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Dendritic trafficking faces physiologically critical speed-precision tradeoffs.

Alex H Williams1,2,3, Cian O'Donnell2,4, Terrence J Sejnowski2,5

  • 1Department of Neurosciences, University of California, San Diego, La Jolla, United States.

Elife
|December 31, 2016
PubMed
Summary
This summary is machine-generated.

The sushi-belt model of neuronal transport, essential for nervous system function, faces challenges. Mathematical modeling reveals inherent trade-offs between speed, precision, and efficiency, potentially explaining long transport delays and local biosynthesis.

Keywords:
active transportcomputational biologymorphologymotor proteinsneurosciencenoneplasticityregulationsystems biologytagging hypothesis

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Area of Science:

  • Neuroscience
  • Cell Biology
  • Systems Biology

Background:

  • Intracellular transport is crucial for nervous system function, enabling the movement of essential molecules like mRNAs and proteins throughout neurons.
  • The 'sushi-belt model' is a leading conceptual framework for neuron-wide cargo trafficking, influenced by local signals such as synaptic input.
  • Despite its influence, the precise predictions and limitations of the sushi-belt model remain incompletely understood.

Purpose of the Study:

  • To rigorously analyze and formalize the sushi-belt model of intracellular transport in neurons using mathematical modeling.
  • To investigate the model's capacity for achieving complex cargo distributions within reconstructed neuronal morphologies.
  • To identify and quantify potential trade-offs between transport speed, precision, and metabolic efficiency inherent to the model.

Main Methods:

  • Development of a mathematical formalization of the sushi-belt model.
  • Simulation of cargo transport dynamics within reconstructed neuronal morphologies.
  • Integration of experimental estimates of trafficking kinetics to predict transport outcomes.

Main Results:

  • The formalized sushi-belt model can generate complex spatial distributions of cargo within neuronal structures.
  • A fundamental, morphology-dependent trade-off exists between the speed, precision, and metabolic efficiency of cargo transport.
  • Model predictions, using experimental kinetics, suggest transport delays of hours to days for effective cargo delivery in dendritic trees.

Conclusions:

  • The sushi-belt model, while capable of complex distributions, imposes significant constraints on transport efficiency.
  • Predicted long transport delays challenge the efficacy of nucleus-to-synapse trafficking as the sole mechanism for cargo supply.
  • These findings provide a potential explanation for the observed prevalence of local biosynthesis in neurons.