Regional innervation of rabbit ciliary ganglion cells by the terminals of preganglionic axons

Abstract

In the rabbit, ciliary ganglion neurons with dendrites maintain inputs from several different axons during the period of synaptic rearrangement that occurs in early postnatal life. Neurons without dendrites, on the other hand, lose the majority of their initial inputs and are innervated in maturity by the terminals of only one or two axons (Purves, D., and R.I. Hume (1981) J. Neurosci. 1: 441-452; Hume, R.I., and D. Purves (1981) Nature 293: 469-471). We have explored the basis of this phenomenon by individually marking preganglionic axons and the neurons they innervate with horseradish peroxidase. In general, the innervation of geometrically complex (multiply innervated) neurons by individual preganglionic axons is regional. That is, the synaptic contacts made by an axon on these neurons are limited to a portion of the postsynaptic surface that includes some, but not all, of the dendrites. This regional innervation of target neurons is consistent with the view that dendrites allow multiple innervation to persist by providing relatively separate postsynaptic domains for individual preganglionic axons. Such regional innervation may mitigate competitive interactions between the several axons which initially innervate the same neuron.

Density of somatic innervation on mammalian autonomic ganglion cells is inversely related to dendritic complexity and preganglionic convergence

“…complexity of its dendrites (Purves and Hume, 1981;Purves and Lichtman, 1985). Competition between axons innervating a cell with no dendrites generally results in a single dominant input in maturity; in contrast, competition on cells with dendrites is mitigated so that an increasing number of inputs is retained on increasingly complex cells Purves, 1981, 1983;Forehand and Purves, 1984). The results of the present study show that the distribution of synapses on target neurons is also influenced by the presence of dendrites.…”

“…Since the cell body is the final common pathway for all ganglion cell activity, asynchronous activity generated by the several different inputs to more complex ganglion cells may limit the ability of synapses from different axons to coexist on the cell body surface. Conversely, synapse formation on dendrites might be less affected by increased convergence because dendrites are innervated by only a subset of the inputs to a particular ganglion cell (Forehand and Purves, 1984) and are to some extent isolated from each other by the passive electrical properties of the dendritic arbor.…”

“…The results show that the density of somatic innervation is inversely proportional to the dendritic complexity of these neurons and to the number of different inputs that they receive. Some of these results have been reported in abstract form (Purves et al, 1984).…”

Development of dendritic calcium currents in ganglion cells of the rat lower lumbar sympathetic chain.

“…suggested that the transmitter action was augmented by a regenerative conductance change initiated distal from the soma. We propose that this results because the synaptic contacts of the strong preganglionic axon exist on a single dendrite (see Forehand & Purves, 1984) and are associated with the region of the membrane containing voltage-dependent calcium channels. Activation of this input invariably evokes an action potential in the ganglion cell when it is not hyperpolarized.…”

Assessing Some Dynamic Properties of the Living Nervous System

“…Thus, repeated imaging of developing neuromuscular junctions in the snake indicates that competing terminals tend to segregate (Balice-Gordon & Lichtman, 1989). This phenomenon may also occur (although quite incompletely) during the initial innervation of developing autonomic ganglion cells Forehand & Purves, 1984;Forehand, 1987).…”