Serotonin-containing neurons in lobsters: the actions of gamma-aminobutyric acid, octopamine, serotonin, and proctolin on activity of a pair of identified neurons in the first abdominal ganglion

Abstract

1. Serotonin has been shown to be an important neurohormone that modulates behavioral output in lobsters. This study explores the neurochemical identity of excitatory and inhibitory inputs to a pair of identified serotonin-containing neurons in the first abdominal ganglion (A1) of the lobster that also contain the pentapeptide proctolin. These neurons are spontaneously active, appear to be driven by an endogenous pacemaking mechanism, and have been shown to play a role in circuits that control behaviorally relevant postures. 2. To explore the exogenous control of neuronal activity, a number of putative neuroactive compounds were superfused over the A1 serotonin-containing neurons in isolated ventral nerve cords. Three amines, gamma-aminobutyric acid (GABA), octopamine, and serotonin, were found to be potent inhibitors in a dose-dependent manner. GABA inhibition had a rapid onset and termination and yielded a transient postinhibitory rebound activity immediately after amine washout; activity eventually returned to the preinhibition level. Octopamine inhibition had a less rapid onset and termination, and the steady-state activity after inhibition was higher than preinhibition firing in most cells (22% of which were statistically significantly increased). Serotonin inhibition had a relatively slow onset and termination, and the steady-state activity after inhibition remained low in most cells (19% significantly decreased). 3. Repeated or prolonged exposure to these three amines reduced the efficacy of inhibition. Three types of desensitization have been empirically defined: 1) rapid desensitization, which tended to dampen the initial inhibition; this was particularly strong for GABA inhibition; 2) low-dose desensitization, in which the A1 serotonin containing neurons became less sensitive to inhibition by a particular concentration of amine after prior exposure to a lower concentration, although the lower concentration may not by itself have had inhibitory effects; this was seen with octopamine inhibition; and 3) long-term desensitization, in which the efficacy of inhibition of a particular amine concentration dwindled with repeated applications (even with up to 160 min washout between applications); this was seen with octopamine and serotonin inhibition, although not for every A1 serotonin-containing neuron analyzed. 4. Bath application of these three amines was still capable of inhibiting the A1 serotonin-containing neurons when inhibitory synaptic transmission was blocked by use of low Ca2+/high Mg2+ solutions. 5. The pentapeptide proctolin excited the A1 serotonin-containing neurons: it activated silent neurons and increased the firing rate of spontaneously active neurons. The excitatory effect outlasted the presence of the peptide.(ABSTRACT TRUNCATED AT 400 WORDS)