Dynamics of excitation and inhibition in the light-adapted Limulus eye in situ

The dynamics of spike discharge in eccentric cell axons from the in situ lateral eye of Limulus, under small sinusoidal modulation of light to which the eye is adapted, are described over two decades of light intensity and nearly three decades of frequency. Steady-state lateral inhibition coefficients, derived from the very low-frequency response, average 0.04 at three interommatidial spacings. The gain vs. frequency of a singly illuminated ommatidium is described closely from 0.004 to 0.4 cps by the linear transfer function s(0.25); this function also accounts approximately for the measured phase leads, the small signal adaptation following small step inputs, and for Pinter's (1966) earlier low-frequency generator potential data. We suggest that such dynamics could arise from a summation in the generator potential of distributed intensity-dependent relaxation processes along the dendrite and rhabdome. Analysis of the dynamic responses of an eccentric cell with and without simultaneously modulated illumination of particular neighbors indicates an effect equivalent to self-inhibition acting via a first-order low-pass filter with time constant 0.42 sec, and steady-state gain near 4.0. The corresponding filters for lateral inhibition required time constants from 0.35 to 1 sec and effective finite delay of 50-90 msec.