Retinal ganglion cells--spatial organization of the receptive field reduces temporal redundancy

According to the 'redundancy reduction' hypothesis, a visual neuron removes correlations from an image to reduce redundancy in the spike train, thus increasing the efficiency of information coding. However, all elaborations of this general hypothesis have treated spatial and temporal correlations separately. To investigate how a retinal ganglion cell responds to combined spatial and temporal correlations, we selected those cells with center-surround receptive field and presented a stimulus with strong spatiotemporal correlations: we presented a random sequence of intensities (of white noise) to the receptive field center and then activated the surround with the same sequence. We found that, for most cells, activating the surround reduced temporal redundancy in the spike train. Although the surround often reduced the information rate of the spike train it always increased the amount of information per spike. However, when the surround was modulated by a different white-noise sequence than the center, eliminating spatial-temporal correlations, the surround no longer reduced redundancy or increased information per spike. The proposed mechanism for redundancy reduction is based on the temporal properties of the center and surround: the surround signal is delayed behind the center signal and subtracted from it; this implements a differentiator which removes low frequencies from the stimulus, thus reducing redundancy in the spike train. These results extend the redundancy reduction hypothesis by indicating that the spatial organization of the receptive field into center and surround can reduce temporal redundancy within the spike train of a ganglion cell.