Action Potential Generation in an Anatomically Constrained Model of Medial Superior Olive Axons

Lehnert, Simon; Ford, Marc C.; Alexandrova, Olga; Hellmundt, Franziska; Felmy, Felix; Grothe, Benedikt; Leibold, Christian

doi:10.1523/jneurosci.4038-13.2014

Cited by 35 publications

(49 citation statements)

References 65 publications

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“…We will always use α = 0.01 in this study. This 137 assumption is plausible for cells with input regions that are much larger than 138 spike-generating regions, and is consistent with previous models of auditory coincidence 139 detector neurons [24,38]. 140 We find the axial conductance (g c ) by expressing it in terms of input resistance and 141 the coupling coefficients.…”

Section: Introductionsupporting

confidence: 80%

Soma-axon coupling configurations that enhance neuronal coincidence detection

Goldwyn

Remme

Rinzel

2018

Preprint

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Coincidence detector neurons transmit timing information by responding preferentially to concurrent synaptic inputs. Principal cells of the medial superior olive (MSO) in the mammalian auditory brainstem are superb coincidence detectors. They encode sound source location with high temporal precision, distinguishing submillisecond timing differences among inputs. We investigate computationally how dynamic coupling between the "input" region (soma and dendrite) and the spike-generating "output" region (axon and axon initial segment) can enhance coincidence detection in MSO neurons. To do this, we formulate a two-compartment neuron model and characterize extensively coincidence detection sensitivity throughout a parameter space of coupling configurations. We focus on the interaction between coupling configuration and two currents that provide dynamic, voltage-gated, negative feedback in subthreshold voltage range: sodium current with rapid inactivation and low-threshold potassium current, I KLT . These currents reduce synaptic summation and can prevent spike generation unless inputs arrive with near simultaneity. We show that strong soma-to-axon coupling promotes the negative feedback effects of sodium inactivation and is, therefore, advantageous for coincidence detection. Furthermore, the "feedforward" combination of strong soma-to-axon coupling and weak axon-to-soma coupling enables spikes to be generated efficiently (few sodium channels needed) and with rapid recovery that enhances high-frequency coincidence detection. These observations detail the functional benefit of the strongly feedforward configuration that has been observed in physiological studies of MSO neurons. We find that I KLT further enhances coincidence detection sensitivity, but with effects that depend on coupling configuration. For instance, in weakly-coupled models, I KLT in the spike-generator compartment enhances coincidence detection more effectively than I KLT in the input compartment. By using a minimal model of soma-to-axon coupling, we connect structure, dynamics, and computation. Here, we consider the particular case of MSO coincidence detectors. In principle, our method for creating and exploring a parameter space of two-compartment models can be applied to other neurons. PLOS1/30 Author summaryBrain cells (neurons) are spatially extended structures. The locations at which neurons receive inputs and generate outputs are often distinct. We formulate and study a minimal mathematical model that describes the dynamical coupling between the input and output regions of a neuron. We construct our model to reflect known properties of neurons in the auditory brainstem that play an important role in our ability to locate sound sources. These neurons are known as "coincidence detectors" because they are most likely to respond when they receive simultaneous inputs. We use simulations to explore coincidence detection sensitivity throughout the parameter space of input-output coupling and to identify the coupling configurations that are best for neu...

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Section: Introductionsupporting

confidence: 80%

Soma-axon coupling configurations that enhance neuronal coincidence detection

Goldwyn

Remme

Rinzel

2018

Preprint

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“…VNTB neurons typically have high R input (>300 MΩ) and exhibit a large voltage drop with the small current steps (Sinclair JL, unpublished observations). In contrast, mouse MSO neurons shared a low R input (<20 MΩ by P21) similar to age-matched gerbils (∼10 MΩ; Lehnert et al 2014; Magnusson et al 2005). …”

Section: Discussionmentioning

confidence: 89%

“…The reduced excitability suppresses action potential responses to temporally distributed inputs and limits dendritic filtering (Lehnert et al 2014; Mathews et al 2010; Scott et al 2005). The difference in amplitudes of low-voltage-activated K v 1-mediated currents in response to perithreshold depolarizations is between ∼1 nA in the mouse (present study) and ∼4 nA in the age-matched gerbil (Scott et al 2005).…”

Section: Discussionmentioning

confidence: 99%

Physiology and anatomy of neurons in the medial superior olive of the mouse

Fischl

Burger

Schmidt-Pauly

et al. 2016

Journal of Neurophysiology

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The medial superior olive (MSO) is an important brain center that computes sound location by comparing small differences in arrival time at the two ears. The MSO is investigated for its specializations for processing with extreme temporal precision. In mice, the MSO is small and difficult to study; thus utilization of genetic methods in MSO studies has been lacking. We present the first comprehensive study of the murine MSO and show that most features are consistent with more heavily investigated species.

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“…To measure these parameters, the injected, short EPSC-approximating current was scaled to evoke action potentials in ϳ40% of the trials (Fig. 7A) (Ammer et al 2012;Cathala et al 2003;Fricker and Miles 2000;Lehnert et al 2014). As in the DNLL (Ammer et al 2012), action-potential latency and jitter decreased significantly between P9 (n ϭ 11) and P25 (n ϭ 10; latency P9: 1.15 Ϯ 0.05 ms, P25: 1.00 Ϯ 0.04 ms, P Ͻ 0.05; jitter P9: 0.17 Ϯ 0.02 ms, P25: 0.12 Ϯ 0.01 ms, P Ͻ 0.05; Fig.…”

Section: Resultsmentioning

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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Action Potential Generation in an Anatomically Constrained Model of Medial Superior Olive Axons

Cited by 35 publications

References 65 publications

Soma-axon coupling configurations that enhance neuronal coincidence detection

Soma-axon coupling configurations that enhance neuronal coincidence detection

Physiology and anatomy of neurons in the medial superior olive of the mouse

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

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