Serotonin and the Small Cardioactive Peptides Differentially Modulate Two Motor Neurons That Innervate the Same Muscle Fibers inAplysia

Abstract

The anterior portion of intrinsic buccal muscle 3 (I3a) is innervated by two motor neurons, B3 and B38, which appear to use glutamate as their fast excitatory transmitter. B3 and B38 express the neuropeptides FMRFamide and the small cardioactive peptides (SCPs), respectively. We have shown previously that stimulation of B38 causes release of the SCPs from terminals in the muscle. The I3a muscle also receives input from neurons that use 5HT as a modulatory transmitter. The SCPs and 5HT potently facilitated B38-evoked excitatory junction potentials (EJPs) but had only a small effect on B3-evoked EJPs; however, both the SCPs and 5HT strongly potentiated contractions evoked by both B3 and B38, indicating that the two substances must also act on excitation-contraction coupling. The selective facilitation of B38-evoked EJPs, however, did manifest itself in other parameters. Decreases in the firing frequencies and burst durations that were threshold to evoke contractions and decreases in the latency between the onset of a burst and the onset of the evoked contraction were all much larger for B38 than for B3. Indeed, B38 bursts recorded during feeding-like behavior would be subthreshold for evoking contractions in the absence of this modulation. All of the effects of the SCPs reversed during washout, whereas those of 5HT were persistent, lasting many hours after washout. Thus, the SCPs and 5HT dramatically change the behavioral output of these motor neurons, increasing the amplitude of contractions evoked by both B3 and B38, and shifting the temporal relationship between bursts in B38 and its evoked contractions.

Variability of Motor Neuron Spike Timing Maintains and Shapes Contractions of the Accessory Radula Closer Muscle ofAplysia

“…In Aplysia, many other muscles, not only in the buccal mass but also, for example, in the gill musculature, resemble the ARC in the speed and nonlinearity of their neuromuscular transforms (Carew et al, 1974;Evans et al, 1996;Fox and Lloyd, 1997;Yu et al, 1999), the irregular firing of their motor neurons (Byrne et al, 1978;Morton and Chiel, 1993;Wu et al, 1994;Jing et al, 2004), and their complex modulation (Church et al, 1993;Fox and Lloyd, 1997;Evans et al, 1999;Keating and Lloyd, 1999;Hurwitz et al, 2000). With the real, irregular motor neuron spike patterns, the contractions of these muscles have shapes very much like those that we recorded here in Figures 4 -7 (Wu et al, 1994).…”

Topographic organization of efferent neurons with different neurochemical characters in the cerebral ganglia of the snailHelix pomatia

“…In Aplysia 5HT (Fox and Lloyd, 1997;Ram et al, 1981;Weiss et al, 1978) and a variety of peptides like Myomodulin (Cropper et al, 1987), small cardioactive peptides and FMRFa (Fox and Lloyd 1997) modulated (increased) the force of contraction and the rate of relaxation of buccal muscles that participate in feeding movements. CARP proved to have inhibitory modulatory effets on the contraction of different mulluscan muscles (Fujiwara-Sakata and Kobayashi, 1992;Hirata et al, 1989a,b).…”

Excitatory neurotransmitters in the tentacle flexor muscles responsible for space positioning of the snail olfactory organ

“…These muscles are innervated by cholinergic buccal (B15 and B16) and cerebral serotonergic (MCC) neurons. Activity of the MCC has no direct effect on the buccal muscles; however, the contractions elicited by stimulation of cholinergic neurons B15 and B16 are potentiated through a postsynaptic mechanism (Fox and Lloyd 1997;Weiss et al 1978;Hurwitz et al 2000). The postsynaptic site of action was further confirmed by the observation that 5-HT elicited significant decrease in the resting tone of the muscle and also accelerated the relaxing Contractions were measured by isometric recording configuration.…”