Synaptic Strengths Dominate Phasing of Motor Circuit: Intrinsic Conductances of Neuron Types Need Not Vary across Animals

Günay, Cengiz; Doloc-Mihu, Anca; Lamb, Damon G.; Calabrese, Ronald L.

doi:10.1523/eneuro.0417-18.2019

Cited by 4 publications

(4 citation statements)

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“…Variability of intrinsic currents in STG neurons may be compensated by cell-type-specific co-regulation of different voltage-gated channels (Khorkova and Golowasch, 2007;Schulz et al, 2007;Temporal et al, 2012;Tran et al, 2019), but it is not known to which degree synaptic currents may be co-regulated. Variability of synaptic currents could be compensated for by variability in intrinsic currents, as has been suggested for the leech heartbeat system (Gunay et al, 2019), and as is implicit in theoretical work that shows similar circuit activity with different combinations of intrinsic and synaptic current levels (Prinz et al, 2004b;Onasch and Gjorgjieva, 2020). Alternatively, compensatory co-regulation of intrinsic currents could lead to consistent neuronal excitability on its own, and variability of synaptic trajectory then must be constrained to allow for consistent phases.…”

Section: Variability and Co-regulationmentioning

confidence: 97%

“…Synaptic currents also vary substantially across individuals and their magnitude is correlated with relative timing of the burst onset of the postsynaptic neuron ( Goaillard et al, 2009 ). In theoretical work, the magnitude of synaptic currents has been varied and tuned alongside voltage-gated conductances to show which combinations and possible mechanisms give rise to similar activity ( Prinz et al, 2004b ; O’Leary et al, 2014 ), and it has been suggested that the relative synaptic strengths must be different in individual animals to produce observed activity phases ( Günay et al, 2019 ). However, it is unknown whether synaptic currents co-vary with individual voltage-gated currents in a correlated manner to compensate for variability in intrinsic neuronal excitability.…”

Section: Introductionmentioning

confidence: 99%

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Inter-Animal Variability in Activity Phase Is Constrained by Synaptic Dynamics in an Oscillatory Network

Anwar¹,

Martínez²,

Bucher³

et al. 2022

eNeuro

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The levels of voltage-gated and synaptic currents in the same neuron type can vary substantially across individuals. Yet, the phase relationships between neurons in oscillatory circuits are often maintained, even in the face of varying oscillation frequencies. We examined whether synaptic and intrinsic currents are matched to maintain constant activity phases across preparations, using the lateral pyloric (LP) neuron of the stomatogastric ganglion (STG) of the crab, Cancer borealis . LP produces stable oscillatory bursts on release from inhibition, with an onset phase that is independent of oscillation frequency. We quantified the parameters that define the shape of the synaptic current inputs across preparations and found no linear correlations with voltage-gated currents. However, several synaptic parameters were correlated with oscillation period and burst onset phase, suggesting they may play a role in phase maintenance. We used dynamic clamp to apply artificial synaptic inputs and found that those synaptic parameters correlated with phase and period were ineffective in influencing burst onset. Instead, parameters that showed the least variability across preparations had the greatest influence. Thus, parameters that influence circuit phasing are constrained across individuals, while those that have little effect simply co-vary with phase and frequency.

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Section: Variability and Co-regulationmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Inter-Animal Variability in Activity Phase Is Constrained by Synaptic Dynamics in an Oscillatory Network

Anwar¹,

Martínez²,

Bucher³

et al. 2022

eNeuro

View full text Add to dashboard Cite

show abstract

“…Variability of intrinsic currents in STG neurons may be compensated by cell-type-specific co-regulation of different voltage-gated channels (Khorkova and Golowasch, 2007;Schulz et al, 2007;Temporal et al, 2012;Tran et al, 2019), but it is not known to which degree synaptic currents may be co-regulated. Variability of synaptic currents could be compensated for by variability in intrinsic currents, as has been suggested for the leech heartbeat system (Gunay et al, 2019), and as is implicit in theoretical work that shows similar circuit activity with different combinations of intrinsic and synaptic current levels (Prinz et al, 2004a;Onasch and Gjorgjieva, 2020). Alternatively, compensatory co-regulation of intrinsic currents could lead to consistent neuronal excitability on its own, and variability of synaptic trajectory then must be constrained to allow for consistent phases.…”

Section: Variability and Co-regulationmentioning

confidence: 97%

Inter-animal variability in activity phase is constrained by synaptic dynamics in an oscillatory network

Anwar

Martínez

Bucher

et al. 2022

Preprint

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The levels of voltage-gated and synaptic currents in the same neuron type can vary substantially across individuals. Yet, the phase relationships between neurons in oscillatory circuits are often maintained, even in the face of varying oscillation frequencies. We examined whether synaptic and intrinsic currents are matched to maintain constant activity phases across preparations, using the lateral pyloric (LP) neuron of the stomatogastric ganglion of the crab, Cancer borealis. LP produces stable oscillatory bursts upon release from inhibition, with an onset phase that is independent of oscillation frequency. We quantified the parameters that define the shape of the synaptic current inputs across preparations and found no linear correlations with voltage-gated currents. However, several synaptic parameters were correlated with oscillation period and burst onset phase, suggesting they may play a role in phase maintenance. We used the dynamic clamp to apply artificial synaptic inputs and found that those synaptic parameters correlated with phase and period were ineffective in influencing burst onset. Instead, parameters that showed the least variability across preparations had the greatest influence. Thus, parameters that influence circuit phasing are constrained across individuals, while those that have little effect simply co-vary with phase and frequency.

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“…It is now well-established that multiple sets of maximal conductances of ion channels can produce very similar neuronal activity patterns in both individual neurons and circuits ( 1 – 10 ). Nonetheless, it is also clear that models of desired intrinsic properties are relatively rarely found by randomly sampling within a space of parameters ( 5 , 6 , 11 ). Thus, it is likely that biological neurons use homeostatic and other developmental mechanisms to successfully find rare sets of values of ion channel conductances that give rise to specific patterns of intrinsic excitability ( 12 – 16 ).…”

mentioning

confidence: 99%

Neuronal morphology enhances robustness to perturbations of channel densities

Zang

Marder

2023

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

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Biological neurons show significant cell-to-cell variability but have the striking ability to maintain their key firing properties in the face of unpredictable perturbations and stochastic noise. Using a population of multi-compartment models consisting of soma, neurites, and axon for the lateral pyloric neuron in the crab stomatogastric ganglion, we explore how rebound bursting is preserved when the 14 channel conductances in each model are all randomly varied. The coupling between the axon and other compartments is critical for the ability of the axon to spike during bursts and consequently determines the set of successful solutions. When the coupling deviates from a biologically realistic range, the neuronal tolerance of conductance variations is lessened. Thus, the gross morphological features of these neurons enhance their robustness to perturbations of channel densities and expand the space of individual variability that can maintain a desired output pattern.

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Synaptic Strengths Dominate Phasing of Motor Circuit: Intrinsic Conductances of Neuron Types Need Not Vary across Animals

Abstract: Visual Abstract

Cited by 4 publications

References 50 publications

Inter-Animal Variability in Activity Phase Is Constrained by Synaptic Dynamics in an Oscillatory Network

Inter-Animal Variability in Activity Phase Is Constrained by Synaptic Dynamics in an Oscillatory Network

Inter-animal variability in activity phase is constrained by synaptic dynamics in an oscillatory network

Neuronal morphology enhances robustness to perturbations of channel densities

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