High-frequency oscillatory potentials (HFOPs) have been recorded from
ganglion cells in cat, rabbit, frog, and mudpuppy retina and in
electroretinograms (ERGs) from humans and other primates. However, the
origin of HFOPs is unknown. Based on patterns of tracer coupling, we
hypothesized that HFOPs could be generated, in part, by negative
feedback from axon-bearing amacrine cells excited via
electrical synapses with neighboring ganglion cells. Computer
simulations were used to determine whether such axon-mediated feedback
was consistent with the experimentally observed properties of HFOPs.
(1) Periodic signals are typically absent from ganglion cell PSTHs, in
part because the phases of retinal HFOPs vary randomly over time and
are only weakly stimulus locked. In the retinal model, this phase
variability resulted from the nonlinear properties of axon-mediated
feedback in combination with synaptic noise. (2) HFOPs increase as a
function of stimulus size up to several times the receptive-field
center diameter. In the model, axon-mediated feedback pooled signals
over a large retinal area, producing HFOPs that were similarly size
dependent. (3) HFOPs are stimulus specific. In the model, gap junctions
between neighboring neurons caused contiguous regions to become phase
locked, but did not synchronize separate regions. Model-generated HFOPs
were consistent with the receptive-field center dynamics and spatial
organization of cat alpha cells. HFOPs did not depend qualitatively on
the exact value of any model parameter or on the numerical precision of
the integration method. We conclude that HFOPs could be mediated, in
part, by circuitry consistent with known retinal anatomy.