Author response: Theoretical relation between axon initial segment geometry and excitability

Goethals, Sarah; Brette, Romain

doi:10.7554/elife.53432.sa2

2020

DOI: 10.7554/elife.53432.sa2

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Author response: Theoretical relation between axon initial segment geometry and excitability

Sarah Goethals

Romain Brette

Abstract: In most vertebrate neurons, action potentials are triggered at the distal end of the axon initial segment (AIS). Both position and length of the AIS vary across and within neuron types, with activity, development and pathology. What is the impact of AIS geometry on excitability? Direct empirical assessment has proven difficult because of the many potential confounding factors. Here we carried a principled theoretical analysis to answer this question. We provide a simple formula relating AIS geometry and sodium… Show more

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Cited by 3 publications

References 77 publications

(157 reference statements)

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Brief sensory deprivation triggers cell type-specific structural and functional plasticity in olfactory bulb neurons

Galliano

Hahn

Browne

et al. 2020

Preprint

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Can alterations in experience trigger different plastic modifications in neuronal structure and function, and if so, how do they integrate at the cellular level? To address this question, we interrogated circuitry in the mouse olfactory bulb responsible for the earliest steps in odour processing. We induced experience-dependent plasticity in mice by blocking one nostril for a day, a minimally-invasive manipulation which leaves the sensory organ undamaged and is akin to the natural transient blockage suffered during common mild rhinal infections. We found that such brief sensory deprivation produced structural and functional plasticity in one highly specialised bulbar cell type: axon-bearing dopaminergic neurons in the glomerular layer. After 24h naris occlusion, the axon initial segment (AIS) in bulbar dopaminergic neurons became significantly shorter, a structural modification that was also associated with a decrease in intrinsic excitability. These effects were specific to the AIS-positive dopaminergic subpopulation, because no experience-dependent alterations in intrinsic excitability were observed in AIS-negative dopaminergic cells. Moreover, 24h naris occlusion produced no structural changes at the AIS of bulbar excitatory neuronsmitral/tufted and external tufted cells -nor did it alter their intrinsic excitability. By targeting excitability in one specialised dopaminergic subpopulation, experience-dependent plasticity in early olfactory networks might act to fine-tune sensory processing in the face of continually fluctuating inputs.

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Brief sensory deprivation triggers cell type-specific structural and functional plasticity in olfactory bulb neurons

Galliano

Hahn

Browne

et al. 2020

Preprint

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Neural excitability increases with axonal resistance between soma and axon initial segment

Fekete

Ankri

Brette

et al. 2020

Preprint

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The position of the axon initial segment (AIS) is thought to play a critical role in neuronal excitability. In particular, empirical studies have found correlations between a distal shift in AIS position and a reduction of excitability. Yet, theoretical work has suggested that the neuron should become more excitable as the distance between soma and AIS is increased, because of increased electrical isolation. Specifically, resistive coupling theory predicts that the action potential (AP) threshold decreases with the logarithm of the axial resistance (Ra) between the middle of the AIS and the soma. However, no direct experimental evidence has been provided so far to support this theoretical prediction. We therefore examined how changes in Ra at the axon hillock impact the voltage threshold (Vth) of the somatic AP in L5 pyramidal neurons. Increasing Ra by mechanically pinching the axon between the soma and the AIS was found to lower the spike threshold by ~6 mV. Conversely, decreasing Ra by replacing a weakly mobile ion (gluconate) by a highly mobile ion (chloride) elevated the spike threshold. All Ra-dependent changes in spike threshold could be reproduced in a Hodgkin-Huxley compartmental model. We conclude that in L5 pyramidal neurons, excitability increases with axial resistance, and therefore with a distal shift of the AIS.

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Ex vivofunctional characterization of mouse olfactory bulb projection neurons reveals a heterogenous continuum

Gadiwalla,

Guillaume,

Huang

et al. 2024

Preprint

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Mitral and tufted cells in the olfactory bulb (OB) act as an input convergence hub and transmit information to higher olfactory areas. Since first characterized, they have been classed as distinct projection neurons based on size and location: laminarly-arranged mitral cells with a diameter larger than 20μm in the mitral layer (ML), and smaller tufted cells spread across both the ML and external plexiform layer (EPL). Recent in vivo work has shown that these neurons encode complementary olfactory information, akin to parallel channels in other sensory systems. Yet, many ex vivo studies still collapse them into a single class, mitral/tufted, when describing their physiological properties and impact on circuit function. Using immunohistochemistry and whole-cell patch clamp electrophysiology in fixed or acute slices from adult mice, we attempted to align in vivo and ex vivo data and test a soma size-based classifier of OB projection neurons using passive and intrinsic firing properties. We found that there is no clear separation between cell types based on passive or active properties. Rather, there is a heterogeneous continuum with three loosely clustered subgroups: EPL tufted cells, putative tufted cells, and putative mitral cells in the ML. These findings illustrate the large functional heterogeneity present within the OB projection neurons and complement existing literature highlighting how heterogeneity in sensory systems is preponderant and possibly used in the OB to decode complex olfactory information.

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Author response: Theoretical relation between axon initial segment geometry and excitability

Cited by 3 publications

References 77 publications

Brief sensory deprivation triggers cell type-specific structural and functional plasticity in olfactory bulb neurons

Brief sensory deprivation triggers cell type-specific structural and functional plasticity in olfactory bulb neurons

Neural excitability increases with axonal resistance between soma and axon initial segment

Ex vivofunctional characterization of mouse olfactory bulb projection neurons reveals a heterogenous continuum

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