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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.