Selectivity for Multiple Stimulus Features in Retinal Ganglion Cells

1 Department of Physiology and Biophysics, University of Washington, Seattle, Washington; 2 Department of Molecular Biology, Princeton University, Princeton, New Jersey; 3 Department of Life Sciences, University of Sussex, United Kingdom Submitted 21 September 2005; accepted in final form 10 August 2006 Under normal viewing conditions, retinal ganglion cells transmit to the brain an encoded version of the visual world. The retina parcels the visual scene into an array of spatiotemporal features, and each ganglion cell conveys information about a small set of these features. We study the temporal features represented by salamander retinal ganglion cells by stimulating with dynamic spatially uniform flicker and recording responses using a multi-electrode array. While standard reverse correlation methods determine a single stimulus feature—the spike-triggered average—multiple features can be relevant to spike generation. We apply covariance analysis to determine the set of features to which each ganglion cell is sensitive. Using this approach, we found that salamander ganglion cells represent a rich vocabulary of different features of a temporally modulated visual stimulus. Individual ganglion cells were sensitive to at least two and sometimes as many as six features in the stimulus. While a fraction of the cells can be described by a filter-and-fire cascade model, many cells have feature selectivity that has not previously been reported. These reverse models were able to account for 80–100% of the information encoded by ganglion cells. Address for reprint requests and other correspondence: M. J. Berry II, Dept. of Molecular Biology, Princeton University, Princeton, NJ 08544 (E-mail: berry{at}princeton.edu )