Complexity and frequency hierarchies in the catfish retina

The intricate connectivity and interactions between neurons in the vertebrate retina have made their individual roles in signal processing very difficult to elucidate. We have used a recently developed mathematical tool, fast orthogonal search (FOS), to probe the catfish outer (distal) and inner (proximal) retina, and study the signal processing within. Through FOS, a given waveform can be decomposed into a parsimonious sinusoidal series containing the most significant constituent frequencies. In particular, we examined the light-evoked first-order Wiener kernels of horizontal cells and on-bipolar cells, and on-off, off- and on-amacrine and ganglion cells. Here we report a hierarchy (correlation coefficient up to 0.86) in preferred frequency and complexity of response corresponding to the retina's structural hierarchy. In addition, clear differences between on-, on-off and off-cell functional characteristics were detected. For example, the kernel waveform for the on-amacrine cell was found to be more complex and to have a higher preferred frequency than that for the off-amacrine cell. Indeed FOS analysis revealed that both off- (sustained) amacrine and off-ganglion cells exhibit significantly less complexity in their waveforms for signal processing of light input than do the corresponding on- and on-off cells. This shows a clear breakdown in symmetry between on- and off-pathways, and suggests that connections to off-cells may provide fewer or a smaller variety of inputs than those to on- and on-off cells. Many of our new findings can be appreciated by assuming an underlying cascade structure for the retinal information processing. The FOS findings in particular support the following previously advanced hypothesis: the transition in nonlinear processing from on-off amacrine to on- off-amacrine cells is due to high-pass linear filtering. Furthermore, our results indicate that the high-pass filtering is more sharply differentiating for the on-amacrine than for the off-amacrine cell.