Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit

Nature. 2011 Jan 20;469(7330):407-10. doi: 10.1038/nature09711. Epub 2010 Dec 19.


Spatial asymmetries in neural connectivity have an important role in creating basic building blocks of neuronal processing. A key circuit module of directionally selective (DS) retinal ganglion cells is a spatially asymmetric inhibitory input from starburst amacrine cells. It is not known how and when this circuit asymmetry is established during development. Here we photostimulate mouse starburst cells targeted with channelrhodopsin-2 (refs 6-8) while recording from a single genetically labelled type of DS cell. We follow the spatial distribution of synaptic strengths between starburst and DS cells during early postnatal development before these neurons can respond to a physiological light stimulus, and confirm connectivity by monosynaptically restricted trans-synaptic rabies viral tracing. We show that asymmetry develops rapidly over a 2-day period through an intermediate state in which random or symmetric synaptic connections have been established. The development of asymmetry involves the spatially selective reorganization of inhibitory synaptic inputs. Intriguingly, the spatial distribution of excitatory synaptic inputs from starburst cells is significantly more symmetric than that of the inhibitory inputs at the end of this developmental period. Our work demonstrates a rapid developmental switch from a symmetric to asymmetric input distribution for inhibition in the neural circuit of a principal cell.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Action Potentials / physiology
  • Amacrine Cells / metabolism
  • Amacrine Cells / physiology
  • Amacrine Cells / radiation effects
  • Animals
  • Channelrhodopsins
  • Female
  • Light
  • Male
  • Mice
  • Models, Neurological*
  • Motion Perception / physiology*
  • Motion*
  • Neural Inhibition / physiology*
  • Neural Pathways / physiology*
  • Neuroanatomical Tract-Tracing Techniques
  • Photic Stimulation
  • Rabies virus / genetics
  • Rabies virus / isolation & purification
  • Rabies virus / physiology
  • Retina / cytology
  • Retina / growth & development
  • Retina / physiology*
  • Retinal Ganglion Cells / physiology
  • Synapses / metabolism


  • Channelrhodopsins