Temporal Dynamics of Convergent Modulation at a Crustacean Neuromuscular Junction

Abstract

At least 10 different substances modulate the amplitude of nerve-evoked contractions of the gastric mill 4 (gm4) muscle of the crab, Cancer borealis. Serotonin, dopamine, octopamine, proctolin, red pigment concentrating hormone, crustacean cardioactive peptide, TNRNFLRFamide, and SDRNFLRFamide increased and -allatostatin-3 and histamine decreased the amplitude of nerve-evoked contractions. Modulator efficacy was frequency dependent; TNRNFLRFamide, proctolin, and allatostatin-3 were more effective when the motor neuron was stimulated at 10 Hz than at 40 Hz, whereas the reverse was true for dopamine and serotonin. The modulators that were most effective at high stimulus frequencies produced a significant decrease in muscle relaxation time; those that were most effective at low stimulus frequencies produced modest increases in relaxation time. Thus modulator actions that appear redundant when examined only at one stimulus frequency are differentiated when a range of stimulus dynamics is studied. The effects of TNRNFLRFamide, serotonin, proctolin, dopamine, and -allatostatin-3 on the amplitude and facilitation of nerve-evoked excitatory junctional potentials (EJPs) in the gm4 and gastric mill 6 (gm6) muscles were compared. The EJPs in gm4 have a large initial amplitude and show relatively little facilitation, whereas the EJPs in gm6 have a small initial amplitude and show considerable facilitation. Modulators that enhanced contractions also enhanced EJP amplitude; -allatostatin-3 reduced EJP amplitude. The effects of these modulators on EJP amplitude were modest and showed no significant frequency dependence. This suggests that the frequency dependence of modulator action on contraction results from effects on excitation-contraction coupling. The modulators affected facilitation at these junctions in a manner consistent with a change in release probability. They produced a change in facilitation that is inversely related to their action on EJP amplitude.

The Neuromuscular Junctions of the Slow and the Fast Excitatory Axon in the Closer of the CrabEriphia spinifronsAre Endowed with Different Ca2+Channel Types and Allow Neuron-Specific Modulation of Transmitter Release by Two Neuropeptides

“…The potentiating effect of proctolin on release at neuromuscular junctions of Eriphia is in accord with previous findings in crustaceans (Pasztor and Golas, 1993;Jorge-Rivera et al, 1998;Rathmayer et al, 2001). We show that the presynaptic targets of this modulation are -AgaTX-sensitive Ca 2ϩ channels resembling the P/Q-type.…”

“…Besides its well known postsynaptic effects, including modulation of the sarcolemmal L-type Ca 2ϩ channels , proctolin also enhances transmitter output at neuromuscular terminals in crustaceans (Pasztor and Golas, 1993;Jorge-Rivera et al, 1998;Rathmayer et al, 2001). …”

Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

“…To achieve this synaptic facilitation earlier in the response would have to be followed by synaptic depression (Markram et al, 1998;Thomson, 2000) or intermittent failure. Competing processes of synaptic facilitation and depression can act as a bandpass filter, selectively emphasizing certain frequencies in a burst of spikes (Sen et al, 1996;Jorge-Rivera et al, 1998;Izhikevich et al, 2003). This may allow different postsynaptic neurons to respond preferentially to different parts of spike train or to favor stronger responses in some postsynaptic targets.…”

Muscles innervated by a single motor neuron exhibit divergent synaptic properties on multiple time scales

“…1A,B). Like many invertebrate and lower vertebrate muscles, STNS muscles typically do not fire action potentials and have slow kinetics (Hooper et al, 1999;Jorge-Rivera et al, 1998;Weimann et al, 1997;Zhurov and Brezina, 2006;Zoccolan et al, 2002). However, 'slow' muscles vary in their ability to respond to individual action potentials and spike patterns versus the integrated spike rate of their motor neuron inputs (Daur et al, 2015;Hooper et al, 2007;Hooper, 1997, 1998;Zhurov and Brezina, 2006).…”

“…In response to a number of different modulatory inputs, LG activity consists of firing rates of 4-20 Hz (50-250 ms inter-spike intervals), burst durations of 2-8 s and interburst intervals of 2-24 s in vitro and in vivo (Beenhakker et al, 2004(Beenhakker et al, , 2005(Beenhakker et al, , 2007Blitz et al, 2004bBlitz et al, , 2008Colton and Nusbaum, 2014;DeLong and Nusbaum, 2010;Diehl et al, 2013;Hedrich et al, 2011;Kirby and Nusbaum, 2007;White and Nusbaum, 2011). Similar to central and peripheral synapses in other systems, electrical responses at neuromuscular junctions in the STNS are shaped by multiple forms of activity-dependent synaptic plasticity including depression, facilitation and augmentation (Daur et al, 2012b;Jorge-Rivera et al, 1998;Katz et al, 1993;Sen et al, 1996;Stein et al, 2006). Facilitation has been identified at some LG neuromuscular synapses in C. borealis, and augmentation and facilitation were characterized at the LG to gm6ab synapse in Cancer pagurus (Jorge-Rivera et al, 1998;Sen et al, 1996;Stein et al, 2006).…”