The electromotor system of the stargazer: A model for integrative actions at electrotonic synapses

The electric organs of Astroscopus are modified from extraocular muscles and innervated by the enlarged oculomotor nuclei. The electromotor neuron somata are contacted by fine processes with which they form gap junctions. Presynaptic vesicles and active zones are also present, although physiological data give no indication of chemically mediated transmission. Antidromic stimulation produces long lasting graded depolarizations in the electromotor neurons. The latency is sufficiently short to indicate that the cells are electrotonically coupled, which was confirmed by direct measurement. Antidromic invasion may normally fail and is easily blocked by hyperpolarization revealing initial segment and axon spikes. Spinal stimulation evokes poststynaptic potentials (PSPs) and orthodromic impulses; the PSPs are not smoothly graded in amplitude. A medullary nucleus innervates the electromotor nucleus; the medullary cells also show short latency graded antidromic depolarizations and presumably are electrotonically coupled. Their coupling accounts for the variability in PSPs evoked by spinal stimulation. Apparent time constants differ greatly for direct stimulation of a single cell, decay of afterhyperpolarization, electrotonic spread from one cell to a neighbor, and decay of PSPs and graded antidromic depolarizations. The differences can be accounted for in terms of a highly interconnected network of electrotonically coupled cells, which was simulated computationally. Because of the long membrane time constant graded antidromic depolarizations summate. Because antidromic invasion is facilitated by depolarization, the antidromic depolarizations can show pronounced facilitation. The observed 'plasticity' within this electrotonically coupled system provides a model for integrative actions at other sites of coupling.