Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network

Distinct motor patterns are selected from a multifunctional neuronal network by activation of different modulatory projection neurons. Subsets of these projection neurons can contain the same neuromodulator(s), yet little is known about the relative influence of such neurons on network activity. We have addressed this issue in the stomatogastric nervous system of the crab Cancer borealis. Within this system, there is a neuronal network in the stomatogastric ganglion (STG) that produces many versions of the pyloric and gastric mill rhythms. These different rhythms result from activation of different projection neurons that innervate the STG from neighboring ganglia and modulate STG network activity. Three pairs of these projection neurons contain the neuropeptide proctolin. These include the previously identified modulatory proctolin neuron and modulatory commissural neuron 1 (MCN1) and the newly identified modulatory commissural neuron 7 (MCN7). We document here that each of these neurons contains a unique complement of cotransmitters and that each of these neurons elicits a distinct version of the pyloric motor pattern. Moreover, only one of them (MCN1) also elicits a gastric mill rhythm. The MCN7-elicited pyloric rhythm includes a pivotal switch by one STG network neuron from playing a minor to a major role in motor pattern generation. Therefore, modulatory neurons that share a peptide transmitter can elicit distinct motor patterns from a common target network.

[1]  R. Calabrese,et al.  FMRF-amide-like substances in the leech. II. Bioactivity on the heartbeat system , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  R. Harris-Warrick,et al.  Serotonergic innervation and modulation of the stomatogastric ganglion of three decapod crustaceans (Panulirus interruptus, Homarus americanus and Cancer irroratus). , 1984, The Journal of experimental biology.

[3]  P. Rudomín,et al.  Local control of information flow in segmental and ascending collaterals of single afferents , 1998, Nature.

[4]  E. Marder,et al.  Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. , 1991, Journal of neurophysiology.

[5]  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.

[6]  Jan-Marino Ramirez,et al.  The neuronal mechanisms of respiratory rhythm generation , 1996, Current Opinion in Neurobiology.

[7]  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.

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

[9]  D A Price,et al.  Release of Peptide Cotransmitters in Aplysia: Regulation and Functional Implications , 1996, The Journal of Neuroscience.

[10]  G. Zupanc Peptidergic transmission: from morphological correlates to functional implications. , 1996, Micron.

[11]  S. Grillner,et al.  Selection and initiation of motor behavior , 1997 .

[12]  M. Nusbaum,et al.  Neuropeptide degradation produces functional inactivation in the crustacean nervous system , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  K. Sigvardt,et al.  The bag cells of Aplysia as a multitransmitter system: identification of alpha bag cell peptide as a second neurotransmitter , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  E. Marder,et al.  Presynaptic control of modulatory fibers by their neural network targets , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Pierre Meyrand,et al.  A switch between two modes of synaptic transmission mediated by presynaptic inhibition , 1995, Nature.

[16]  Eve Marder,et al.  Peptidergic Modulation of Synaptic Transmission in a Rhythmic Motor System , 1997 .

[17]  R. Harris-Warrick,et al.  Dopamine modulates graded and spike-evoked synaptic inhibition independently at single synapses in pyloric network of lobster. , 1998, Journal of neurophysiology.

[18]  M. P. Nusbaum,et al.  Pyloric motor pattern modification by a newly identified projection neuron in the crab stomatogastric nervous system. , 1996, Journal of neurophysiology.

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

[20]  Immunocytochemical localization of multiple cholecystokinin-like peptides in the stomatogastric nervous system of the crab Cancer borealis. , 1995, The Journal of experimental biology.

[21]  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.

[22]  L. Holden-Dye,et al.  Evolutionary aspects of transmitter molecules, their receptors and channels , 1991, Parasitology.

[23]  M. P. Nusbaum,et al.  Motor Pattern Selection via Inhibition of Parallel Pathways , 1997, The Journal of Neuroscience.

[24]  R. Harris-Warrick,et al.  Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells. , 1989, Journal of neurophysiology.

[25]  M. P. Nusbaum,et al.  Intercircuit Control of Motor Pattern Modulation by Presynaptic Inhibition , 1997, The Journal of Neuroscience.

[26]  M. O'Shea,et al.  Neuropeptide proctolin (H-Arg-Tyr-Leu-Pro-Thr-OH): immunological detection and neuronal localization in insect central nervous system. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[27]  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.

[28]  J. Bornstein,et al.  Roles of peptides in transmission in the enteric nervous system , 1992, Trends in Neurosciences.

[29]  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.

[30]  G. Aston-Jones,et al.  Role of the locus coeruleus in emotional activation. , 1996, Progress in brain research.

[31]  R. Satterlie,et al.  Cerebral serotonergic neurons reciprocally modulate swim and withdrawal neural networks in the mollusk Clione limacina. , 1996, Journal of neurophysiology.

[32]  K. R. Weiss,et al.  Costorage and Corelease of Modulatory Peptide Cotransmitters with Partially Antagonistic Actions on the Accessory Radula Closer Muscle ofAplysia californica , 1996, The Journal of Neuroscience.

[33]  K. R. Weiss,et al.  A Cerebral Central Pattern Generator in Aplysia and Its Connections with Buccal Feeding Circuitry , 1996, The Journal of Neuroscience.

[34]  M. Sofroniew,et al.  Chapter 30 The ascending basal forebrain cholinergic system , 1996 .

[35]  E. Marder,et al.  Organization of the stomatogastric neuropil of the crab, Cancer borealis, as revealed by modulator immunocytochemistry , 1997, Cell and Tissue Research.

[36]  P. Katz,et al.  Intrinsic neuromodulation in the Tritonia swim CPG: the serotonergic dorsal swim interneurons act presynaptically to enhance transmitter release from interneuron C2 , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  D. Richter,et al.  Nucleus raphe obscurus evokes 5-HT-1A receptor-mediated modulation of respiratory neurons , 1997, Brain Research.

[38]  D. McCormick Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity , 1992, Progress in Neurobiology.

[39]  D. H. Edwards,et al.  Serotonin, social status and aggression , 1997, Current Opinion in Neurobiology.

[40]  K. R. Weiss,et al.  Analyzing the functional consequences of transmitter complexity , 1997, Trends in Neurosciences.

[41]  W. Kristan,et al.  Swim initiation in the leech by serotonin-containing interneurones, cells 21 and 61. , 1986, The Journal of experimental biology.

[42]  E. Kravitz,et al.  Mapping of serotonin-like immunoreactivity in the lobster nervous system , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  J. Lundberg Pharmacology of cotransmission in the autonomic nervous system: integrative aspects on amines, neuropeptides, adenosine triphosphate, amino acids and nitric oxide. , 1996, Pharmacological reviews.

[44]  K. Pearson Common principles of motor control in vertebrates and invertebrates. , 1993, Annual review of neuroscience.

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

[46]  H. Keshishian,et al.  Identification and distribution of a proctolin‐like neuropeptide in the nervous system of the gypsy moth, Lymantria dispar, and in other lepidoptera , 1989, The Journal of comparative neurology.

[47]  B. Jacobs,et al.  Serotonin and motor activity , 1997, Current Opinion in Neurobiology.

[48]  E. Marder,et al.  Buccalin-like and myomodulin-like peptides in the stomatogastric ganglion of the crab Cancer borealis. , 1994, The Journal of experimental biology.

[49]  K. Sillar,et al.  Aminergic Modulation of Glycine Release in a Spinal Network Controlling Swimming in Xenopus Laevis , 1997, The Journal of physiology.

[50]  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 .

[51]  E. Marder,et al.  The behavioral repertoire of the gastric mill in the crab, Cancer pagurus: an in situ endoscopic and electrophysiological examination , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  Michael P. Nusbaum,et al.  Presynaptic control of neurones in pattern-generating networks , 1994, Current Opinion in Neurobiology.

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

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

[55]  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.

[56]  S. Grillner,et al.  Differential effects of the reticulospinal system on locomotion in lamprey. , 1998, Journal of neurophysiology.

[57]  M. P. Nusbaum,et al.  Distribution of modulatory inputs to the stomatogastric ganglion of the crab, Cancer borealis , 1992, The Journal of comparative neurology.

[58]  J. Juranek,et al.  Segregation of Behavior-Specific Synaptic Inputs to a Vertebrate Neuronal Oscillator , 1998, The Journal of Neuroscience.

[59]  M J Coleman,et al.  Functional consequences of compartmentalization of synaptic input , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[61]  Brian J. Norris,et al.  Recruitment of a projection neuron determines gastric mill motor pattern selection in the stomatogastric nervous system of the crab, Cancer borealis. , 1994, Journal of neurophysiology.

[62]  S. Kombian,et al.  Peptidergic Modulation of Synaptic Transmission in the Parabrachial Nucleus In Vitro: Importance of Degradative Enzymes in Regulating Synaptic Efficacy , 1996, The Journal of Neuroscience.

[63]  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.

[64]  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.