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

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.Author Summary: Our sensory systems have to process stimuli under a wide range of environmental conditions. To cope with this challenge, the involved neurons adapt by adjusting their signal processing to the recently encountered intensity range. In the visual system, one finds, for example, that higher visual contrast leads to changes in how visual signals are temporally filtered, making signal processing faster and more band-pass-like at higher contrast. By analyzing signals from neurons in the retina of salamanders, we here found that these adaptation effects can be described by a fixed set of filters, independent of contrast, whose relative contributions change with contrast. Also, we found that different phenomena contribute to this adaptation. In particular, some cells change their relative sensitivity to light increments and light decrements, whereas other cells are influenced by a strong contrast-dependence of the exact timing of their responses. Our results show that contrast adaptation in the retina is not an entirely homogeneous phenomenon, and that models with multiple filters can help in characterizing sensory adaptation.