Two stages of integration in a leech visual interneuron

Summary

• 1. The lateral visual (LV) cells of the medicinal leech,Hirudo medicinalis, are excited by photoreceptors having axons in the ipsilateral DC and DD nerves. Activating the photoreceptors photically or electrically yields at least three kinds of event in the LV cell (Fig. 1B).

• 2. There are very small events, which appear to be electrical coupling potentials from the photoreceptors (Fig. 6); there are large events, which appear to be action potentials arising in the main neurite and propagating out the axon (Figs. 2, 5); and finally, there are unusual medium-sized events.

• 3. These medium-sized events appear to be ‘stacks’ of several small spike-like components (Fig. 7A). These small spikes have different thresholds and latencies, suggesting that they arise at different initiation sites (Fig. 7B).

• 4. Small spikes are not chemical excitatory postsynaptic potentials (EPSPs), since they persist in high Mg saline (Fig. 7). They are not antidromic impulses arising distally in the axon, since they do not collide with orthodromic action potentials (Fig. 8). Nor, given the initiation kinetics of small spikes, are they coupling potentials from neurons having axons in the optic nerves (Figs. 11, 12).

• 5. Moderate hyperpolarization increases the amplitude of small spikes, but strong hyperpolarization blocks them (Fig. 9). Very strong hyperpolarizing pulses elicit small spikes by anode break excitation (Fig. 10).

• 6. These results suggest that small spikes may be active responses that arise locally in the dendrites of the LV cell but fail to propagate actively into the main neurite and axon (Fig. 16).

• 7. Alternatively, small spikes may be coupling potentials from unidentified interneurons that are strongly electrically coupled to the LV cell. In order to account for the results, however, there would have to be at least 24 such interneurons. The failure to find any coupling neurons, despite extensive searching, makes this alternative possibility increasingly unlikely.

• 8. The small spikes activated by axons in the DC nerve appear to be distinct from those activated by axons in the DD nerve (Figs. 13, 14).

• 9. Within the main neurite the small spikes behave like conventional EPSPs: they sum temporally and spatially, and they interact with inhibitory synaptic input to set the firing level of the LV cell (Figs. 12A, 15).

• 10. Thus, there appear to be two stages of integration in the activation of the LV cell: at the first stage, EPSPs from the photoreceptors sum to elicit small spikes; at the second stage, the small spikes sum to generate action potentials.