Soma-axon coupling configurations that enhance neuronal coincidence detection

Joshua H. Goldwyn, Michiel W.H. Remme, John Rinzel

Research output: Contribution to journalArticle

Abstract

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, IKLT. 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 IKLT further enhances coincidence detection sensitivity, but with effects that depend on coupling configuration. For instance, in models with weak soma-to-axon and weak axon-to-soma coupling, IKLT in the axon enhances coincidence detection more effectively than IKLT in the soma. By using a minimal model of soma-to-axon coupling, we connect structure, dynamics, and computation. Although we consider the particular case of MSO coincidence detectors, our method for creating and exploring a parameter space of two-compartment models can be applied to other neurons.

Original languageEnglish (US)
Pages (from-to)e1006476
JournalPLoS computational biology
Volume15
Issue number3
DOIs
StatePublished - Mar 1 2019

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Carisoprodol
Coincidence
axons
Axons
Configuration
Neurons
neurons
Neuron
sodium
Spike
Sodium
detectors
Compartment Model
Negative Feedback
Detector
Feedforward
Detectors
Parameter Space
Timing
inactivation

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Modeling and Simulation
  • Ecology
  • Molecular Biology
  • Genetics
  • Cellular and Molecular Neuroscience
  • Computational Theory and Mathematics

Cite this

Soma-axon coupling configurations that enhance neuronal coincidence detection. / Goldwyn, Joshua H.; Remme, Michiel W.H.; Rinzel, John.

In: PLoS computational biology, Vol. 15, No. 3, 01.03.2019, p. e1006476.

Research output: Contribution to journalArticle

Goldwyn, Joshua H. ; Remme, Michiel W.H. ; Rinzel, John. / Soma-axon coupling configurations that enhance neuronal coincidence detection. In: PLoS computational biology. 2019 ; Vol. 15, No. 3. pp. e1006476.
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