Synchronized firing and visual signaling in primate retinal ganglion cells

E.J. Chichilnisky

The Salk Institute

Action potentials occurring nearly simultaneously in different neurons have been suggested to play an important role in neural signaling. Does synchronized firing contribute to visual signaling by primate retinal ganglion cells (RGCs)? Using multi-electrode recordings from isolated retinas of macaque monkeys, we reported previously that (a) neighboring RGCs fired synchronized spikes (5 ms) at about twice the rate expected by chance, (b) synchronized firing was created by cell-type specific local retinal circuits, and (c) receptive fields of synchronized spikes were slightly smaller than the combined receptive fields of individual cells, possibly consistent with the suggestion from salamander recordings that synchronized spikes carry fine-grained spatial information. Here we examine further the role of synchronized firing in retinal signaling. Spike trains from pairs of cells were coarsely (plus or minus 20 ms) but not precisely (plus or minus 5 ms) synchronized across repeated trials of the same stimulus, indicating that precisely synchronized spikes did not arise simply from highly reproducible light responses and common stimulation, but were generated by the retinal circuitry in a manner not entirely determined by the stimulus. Receptive fields of precisely and coarsely synchronized spikes were very similar, suggesting that any fine-grained spatial information in synchronized spikes can be attributed to the coarse synchronization generated by common input to cells with overlapping receptive fields. To determine whether precisely synchronized spikes could be used to convey stimulus information to the brain not present in individual spike trains, linear reconstructions of white noise stimuli were obtained using (a) spike trains of two cells, or (b) spike trains of two cells and a synthetic spike train containing synchronized spikes, controlled for additional degrees of freedom in reconstruction. Separate treatment of synchronized spikes did not improve the accuracy of stimulus reconstruction. These results suggest that precisely synchronized spikes are not a significant source of distinctive visual signals in primate RGCs.