binaural interaction is a non-linear process (for a review, see Wilson and Krishnan 2005). In addition, precisely timed neural inhibition (Brand et al 2002;Myoga et al 2014) and binaural excitatory/inhibitory response properties of neurons (e.g., Langford 1984) may also be contributing factors to these FFR amplitude differences.…”

Section: Neurophonics and Binaural Processingmentioning

confidence: 98%

Neural Correlates of the Binaural Masking Level Difference in Human Frequency-Following Responses

Clinard

Hodgson

Scherer

2016

JARO

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The binaural masking level difference (BMLD) is an auditory phenomenon where binaural tone-in-noise detection is improved when the phase of either signal or noise is inverted in one of the ears (SN or SN, respectively), relative to detection when signal and noise are in identical phase at each ear (SN). Processing related to BMLDs and interaural time differences has been confirmed in the auditory brainstem of non-human mammals; in the human auditory brainstem, phase-locked neural responses elicited by BMLD stimuli have not been systematically examined across signal-to-noise ratio. Behavioral and physiological testing was performed in three binaural stimulus conditions: SN, SN, and SN. BMLDs at 500 Hz were obtained from 14 young, normal-hearing adults (ages 21-26). Physiological BMLDs used the frequency-following response (FFR), a scalp-recorded auditory evoked potential dependent on sustained phase-locked neural activity; FFR tone-in-noise detection thresholds were used to calculate physiological BMLDs. FFR BMLDs were significantly smaller (poorer) than behavioral BMLDs, and FFR BMLDs did not reflect a physiological release from masking, on average. Raw FFR amplitude showed substantial reductions in the SN condition relative to SN and SN conditions, consistent with negative effects of phase summation from left and right ear FFRs. FFR amplitude differences between stimulus conditions (e.g., SN amplitude-SN amplitude) were significantly predictive of behavioral SN BMLDs; individuals with larger amplitude differences had larger (better) behavioral B MLDs and individuals with smaller amplitude differences had smaller (poorer) behavioral B MLDs. These data indicate a role for sustained phase-locked neural activity in BMLDs of humans and are the first to show predictive relationships between behavioral BMLDs and human brainstem responses.

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Section: Neurophonics and Binaural Processingmentioning

confidence: 98%

Neural Correlates of the Binaural Masking Level Difference in Human Frequency-Following Responses

Clinard

Hodgson

Scherer

2016

JARO

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“…It follows that a preceding of inhibition relative to excitation might be of crucial relevance for the computation of ITDs (5,26). Although the exact way the different MSO inputs are integrated to realize ITD resolution of about 30 μs on a single cell level is still highly controversial (22,(62)(63)(64), there is evidence for extraordinary temporal precision of the glycinergic MNTB input to the MSO including an experience-driven developmental selection of very few but strong inputs that show fast inhibitory postsynaptic currents (IPSCs)/inhibitory postsynaptic potentials (IPSPs). Our findings of morphological and physiological specializations in the inhibitory pathway strongly corroborate that not only fast, but precisely timed inhibition to the MSO is of central importance for the ITD processing mechanism.…”

Section: Discussionmentioning

confidence: 99%

Input timing for spatial processing is precisely tuned via constant synaptic delays and myelination patterns in the auditory brainstem

Stange-Marten¹,

Nabel²,

Sinclair³

et al. 2017

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

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Precise timing of synaptic inputs is a fundamental principle of neural circuit processing. The temporal precision of postsynaptic input integration is known to vary with the computational requirements of a circuit, yet how the timing of action potentials is tuned presynaptically to match these processing demands is not well understood. In particular, action potential timing is shaped by the axonal conduction velocity and the duration of synaptic transmission delays within a pathway. However, it is not known to what extent these factors are adapted to the functional constraints of the respective circuit. Here, we report the finding of activity-invariant synaptic transmission delays as a functional adaptation for input timing adjustment in a brainstem sound localization circuit. We compared axonal and synaptic properties of the same pathway between two species with dissimilar timing requirements (gerbil and mouse): In gerbils (like humans), neuronal processing of sound source location requires exceptionally high input precision in the range of microseconds, but not in mice. Activityinvariant synaptic transmission and conduction delays were present exclusively in fast conducting axons of gerbils that also exhibited unusual structural adaptations in axon myelination for increased conduction velocity. In contrast, synaptic transmission delays in mice varied depending on activity levels, and axonal myelination and conduction velocity exhibited no adaptations. Thus, the specializations in gerbils and their absence in mice suggest an optimization of axonal and synaptic properties to the specific demands of sound localization. These findings significantly advance our understanding of structural and functional adaptations for circuit processing. myelination | synaptic transmission delay | sound localization | circuit processing | input timing T emporal integration of bioelectrical signals via chemical synapses is fundamental to neuronal computations. During circuit processing, neuronal information transfer via action potentials is controlled by exact differences in the occurrence between excitatory and inhibitory inputs (1-5). The arrival time of inputs within circuits in turn is largely shaped by the conduction delay of action potentials along the axons and during synaptic transmission. During ongoing activity, the transmission delays of chemical synapses generally increase in the range of hundreds of microseconds due to short-term adaptations (6-9). However, because temporal integration on postsynaptic neurons usually operates on time scales in the range of milliseconds or even longer (10, 11), sluggishness arising from synaptic mechanisms and axonal conductance is negligible for most of these computations. There are, however, some essential neuronal processing tasks that challenge the temporal precision of our nervous system. For instance, weakly electric fish detect miniature changes in the frequency of a constant electrical field. The neuronal circuits in these animals use electrical instead of chemical synapses in t...

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“…From the comparison of these developmental profiles (Ammer et al 2012;Chirila et al 2007;Magnusson et al 2005;Scott et al 2005), it is tempting to speculate that the time course of refinement is related to the complexity of the integrational task of a neuron. Neurons in the medial superior olive integrate excitation and inhibition with active conductances with submillisecond precision (Golding and Oertel 2012;Grothe 2003;Myoga et al 2014). Although the integration of excitation and inhibition is also of functional relevance in the dorsal nucleus of the lateral lemniscus, the timing is less exquisite, as it operates within tens of milliseconds (Burger and Pollak 2001;Pecka et al 2007;Siveke et al 2006;Yang and Pollak 1994).…”

Section: Discussionmentioning

confidence: 99%

Development and modulation of intrinsic membrane properties control the temporal precision of auditory brain stem neurons

Franzen

Gleiss

Berger

et al. 2015

Journal of Neurophysiology

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Franzen DL, Gleiss SA, Berger C, Kümpfbeck FS, Ammer JJ, Felmy F. Development and modulation of intrinsic membrane properties control the temporal precision of auditory brain stem neurons. J Neurophysiol 113: 524 -536, 2015. First published October 29, 2014 doi:10.1152/jn.00601.2014.-Passive and active membrane properties determine the voltage responses of neurons. Within the auditory brain stem, refinements in these intrinsic properties during late postnatal development usually generate short integration times and precise action-potential generation. This developmentally acquired temporal precision is crucial for auditory signal processing. How the interactions of these intrinsic properties develop in concert to enable auditory neurons to transfer information with high temporal precision has not yet been elucidated in detail. Here, we show how the developmental interaction of intrinsic membrane parameters generates high firing precision. We performed in vitro recordings from neurons of postnatal days 9 -28 in the ventral nucleus of the lateral lemniscus of Mongolian gerbils, an auditory brain stem structure that converts excitatory to inhibitory information with high temporal precision. During this developmental period, the input resistance and capacitance decrease, and action potentials acquire faster kinetics and enhanced precision. Depending on the stimulation time course, the input resistance and capacitance contribute differentially to action-potential thresholds. The decrease in input resistance, however, is sufficient to explain the enhanced action-potential precision. Alterations in passive membrane properties also interact with a developmental change in potassium currents to generate the emergence of the mature firing pattern, characteristic of coincidence-detector neurons. Cholinergic receptormediated depolarizations further modulate this intrinsic excitability profile by eliciting changes in the threshold and firing pattern, irrespective of the developmental stage. Thus our findings reveal how intrinsic membrane properties interact developmentally to promote temporally precise information processing.ventral nucleus of the lateral lemniscus; postnatal development; neuronal excitability; cholinergic modulation THE ABILITY OF A NEURON TO generate action potentials with high temporal precision depends on the interaction of passive and active membrane properties (Ammer et al.

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Glycinergic inhibition tunes coincidence detection in the auditory brainstem

Cited by 90 publications

References 59 publications

Neural Correlates of the Binaural Masking Level Difference in Human Frequency-Following Responses

Neural Correlates of the Binaural Masking Level Difference in Human Frequency-Following Responses

Input timing for spatial processing is precisely tuned via constant synaptic delays and myelination patterns in the auditory brainstem

Development and modulation of intrinsic membrane properties control the temporal precision of auditory brain stem neurons

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