Adaptation to changes in higher-order stimulus statistics in the salamander retina

PLoS One. 2014 Jan 21;9(1):e85841. doi: 10.1371/journal.pone.0085841. eCollection 2014.


Adaptation in the retina is thought to optimize the encoding of natural light signals into sequences of spikes sent to the brain. While adaptive changes in retinal processing to the variations of the mean luminance level and second-order stimulus statistics have been documented before, no such measurements have been performed when higher-order moments of the light distribution change. We therefore measured the ganglion cell responses in the tiger salamander retina to controlled changes in the second (contrast), third (skew) and fourth (kurtosis) moments of the light intensity distribution of spatially uniform temporally independent stimuli. The skew and kurtosis of the stimuli were chosen to cover the range observed in natural scenes. We quantified adaptation in ganglion cells by studying linear-nonlinear models that capture well the retinal encoding properties across all stimuli. We found that the encoding properties of retinal ganglion cells change only marginally when higher-order statistics change, compared to the changes observed in response to the variation in contrast. By analyzing optimal coding in LN-type models, we showed that neurons can maintain a high information rate without large dynamic adaptation to changes in skew or kurtosis. This is because, for uncorrelated stimuli, spatio-temporal summation within the receptive field averages away non-gaussian aspects of the light intensity distribution.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Action Potentials / radiation effects
  • Adaptation, Ocular / radiation effects*
  • Animals
  • Light
  • Linear Models
  • Nonlinear Dynamics
  • Photic Stimulation*
  • Retina / physiology*
  • Retina / radiation effects*
  • Retinal Ganglion Cells / physiology
  • Retinal Ganglion Cells / radiation effects
  • Retinal Neurons / physiology
  • Retinal Neurons / radiation effects
  • Statistics as Topic
  • Urodela / physiology*

Grant support

This work was supported by The Israel Science Foundation and The Human Frontiers Science Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.