Neural control of swimming in Aplysia brasiliana. III. Serotonergic modulatory neurons

Abstract

1. We describe a group of serotonergic neurons in the pedal ganglia of Aplysia brasiliana and characterize their modulatory effects on the motoneuron input to swimming muscles of the parapodia. Each pedal ganglion contains one cluster of large neurons near its dorsomedial surface that fires in phase with opening (downstroke) of the parapodia; these have been designated parapodial opener-phase (POP) cells. 2. POP cells are large, number 15-20 per ganglion, have peripheral axons in parapodial nerves, have distinctively shaped action potentials, and fire in bursts phasically with motoneurons during the opening, or downstroke portion, of parapodial movement during fictive swimming. Firing individual POP cells with intracellular current indicates that they have no direct detectable effect on muscle, causing neither junction potentials nor contractions. 3. 5,7-Dihydroxytryptamine (5,7-DHT) staining, immunocytochemistry using serotonin (5-HT) antibodies, and direct biochemical measurements revealed that POP cells are serotonergic. Serotonergic nerve endings were also seen in parapodial muscle. 4. Simultaneous intracellular recordings and use of altered divalent concentrations revealed that no detectable direct synaptic interactions exist between POP cells and motor neurons. 5. When POP cells and motoneurons were simultaneously recorded while measuring muscle contractions, it was found that POP cell activity enhances motoneuron-induced tension by 120-900%, averaging around 300%. Variability in the efficacy of individual POP cells suggests that they may influence specific regions or groups of muscle fibers. 6. POP cell activity also significantly increased the rate of relaxation of parapodial muscle contractions, averaging about a 40% reduction in the time required to relax to one-half peak tension. Increased relaxation rate implies a postsynaptic change in muscle behavior. 7. The effectiveness of POP cells to increase contraction tension and relaxation rate was positively correlated with POP cell spike frequency. These effects were slow (seconds) in onset and could persist for a minute or more after cessation of POP firing. Concurrent motoneuron activity is not required for modulation by POP cells. 8. Simultaneous intracellular recording from a POP cell, motoneuron, and muscle fiber revealed that POP cell activity enhanced the amplitude of motoneuron-induced excitatory junction potentials (EJPs). Activity of POP cells did not alter muscle fiber membrane potential, but the experiments left open the possibility that EJP enhancement is presynaptic, postsynaptic, or a combination.(ABSTRACT TRUNCATED AT 400 WORDS)

Serotonin Injections Induce Metamorphosis in Larvae of the Gastropod Mollusc Ilyanassa obsoleta

“…Still, these experiments allow us to further define the locus of 5-HT activity in the larval nervous system. 5-HT plays numerous roles in molluscan nervous systems (Walker, 1986) and major groups of serotonergic neurons have been identified in several gastropod taxa (Koshtoyants et al, 1961;Walker 1986;Jahan-Parwar et al, 1987;Goldberg and Kater, 1989;Diefenbach and Goldberg, 1990;McPherson and Blankenship, 1991;Fitzgerald and Carew, 1991). For example, 5-HT regulates neurite extension and growth-cone motility in the freshwater snail Helisoma trivolvis (Price and Goldberg, 1993); stimulates motor neurons in Aplysia california (Ram et al, 1991); plays an important role in molluscan peripheral tissues, especially the heart (Walker, 1986); and heightens motor activity in embryonic gastropods in a developmentally sensitive manner (Koshtoyants et al, 1961;Diefenbach et al, 1991).…”

“…Its role as a neurotransmitter and neuromodulator in a wide range of behaviors in molluscs was extensively reviewed by Walker (1986). As examples, serotonin is active in controlling heartbeat rhythm (Liebeswar et al, 1975) and feeding and biting behaviors (Weiss et al, 1978;Kupfermann and Weiss, 1981;Gelperin, 1981;Ram et al, 1981;1991;Yeoman et al, 1994), and in modulating swimming motor patterns (Parsons and Pinsker, 1989;McPherson and Blankenship, 1991;Satterlie and Norekian, 1995). It also regulates ciliary beating in larval and adult stages of several molluscan species (Gosselin, 1961;Diefenbach and Goldberg, 1990;Diefenbach et al, 1991;Goldberg et al, 1994).…”

Systemic serotonin sulfate in opisthobranch mollusks

“…In gastropod mollusks, 5-HT is involved in many neurophysiological processes, including sensitization and facilitation of withdrawal reflexes (Hawkins et al 1993), feeding behavior (Gillette and Davis 1977) and locomotion (McPherson and Blankenship 1991). However, 5-HT-related metabolites have received considerably less attention.…”

Serotonin modulates muscle function in the medicinal leechHirudo verbana

“…However, 5-HT does enhance force production in the body wall muscle of other annelids during spontaneous [19,20], acetylcholine-induced [17] and electrically stimulated contractions [21]. There is a similar potentiating effect of 5-HT on Aplysia muscle [22], associated with a 5-HT-mediated increase in inward calcium currents across muscle cell membranes [23,24]. Confirmation of a similar 5-HT-mediated mechanism in Hirudo muscle requires further investigation.…”