Apportionment of the terminals from single preganglionic axons to target neurones in the rabbit ciliary ganglion.

Abstract

We have studied the apportionment of terminals from single preganglionic axons to target neurones in the ciliary ganglion of adult rabbits. Both electrical recording and intra-axonal injection of horseradish peroxidase (HRP) showed that each preganglionic axon innervates only a small fraction of the ganglion cell population (about 10-20 of the approximately 400 ganglion cells). Examination of ganglia in whole mounts showed that neurones whose cell bodies were enveloped by HRP-labelled boutons from a single axon were often surrounded by other neurones which received no contacts from the labelled fibre. Electron microscopical examination of labelled presynaptic terminals on individual ganglion cells confirmed that the boutons of single axons were sharply confined to particular target cells. This suggests that individual target neurones (or portions of them) are the unit of innervation during the development of these synaptic connexions. Comparison of the amplitudes of synaptic responses in singly and multiply innervated ganglion cells indicated that, on average, an individual axon made a weaker synaptic connexion with a multiply innervated neurone than with neurone that received only one input. Moreover, neurones innervated by several different axons tended to have fewer synapses on their somata than neurones innervated by only one or two preganglionic axons. Individual post-synaptic profiles were often contacted exclusively by labelled terminals when examined in the electron microscope. Since many of these neurones are multiply innervated, this observation suggests some regional separation of the several inputs contacting the same cell. For several reasons, however, this inference must be regarded as tentative. Taken together, these findings provide a possible explanation of the correlation between the dendritic geometry of ganglion cells and the number of different axons that innervate them (Purves & Hume, 1981). The several axons that initially innervate ganglion cells without dendrites evidently compete during early life until only a single input remains. On ganglion cells with dendrites, however, the number of inputs that persists is proportional to dendritic complexity. The present results suggest that the diminished competition between axons innervating neurones with dendrites may result from some degree of terminal segregation on dendritic arborizations.