Ambient illumination toggles a neuronal circuit switch in the retina and visual perception at cone threshold

Neuron. 2013 Apr 24;78(2):325-38. doi: 10.1016/j.neuron.2013.02.014. Epub 2013 Mar 28.

Abstract

Gradual changes in the sensory environment can lead to abrupt changes in brain computations and perception. However, mechanistic understanding of the mediating microcircuits is missing. By sliding through light levels from starlight to daylight, we identify retinal ganglion cell types in the mouse that abruptly and reversibly switch the weighting of center and surround interactions in their receptive field around cone threshold. Two-photon-targeted recordings and genetic and viral tracing experiments revealed that the circuit element responsible for the switch is a large inhibitory neuron that provides direct inhibition to ganglion cells. Our experiments suggest that weak excitatory input via electrical synapses together with the spiking threshold in inhibitory cells act as a switch. We also reveal a switch-like component in the spatial integration properties of human vision at cone threshold. This work demonstrates that circuits in the retina can quickly and reversibly switch between two distinct states, implementing distinct perceptual regimes at different light levels.

Publication types

  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Action Potentials / physiology
  • Action Potentials / radiation effects
  • Animals
  • Choline O-Acetyltransferase / metabolism
  • Connexins / genetics
  • Herpesvirus 1, Human / metabolism
  • Humans
  • Imaging, Three-Dimensional
  • Lighting*
  • Mice
  • Mice, Transgenic
  • Nerve Net / physiology
  • Neural Inhibition / genetics
  • Neural Inhibition / physiology
  • Parvalbumins / deficiency
  • Parvalbumins / metabolism
  • Patch-Clamp Techniques
  • Photic Stimulation
  • Retina / cytology
  • Retinal Cone Photoreceptor Cells / physiology*
  • Retinal Ganglion Cells / metabolism
  • Retinal Ganglion Cells / physiology*
  • Visual Pathways / physiology*
  • Visual Perception / physiology*

Substances

  • Connexins
  • Parvalbumins
  • connexin 36
  • Choline O-Acetyltransferase