Abstract
1. Despite the considerable progress made in understanding the role of electrical activity in triggering secretion, the developmental relationships between excitability and secretion are not well understood. The well-characterized bag cell neurons of Aplysia provide an advantageous system in which to investigate developmental interactions of these two key properties of neurons. 2. A prolonged afterdischarge triggers egg laying hormone (ELH) secretion in mature bag cell neurons. To investigate secretion in the developmental framework of excitability, we first examined whether immature neurons, which are incapable of the mature form of excitability (afterdischarge), contain ELH and whether this hormone is packaged in vesicles. We used immunoelectron microscopy to compare vesicular localization of ELH and to compare the size and density of ELH-containing vesicles in neurons from adult and juvenile Aplysia. This comparison revealed that immature neurons contain ELH in vesicles in the size range of secretory vesicles. However, they lack a class of large vesicles (> 250 nm in diameter) that is characteristic of mature neurons. 3. To investigate whether the ELH contained in immature bag cell neurons could be secreted in response to electrical activity, we used the potassium channel blocker tetraethylammonium (TEA) combined with nerve stimulation to depolarize neurons from both juvenile animals (ovotestes do not contain eggs) and from adult Aplysia (ovotestes contain eggs). Using radioimmunoassay, we have found that the duration and amount of ELH secreted from bag cell neurons from juvenile Aplysia in response to TEA does not depend on whether or not the cells can be induced to afterdischarge, and the amount and duration of ELH secreted from bag cell neurons of juvenile Aplysia (whether or not they afterdischarged) differed from those secreted by adult neurons. However, by normalizing for body size, we found that the final estimated hemolymph concentration of ELH would be similar in juvenile and adult animals. 4. We investigated the potential functional significance of secretion of bag cell hormones in juvenile Aplysia by attempting to bypass the bag cell neurons and directly activate downstream elements with extract from adult bag cell neurons (BCE), known to contain ELH and other peptides. We found that juvenile Aplysia exhibit at least one component of egg-laying behavior, cessation of locomotion, in response to BCE during a developmental period (as measured by weight) in which they normally would possess neurons incapable of afterdischarge. Thus developmental regulation of excitability in the bag cell neurons may prevent inappropriate hormone release and subsequent premature expression of reproductive behaviors.
Highlights
The principal function of neuroendocrine cells is the regulated secretion of hormones
We have found that the duration and amount of ELH secreted from bag cell neurons from juvenile Aplysia in response to TEA does not depend on whether or not the cells can be induced to afterdischarge, and the amount and duration of ELH secreted from bag cell neurons of juvenile Aplysia differed from those secreted by adult neurons
The juvenile Aplysia weighed < 11 g and most probably contained immature bag cell neurons that were incapable of afterdischarge, which is the mature form of excitability (Nick et al 1993, 1996)
Summary
The principal function of neuroendocrine cells is the regulated secretion of hormones ( for review, see Schlegel and Mollard 1995). The bag cell neurons of Aplysia californica provide a system that has several advantages for the investigation of the development of secretion relative to the differentiation of excitability: 1) the neurons are relatively large and identified, even in juvenile animals (Leibowitz and Castellucci 1983; McAllister et al 1983; Nick et al 1993); 2) mature neurons exhibit a well-described, stereotypical pattern of excitability, a regenerative afterdischarge, which is a period of prolonged depolarization and repetitive firing ( 15 - 30 min) ( Kupfermann and Kandell970; for review, see Conn and Kaczmarek 1989) that triggers the release of peptide hormones; 3) mature neurons contain very high concentrations of a peptide hormone, egg laying hormone (ELH), which triggers egglaying behaviors (Bernheim and Mayeri 1995; Chiu et al 1979) ; and 4) bag cell neurons can be identified and their activity recorded early in development before they have the capacity to exhibit an afterdischarge (Nick et al 1993; present study). Detailed electrophysiological analysis revealed that specific ion currents are up-regulated
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