Synaptic actions of identified peptidergic neuron R15 in Aplysia. I. Activation of respiratory pumping

Abstract

The purpose of the study described in this and the following two companion papers was to determine the synaptic actions of neuron R15, an endogenously bursting neurosecretory cell in Aplysia, as a step toward determining its physiological function. The results described in this paper demonstrate that activity in R15 increases the frequency of bursting in the R25/L25 network that triggers respiratory pumping. This excitatory modulatory effect appears to be mediated by R15 alpha 1 peptide. R15 activates both strong and weak modes of respiratory pumping. In contrast, the two R20 cells, which are thought to use the neuropeptides SCPA and SCPB as transmitters, elicit only strong episodes of respiratory pumping. The synaptic actions of R15 also differ from those of the R20 cells in being longer lasting and in exhibiting profound desensitization. Chronic recording of R15 activity in vivo indicates that it does not burst spontaneously in the intact animal, so the synaptic actions of R15 are not chronically desensitized. The neuroendocrine bag cells, which initiate egg laying, had been shown by others to excite R15 and the R25/L25 network that triggers respiratory pumping. Our data indicate that the excitatory effects of the bag cells on the R25/L25 cells are mediated in part by R15.

Operant Conditioning of Gill Withdrawal inAplysia

“…*p Ͻ 0.05 compared with the matched control animals. EXT or Ext, Extinction; PRE, pretest period; Con, control; Exp, experimental. involve changes in the biophysical properties or synaptic connections of the L25 and R25 neurons, which are the major elements of the pattern generator for the contractions (Byrne and Koester, 1978;Byrne, 1983;Koester, 1989), and changes in the frequency of spontaneous contractions could involve changes in the firing or effects of the peptidergic modulatory neurons R15 and R20 (Alevizos et al, 1989(Alevizos et al, , 1991, which produce slow excitation of the L25 and R25 neurons. Such changes in the properties of neurons in a central pattern generator are thought to contribute to operant conditioning of feeding in Aplysia (Nargeot et al, 1999a,b;Brembs et al, 2002) and may also contribute to operant conditioning of aerial respiration in Lymnea (Spencer et al, 1999(Spencer et al, , 2002Scheibenstock et al, 2002).…”

Respiratory pumping in Aplysia fasciata as part of an integrated defensive response to increases and decreases in seawater concentration

“…The R20 cells contain a number of peptides, including two previously-identified, SCPA and SCPB (Alevizos et al 1989). Stimulating an R20 neuron, or application of SCPB, activates respiratory pumping in a decelerating activity pattern (Alevizos et al 1991) similar to that seen in response to shock, decrease in pH, and to 75% or 140% seawater. These data suggest that the R20 neurons may activate respiratory pumping in a defensive context, in response to many noxious stimuli.…”

“…However, this response is unlikely to be related to regulation of respiratory pumping. Excitation of R15, rather than its inhibition, can initiate respiratory pumping (Alevizos et al 1991). In addition, hyperpolarization of R15 is signaled by receptors that respond to a decrease in osmolarity, rather than to a decrease in salt content (Stinnakre and Tauc 1969).…”

“…Stimulating the bag cells which release egg-laying hormone (ELH) increases the pump rate (Schaefer and Brownell 1986), as does stimulating neuron R15, which has been postulated to have a role in initiating egg-laying (Alevizos et al 1991). Respiratory pumping is also increased during female mating and courtship .…”

“…The L25 and R25 interneurons of the abdominal ganglion act as both command ceils and central pattern generators for respiratory pumping (Byrne 1983;Byrne and Koester 1978;Koester 1989). Neurons that modulate the activity of the L25 and R25 cells, and so change the frequency of respiratory pumping, have also been identified (Alevizos et al 1989(Alevizos et al , 1991Cleary et al 1991;Schaefer and Brownell 1986). However, despite the information available on the circuitry controlling the gill, the natural functions of the behaviors in which gill contractions occur are incompletely understood.…”