Passive current flow and morphology in the terminal arborizations of the posterior pituitary

Abstract

1. Patch-clamp techniques were used to study the morphology and electrotonic properties of the terminal arborizations of the posterior pituitary. 2. Neurobiotin-labeling experiments revealed axons and swellings connected to the structure that was patch clamped. The large swellings were en passant and situated along axons in a topological arrangement identical to that of the small varicosities. Axons had many varicosities and few branches, reflecting a predominant architectural motif of beads on a string rather than berries on a bush. 3. Cable theory was used to analyze passive current transients produced by voltage steps under whole-cell clamp. Most charging transients were not consistent with an equivalent cylinder representation as posited by the Rall model for a motoneuron. A few charging transients were consistent with the Rall model and provided estimates for basic membrane and cable properties. 4. Some of the charging transients that violated predictions of the Rall model were consistent with an alternative model, in which the patch-clamped swelling was assumed to be coupled to another swelling by a segment of axon. This model was called the Dumbbell model, and it, together with the neurobiotin-labeling experiments, indicated that a significant number of large swellings were less than one length constant away from another large swelling. 5. Large swellings can have diameters approximately 30 times larger than the diameters of the connecting axons. These swellings lie along the axon such that action potentials must propagate through them to spread excitation through the entire terminal arborization. These large swellings could be sites where action-potential propagation is more likely to fail. 6. The information presented here about neurohypophysial nerve terminals should be useful in further investigations of how terminal arborization geometry and membrane properties influence neurosecretion and synaptic transmission.