Development of neurons in the abdominal ganglion of Aplysia californica: II. Nonneural support cells

Abstract

The release by nonneural support cells of a diffusable chemical substance into the local environment in which sympathetic neurons develop is thought to play a crucial role in their differentiation. In this paper, we describe a novel class of nonneural support cells associated with a central ganglion of Aplysia californica during the premetamorphic stages of development. These support cells contain secretory granules whose contents are primarily released at metamorphosis. The release of these contents may signal the burst of neuronal growth and maturation that occurs following metamorphosis. The evidence in support of this notion is the following: (1) Spontaneous release of the granule material at metamorphosis coincides with an increase in cell body growth and a more marked increase in the density of synapses of the abdominal ganglion. (2) Premature release of the granule material before metamorphosis with artificial seawater containing a high concentration of potassium results in a burst in cell body growth and a premature increase in synapse density. (3) Premature release of granule material also results in a precocious increase in the number of spines formed and synaptic contacts received by specific identified cells. Based on the findings in this and the preceding paper, we propose a two-stage model of the developmental program for differentiation of neurons in the abdominal ganglion. First, axosomatic contacts trigger axonal outgrowth. Second, material released from the granules of the support cells stimulates further steps in neuronal differentiation, including cell growth, spine development, and synapse formation.