Spatial segregation of adaptation and predictive sensitization in retinal ganglion cells

Neuron. 2013 Aug 7;79(3):541-54. doi: 10.1016/j.neuron.2013.06.011.

Abstract

Sensory systems change their sensitivity based on recent stimuli to adjust their response range to the range of inputs and to predict future sensory input. Here, we report the presence of retinal ganglion cells that have antagonistic plasticity, showing central adaptation and peripheral sensitization. Ganglion cell responses were captured by a spatiotemporal model with independently adapting excitatory and inhibitory subunits, and sensitization requires GABAergic inhibition. Using a simple theory of signal detection, we show that the sensitizing surround conforms to an optimal inference model that continually updates the prior signal probability. This indicates that small receptive field regions have dual functionality--to adapt to the local range of signals but sensitize based upon the probability of the presence of that signal. Within this framework, we show that sensitization predicts the location of a nearby object, revealing prediction as a functional role for adapting inhibition in the nervous system.

Publication types

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

MeSH terms

  • Action Potentials / physiology
  • Adaptation, Physiological / physiology*
  • Ambystoma
  • Aminobutyrates / pharmacology
  • Animals
  • Contrast Sensitivity / physiology*
  • Dose-Response Relationship, Drug
  • Excitatory Amino Acid Agonists / pharmacology
  • GABA Antagonists / pharmacology
  • Glycine Agents / pharmacology
  • Larva
  • Models, Biological
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology
  • Photic Stimulation
  • Picrotoxin / pharmacology
  • Predictive Value of Tests
  • Retina / cytology*
  • Retinal Ganglion Cells / classification
  • Retinal Ganglion Cells / physiology*
  • Signal Detection, Psychological
  • Strychnine / pharmacology
  • Visual Fields*
  • Visual Pathways / physiology*

Substances

  • Aminobutyrates
  • Excitatory Amino Acid Agonists
  • GABA Antagonists
  • Glycine Agents
  • Picrotoxin
  • 2-amino-4-phosphonobutyric acid
  • Strychnine