Dendro-dendritic cholinergic excitation controls dendritic spike initiation in retinal ganglion cells

Nat Commun. 2017 Jun 7:8:15683. doi: 10.1038/ncomms15683.

Abstract

The retina processes visual images to compute features such as the direction of image motion. Starburst amacrine cells (SACs), axonless feed-forward interneurons, are essential components of the retinal direction-selective circuitry. Recent work has highlighted that SAC-mediated dendro-dendritic inhibition controls the action potential output of direction-selective ganglion cells (DSGCs) by vetoing dendritic spike initiation. However, SACs co-release GABA and the excitatory neurotransmitter acetylcholine at dendritic sites. Here we use direct dendritic recordings to show that preferred direction light stimuli evoke SAC-mediated acetylcholine release, which powerfully controls the stimulus sensitivity, receptive field size and action potential output of ON-DSGCs by acting as an excitatory drive for the initiation of dendritic spikes. Consistent with this, paired recordings reveal that the activation of single ON-SACs drove dendritic spike generation, because of predominate cholinergic excitation received on the preferred side of ON-DSGCs. Thus, dendro-dendritic release of neurotransmitters from SACs bi-directionally gate dendritic spike initiation to control the directionally selective action potential output of retinal ganglion cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / chemistry*
  • Action Potentials*
  • Algorithms
  • Amacrine Cells / cytology
  • Animals
  • Cholinergic Agents / chemistry
  • Dendrites / physiology*
  • Female
  • Male
  • Neural Inhibition / physiology
  • Photic Stimulation
  • Photons
  • Rabbits
  • Receptors, Cholinergic / metabolism
  • Retina / metabolism
  • Retinal Ganglion Cells / cytology*
  • Signal Transduction
  • Synapses / physiology
  • Temperature

Substances

  • Cholinergic Agents
  • Receptors, Cholinergic
  • Acetylcholine