Temporal dynamics of convergent modulation at a crustacean neuromuscular junction.

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.

[1]  C. Govind,et al.  Synaptic Structure and Transmitter Release in Crustacean Phasic and Tonic Motor Neurons , 1998, The Journal of Neuroscience.

[2]  Quigley,et al.  Physiological effects of two FMRFamide-related peptides from the crayfish Procambarus clarkii , 1995, Journal of Experimental Biology.

[3]  D. Maynard,et al.  The structure of the stomatogastric neuromuscular system in Callinectes sapidus, Homarus americanus and Panulirus argus (Decapoda Crustacea). , 1974, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[4]  E. Marder,et al.  1 – Modulatory control of multiple task processing in the stomatogastric nervous system , 1992 .

[5]  The effects of myomodulin and structurally related neuropeptides on skeletal neuromuscular transmission in the locust. , 1994, The Journal of experimental biology.

[6]  E Marder,et al.  A modulatory proctolin-containing neuron (MPN). II. State-dependent modulation of rhythmic motor activity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  I. Kupfermann,et al.  Release of peptide cotransmitters from a cholinergic motor neuron under physiological conditions. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[8]  E. Marder,et al.  Principles of rhythmic motor pattern generation. , 1996, Physiological reviews.

[9]  M. Moulins,et al.  Muscarinic modulation of a pattern-generating network: control of neuronal properties , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  P W Gean,et al.  Isoproterenol potentiates synaptic transmission primarily by enhancing presynaptic calcium influx via P- and/or Q-type calcium channels in the rat amygdala , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  J. Jorge-Rivera,et al.  Allatostatin decreases stomatogastric neuromuscular transmission in the crab Cancer borealis. , 1997, The Journal of experimental biology.

[12]  E Marder,et al.  Matching neural and muscle oscillators: control by FMRFamide-like peptides , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  E. Marder,et al.  Decoding Synapses , 1996, The Journal of Neuroscience.

[14]  K. R. Weiss,et al.  Enhancement of Ca current in the accessory radula closer muscle of Aplysia californica by neuromodulators that potentiate its contractions , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  E. Marder,et al.  Modulatory action and distribution of the neuropeptide proctolin in the crustacean stomatogastric nervous system , 1986, The Journal of comparative neurology.

[16]  E. Marder,et al.  Matrix of neuromodulators in neurosecretory structures of the crab Cancer borealis. , 1995, The Journal of experimental biology.

[17]  L. Abbott,et al.  A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex , 1997, The Journal of Neuroscience.

[18]  S. L. Hooper,et al.  Physiology and biochemistry of peptidergic cotransmission in Aplysia , 1993, Journal of Physiology-Paris.

[19]  E Marder,et al.  Modulation of Oscillator Interactions in the Crab Stomatogastric Ganglion by Crustacean Cardioactive Peptide , 1997, The Journal of Neuroscience.

[20]  E Marder,et al.  The effects of SDRNFLRFamide and TNRNFLRFamide on the motor patterns of the stomatogastric ganglion of the crab Cancer borealis. , 1993, The Journal of experimental biology.

[21]  M. Bear,et al.  Metaplasticity: the plasticity of synaptic plasticity , 1996, Trends in Neurosciences.

[22]  Eve Marder,et al.  Neurotransmitter Modulation of the Stomatogastric Ganglion of Decapod Crustaceans , 1985 .

[23]  A. Selverston,et al.  Mechanisms of gastric rhythm generation in the isolated stomatogastric ganglion of spiny lobsters: bursting pacemaker potentials, synaptic interactions, and muscarinic modulation. , 1992, Journal of neurophysiology.

[24]  E. Kravitz,et al.  Peptide F1, an N-terminally extended analog of FMRFamide, enhances contractile activity in multiple target tissues in lobster. , 1995, The Journal of experimental biology.

[25]  S. Hooper,et al.  Muscle Response to Changing Neuronal Input in the Lobster (Panulirus interruptus) Stomatogastric System: Spike Number- versus Spike Frequency-Dependent Domains , 1997, The Journal of Neuroscience.

[26]  E. Kravitz,et al.  The action of serotonin on excitatory nerve terminals in lobster nerve‐muscle preparations. , 1982, The Journal of physiology.

[27]  I. Cooke,et al.  Fluorescence localization of monoamines in crab neurosecretory structures. , 1970, The Journal of experimental biology.

[28]  WG Regehr,et al.  A quantitative analysis of presynaptic calcium dynamics that contribute to short-term enhancement , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  H. Atwood,et al.  Synaptic differentiation of a single motor neuron: conjoint definition of transmitter release, presynaptic calcium signals, and ultrastructure , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  E. Marder.  Cholinergic motor neurones in the stomatogastric system of the lobster. , 1976, The Journal of physiology.

[31]  R. Harris-Warrick,et al.  Aminergic modulation in lobster stomatogastric ganglion. I. Effects on motor pattern and activity of neurons within the pyloric circuit. , 1986, Journal of neurophysiology.

[32]  I. V. Orekhova,et al.  Functional Uncoupling of Linked Neurotransmitter Effects by Combinatorial Convergence , 1996, Science.

[33]  P. Katz,et al.  Facilitation and depression at different branches of the same motor axon: evidence for presynaptic differences in release , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  E. Marder.  Neurotransmitters and Neuromodulators , 1987 .

[35]  Brian J. Norris,et al.  Identification of motor neurons that contain a FMRFamidelike peptide and the effects of FMRFamide on longitudinal muscle in the medicinal leech, Hirudo medicinalis , 1987, The Journal of comparative neurology.

[36]  M. Siegler,et al.  Octopamine mediated relaxation of maintained and catch tension in locust skeletal muscle. , 1982, The Journal of physiology.

[37]  P. S. Dickinson,et al.  Neurotransmitter interactions in the stomatogastric system of the spiny lobster: one peptide alters the response of a central pattern generator to a second peptide. , 1997, Journal of neurophysiology.

[38]  E. Marder,et al.  Distribution and effects of tachykinin‐like peptides in the stomatogastric nervous system of the crab, Cancer borealis , 1995, The Journal of comparative neurology.

[39]  E. Marder,et al.  A NEURONAL ROLE FOR A CRUSTACEAN RED PIGMENT CONCENTRATING HORMONE-LIKE PEPTIDE: NEUROMODULATION OF THE PYLORIC RHYTHM IN THE CRAB, CANCER BOREALIS , 1988 .

[40]  Block of glutamatergic excitatory synaptic channels by chlorisondamine. , 1981, Molecular pharmacology.

[41]  E. Schuman,et al.  Neurotrophin-induced modulation of synaptic transmission in the adult hippocampus , 1995, Journal of Physiology-Paris.

[42]  I Kupfermann,et al.  Multiple neuropeptides in cholinergic motor neurons of Aplysia: evidence for modulation intrinsic to the motor circuit. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[43]  P. Skiebe,et al.  Allatostatin peptides in the crab stomatogastric nervous system: inhibition of the pyloric motor pattern and distribution of allatostatin-like immunoreactivity. , 1994, The Journal of experimental biology.

[44]  M. P. Nusbaum,et al.  Two novel tachykinin-related peptides from the nervous system of the crab Cancer borealis. , 1997, The Journal of experimental biology.

[45]  M. O'Shea,et al.  Physiological consequences of a peptide cotransmitter in a crayfish nerve-muscle preparation , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  J. T. Hackett,et al.  Facilitation at the lobster neuromuscular junction: a stimulus-dependent mobilization model. , 1997, Journal of neurophysiology.

[47]  Peter D. Evans,et al.  Peptidergic and Aminergic Modulation of Insect Skeletal Muscle , 1986 .

[48]  R. Harris-Warrick.  In: Dynamic Biological Networks: The Stomatogastric Nervous System , 1992 .

[49]  R. Harris-Warrick,et al.  Aminergic modulation in lobster stomatogastric ganglion. II. Target neurons of dopamine, octopamine, and serotonin within the pyloric circuit. , 1986, Journal of neurophysiology.

[50]  C. Lingle.  The Modulatory Action of Dopamine on Crustacean Foregut Neuromuscular Preparations , 1981 .

[51]  S. W. Kuffler,et al.  Presynaptic inhibition at the crayfish neuromuscular junction , 1961, The Journal of physiology.

[52]  K. Weiss,et al.  Activation of K current in the accessory radula closer muscle of Aplysia californica by neuromodulators that depress its contractions , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  E Marder,et al.  A modulatory proctolin-containing neuron (MPN). I. Identification and characterization , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  E Marder,et al.  Modulation of the lobster pyloric rhythm by the peptide proctolin , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  E. Marder,et al.  Distribution and partial characterization of FMRFamide‐like peptides in the stomatogastric nervous systems of the rock crab, Cancer borealis, and the spiny lobster, Panulirus interruptus , 1987, The Journal of comparative neurology.

[56]  E. Marder,et al.  Switching neurons are integral members of multiple oscillatory networks , 1994, Current Biology.

[57]  P. Evans.  Studies on the mode of action of octopamine, 5-hydroxytryptamine and proctolin on a myogenic rhythm in the locust. , 1984, The Journal of experimental biology.

[58]  H. Atwood,et al.  Short-term and long-term plasticity and physiological differentiation of crustacean motor synapses. , 1986, International review of neurobiology.