Interval coding and band-pass filtering at oculomotor synapses in crayfish

Abstract

1. Crayfish exhibit steady-state compensatory eyestalk rotations in response to rotations of the organism or the visual surround. For stimuli in the vertical planes (pitch or roll) the visual reflexes are mediated by identified visual interneurons [sustaining fibers (SFs)], which synapse on identified oculomotor neurons (Mns) (18). 2. The optimal visual stimulus is broad-field intense illumination (simulated skylight) distributed over the dorsal half of the cornea. These stimuli are also optimal for eliciting a regular pacing discharge in SFs with dorsal receptive fields (17). Since a unique discharge pattern is associated with the reflex stimulus, we proposed that the pacing discharge interval encodes the stimulus condition and is optimal for driving the motoneuron discharge. 3. The cross-correlation of SF and Mn impulse trains exhibit large peaks (or troughs) at short latencies associated with strong excitatory (or inhibitory) interactions and “secondary effects” at longer delays associated with the periodicity of the Mn impulse train. The secondary peaks and troughs indicate delayed periods of elevated or depressed Mn excitability synchronized to the reference train (SF) events. From the structure of the cross-correlograms and the motoneuron autocorrelograms we predicted that the spike-to-spike synaptic throughput should be differentially sensitive to the various classes of SF interspike intervals. 4. The hypotheses were tested with logical-correlation functions that directly measure the relative synaptic efficacy of several classes of SF intervals during a continuous train at constant mean rate. The results indicate that the SF-to-Mn excitatory synapse is maximally driven by SF impulses separated by approximately 85 ms. These events are about 2.5 times as effective as the impulses associated with short intervals (less than 20 ms) and 1.4 times as effective as the spikes of long intervals (250 ms). The optimal interval in the various preparations is highly to correlated to the period of the Mn discharge and the SF modal interspike interval. Inhibitory synapses are also differentially sensitive to the SF interspike intervals, but they exhibit summation rather than depression in response to short interspike intervals. 5. These results are generally consistent with previously formulated relationships (39), which govern the synaptic modulation of pacemakers and may apply to any synaptic interaction in which the postsynaptic neuron exhibits a regular discharge. 6. Combinations of long and short intervals with the same mean rate as the optimal interval are not as effective in driving the SF-to-Mn synapse.(ABSTRACT TRUNCATED AT 400 WORDS)