Species-specific wiring for direction selectivity in the mammalian retina

Nature. 2016 Jul 7;535(7610):105-10. doi: 10.1038/nature18609. Epub 2016 Jun 22.

Abstract

Directionally tuned signalling in starburst amacrine cell (SAC) dendrites lies at the heart of the circuit that detects the direction of moving stimuli in the mammalian retina. The relative contributions of intrinsic cellular properties and network connectivity to SAC direction selectivity remain unclear. Here we present a detailed connectomic reconstruction of SAC circuitry in mouse retina and describe two previously unknown features of synapse distributions along SAC dendrites: input and output synapses are segregated, with inputs restricted to proximal dendrites; and the distribution of inhibitory inputs is fundamentally different from that observed in rabbit retina. An anatomically constrained SAC network model suggests that SAC–SAC wiring differences between mouse and rabbit retina underlie distinct contributions of synaptic inhibition to velocity and contrast tuning and receptive field structure. In particular, the model indicates that mouse connectivity enables SACs to encode lower linear velocities that account for smaller eye diameter, thereby conserving angular velocity tuning. These predictions are confirmed with calcium imaging of mouse SAC dendrites responding to directional stimuli.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amacrine Cells / physiology
  • Animals
  • Calcium / metabolism
  • Computer Simulation
  • Connectome*
  • Dendrites / physiology
  • Excitatory Postsynaptic Potentials
  • Female
  • Male
  • Mice
  • Models, Neurological
  • Motion Perception / physiology*
  • Neural Inhibition
  • Neural Pathways / physiology*
  • Photic Stimulation
  • Presynaptic Terminals / metabolism
  • Rabbits
  • Retina / anatomy & histology
  • Retina / cytology*
  • Retina / physiology*
  • Retinal Bipolar Cells / physiology
  • Species Specificity
  • Synapses / physiology*

Substances

  • Calcium