The effect of the neuropeptide FMRFamide on Aplysia californica siphon motoneurons involves multiple ionic currents that vary seasonally

Abstract

The molluscan neuropeptide FMRFamide has a number of inhibitory actions on the sensory neurons and motoneurons mediating the defensive gill and siphon withdrawal reflex pathway of Aplysia californica. Exogenous application of FMRFamide has a biphasic, dual-polarity effect on the majority of LFS siphon motoneurons, causing a transient depolarization followed by a prolonged hyperpolarization. FMRFamide induces this response in LFS neurons by causing an increase in multiple ionic currents, including a transient Na+ current, a slow prolonged Na+ current, a 4-aminopyridine (4-AP)-sensitive K+ current and a 4-AP-insensitive K+ current. We have found that a subset of LFS neurons exhibits an exclusively excitatory, biphasic response to FMRFamide, consisting of a transient depolarization followed by a prolonged depolarization of reduced magnitude. Over a period of 29 months, we consistently observed an increase in the incidence of the exclusively excitatory response during the summer months (June to September). From October to May, we observed an exclusively excitatory response to FMRFamide in 19 % of LFS neurons; yet, in the summer months, 51 % of LFS neurons exhibited this response pattern. We compared the ionic basis of the exclusively excitatory response to FMRFamide with the ionic mechanisms mediating the more frequently observed excitatory/inhibitory response. The exclusively excitatory response involves three of the same ionic components as the more typical excitatory/inhibitory response, including the activation of a transient Na+ current, a slow prolonged Na+ current and a 4-AP-insensitive K+ current. The principal difference between the two response types is that FMRFamide fails to activate a 4-AP-sensitive K+ current in those LFS neurons that exhibit an exclusively excitatory response to the peptide. In addition, LFS neurons with an exclusively excitatory response tend to show a coordinated increase in the magnitude of the inward current component of the FMRFamide response. Together, these changes during the summer months may enable this modulatory peptide to bring LFS neurons to suprathreshold levels of activity for eliciting a siphon withdrawal and should substantially alter the neuromodulatory effects of the peptide.