Spike-Triggered Covariance Analysis Reveals Phenomenological Diversity of Contrast Adaptation in the Retina

PLoS Comput Biol. 2015 Jul 31;11(7):e1004425. doi: 10.1371/journal.pcbi.1004425. eCollection 2015 Jul.

Abstract

When visual contrast changes, retinal ganglion cells adapt by adjusting their sensitivity as well as their temporal filtering characteristics. The latter has classically been described by contrast-induced gain changes that depend on temporal frequency. Here, we explored a new perspective on contrast-induced changes in temporal filtering by using spike-triggered covariance analysis to extract multiple parallel temporal filters for individual ganglion cells. Based on multielectrode-array recordings from ganglion cells in the isolated salamander retina, we found that contrast adaptation of temporal filtering can largely be captured by contrast-invariant sets of filters with contrast-dependent weights. Moreover, differences among the ganglion cells in the filter sets and their contrast-dependent contributions allowed us to phenomenologically distinguish three types of filter changes. The first type is characterized by newly emerging features at higher contrast, which can be reproduced by computational models that contain response-triggered gain-control mechanisms. The second type follows from stronger adaptation in the Off pathway as compared to the On pathway in On-Off-type ganglion cells. Finally, we found that, in a subset of neurons, contrast-induced filter changes are governed by particularly strong spike-timing dynamics, in particular by pronounced stimulus-dependent latency shifts that can be observed in these cells. Together, our results show that the contrast dependence of temporal filtering in retinal ganglion cells has a multifaceted phenomenology and that a multi-filter analysis can provide a useful basis for capturing the underlying signal-processing dynamics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology*
  • Adaptation, Ocular / physiology*
  • Animals
  • Computer Simulation
  • Contrast Sensitivity / physiology*
  • Models, Neurological*
  • Nerve Net / physiology*
  • Neural Inhibition / physiology
  • Retinal Ganglion Cells / physiology*
  • Urodela

Grant support

This work was supported by the International Human Frontier Science Program Organization, by the Deutsche Forschungsgemeinschaft (GO 1408/2-1 and Collaborative Research Center 889, C1), and by the European Union Seventh Framework Programme (FP7-ICT-2011.9.11) under grant agreement no 600954 (“VISUALISE”). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.