An investigation of dendritic delay in octopus cells of the mammalian cochlear nucleus

Martin J Spencer,Anthony N Burkitt,Ian C Bruce,Hamish Meffin,David B Grayden

doi:10.3389/fncom.2012.00083

Martin J Spencer, Anthony N Burkitt + Show 3 more

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https://doi.org/10.3389/fncom.2012.00083

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Abstract

Octopus cells, located in the mammalian auditory brainstem, receive their excitatory synaptic input exclusively from auditory nerve fibers (ANFs). They respond with accurately timed spikes but are broadly tuned for sound frequency. Since the representation of information in the auditory nerve is well understood, it is possible to pose a number of questions about the relationship between the intrinsic electrophysiology, dendritic morphology, synaptic connectivity, and the ultimate functional role of octopus cells in the brainstem. This study employed a multi-compartmental Hodgkin-Huxley model to determine whether dendritic delay in octopus cells improves synaptic input coincidence detection in octopus cells by compensating for the cochlear traveling wave delay. The propagation time of post-synaptic potentials from synapse to soma was investigated. We found that the total dendritic delay was approximately 0.275 ms. It was observed that low-threshold potassium channels in the dendrites reduce the amplitude dependence of the dendritic delay of post-synaptic potentials. As our hypothesis predicted, the model was most sensitive to acoustic onset events, such as the glottal pulses in speech when the synaptic inputs were arranged such that the model's dendritic delay compensated for the cochlear traveling wave delay across the ANFs. The range of sound frequency input from ANFs was also investigated. The results suggested that input to octopus cells is dominated by high frequency ANFs.

Highlights

An important problem in neuroscience is to understand how neural function and processing are related to properties of the neuron, such as intrinsic electrophysiology, dendritic morphology, and patterns of synaptic innervation (Bock et al, 2011; Briggman et al, 2011; Seung, 2011)
The total synaptic drive was maintained by increasing the number of auditory nerve fibers (ANFs) by 25% to 375
Previous Hodgkin-Huxley computational models (Cai et al, 1997; Kipke and Levy, 1997; Levy and Kipke, 1997, 1998; Cai et al, 2000; Hemmert et al, 2005; McGinley et al, 2005) and two simplified models (Kalluri and Delgutte, 2003a,b) have made a number of contributions to the understanding of the behavior of octopus cells. These include a re-creation of the onset response, entrainment to amplitude modulated tones, and a dependence of the spike threshold upon the rate of change in the membrane potential

Summary

Introduction

An important problem in neuroscience is to understand how neural function and processing are related to properties of the neuron, such as intrinsic electrophysiology, dendritic morphology, and patterns of synaptic innervation (Bock et al, 2011; Briggman et al, 2011; Seung, 2011). Octopus cells, located within the cochlear nucleus of mammals (Harrison and Irving, 1966; Osen, 1969), are known to respond with finely timed action potentials to acoustic onset events, such as the glottal pulses in speech (Godfrey et al, 1975; Rhode and Smith, 1986; Rhode, 1998). These sounds are characteristic of animal vocalizations, including speech and some environmental noise. This raises the question of how octopus cells can respond with precise timing to broadband peaks in the temporal sound envelope, given that their input is temporally diffuse

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Conclusion