CONTROL OF CENTRAL PATTERN GENERATORS BY AN IDENTIFIED NEURONE IN CRUSTACEA: ACTIVATION OF THE GASTRIC MILL MOTOR PATTERN BY A NEURONE KNOWN TO MODULATE THE PYLORIC NETWORK

Summary In the red lobster (Palinurus vulgaris), an identified neurone, the anterior pyloric modulator neurone (APM), which has previously been shown to modulate the output of the pyloric central pattern generator, was shown to modulate the output of the gastric mill central pattern generator. APM activity induced a rhythm when the network was silent and increased rhythmic activity when the network was already active. Rhythmic activity was induced whether APM fired in single bursts, tonically or in repetitive bursts. A single burst in APM induced a rhythm which considerably outlasted the burst, whereas repetitive bursts effectively entrained the gastric oscillator. These modulations involved two major mechanisms. (1) APM induced or enhanced plateau properties in some of the gastric mill neurones. (2) APM activated the extrinsic inputs to the network, thus increasing the excitatory synaptic drive to most of the neurones of the network. As a result, when APM was active, all the neurones of the pattern generator actively participated in the rhythmic activity. By its actions on two separate but behaviourally related neural networks, the APM neurone may be able to control an entire concert of related types of behaviour.

[1]  R. Robertson,et al.  Oscillatory command input to the motor pattern generators of the crustacean stomatogastric ganglion , 2004, Journal of Comparative Physiology A.

[2]  W. Kristan,et al.  The dual role of serotonin in leech swimming. , 1982, Journal de physiologie.

[3]  D. F. Russell Rhythmic excitatory inputs to the lobster stomatogastric ganglion , 1976, Brain Research.

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

[5]  R. Robertson,et al.  Control of rhythmic behaviour by a hierarchy of linked oscillators in crustacea , 1981, Neuroscience Letters.

[6]  D. F. Russell,et al.  Bursting neural networks: a reexamination. , 1978, Science.

[7]  H. Chiel,et al.  Sensory function and gating of histaminergic neuron C2 in Aplysia , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  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.

[9]  I Kupfermann,et al.  Modulatory actions of neurotransmitters. , 1979, Annual review of neuroscience.

[10]  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 .

[11]  M. Moulins,et al.  Participation of an Unpaired Motor Neurone in the Bilaterally Organized Oesophageal Rhythm in the Lobsters Jasus Lalandii and Palinurus Vulgaris , 1981 .

[12]  M. Moulins,et al.  Suppressive control of a rhythmic central pattern generator by an identified modulatory neuron in crustacea , 1987, Neuroscience Letters.

[13]  M. Moulins,et al.  A disynaptic sensorimotor pathway in the lobster stomatogastric system. , 1988, Journal of neurophysiology.

[14]  Allen I. Selverston,et al.  Neural Mechanisms for the Production of the Lobster Pyloric Motor Pattern , 1985 .

[15]  D. F. Russell Pattern and reset analysis of the gastric mill rhythm in a spiny lobster, Panulirus interruptus. , 1985, The Journal of experimental biology.

[16]  J. Miller,et al.  Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. I. Pyloric system. , 1980, Journal of neurophysiology.

[17]  W. B. Adams,et al.  The generation and modulation of endogenous rhythmicity in the Aplysia bursting pacemaker neurone R15. , 1985, Progress in biophysics and molecular biology.

[18]  D. A. Brown,et al.  M‐currents and other potassium currents in bullfrog sympathetic neurones , 1982, The Journal of physiology.

[19]  H. Chiel,et al.  An identified histaminergic neuron modulates feeding motor circuitry in Aplysia , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  A. Selverston,et al.  Oscillatory neural networks. , 1985, Annual review of physiology.

[21]  J. Miller,et al.  Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. IV. Network properties of pyloric system. , 1982, Journal of neurophysiology.

[22]  A. Selverston Gastric Mill Mechanisms , 1987 .

[23]  L. Kaczmarek,et al.  Neuromodulation : the biochemical control of neuronal excitability , 1987 .

[24]  D. F. Russell,et al.  Synaptic regulation of cellular properties and burst oscillations of neurons in gastric mill system of spiny lobsters, Panulirus interruptus. , 1984, Journal of neurophysiology.

[25]  D F Russell,et al.  Endogenous burst capability in a neuron of the gastric mill pattern generator of the spiny lobster Panulirus interruptus. , 1984, Journal of neurobiology.

[26]  R. Nicoll Neurotransmitters can say more than just ‘yes’ or ‘no’ , 1982, Trends in Neurosciences.

[27]  H. C. Hartzell,et al.  Mechanisms of slow postsynaptic potentials , 1981, Nature.

[28]  A. Selverston,et al.  Organization of the stomatogastric ganglion of the spiny lobster , 2004, Journal of comparative physiology.

[29]  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.

[30]  M. O'Shea,et al.  Neuropeptide function: the invertebrate contribution. , 1985, Annual review of neuroscience.

[31]  A. Selverston,et al.  The stomatogastric nervous system: Structure and function of a small neural network , 1976, Progress in Neurobiology.

[32]  P. S. Dickinson,et al.  Control of a central pattern generator by an identified modulatory interneurone in crustacea. I. Modulation of the pyloric motor output. , 1983, The Journal of experimental biology.

[33]  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.

[34]  W. Kristan,et al.  Neurons controlling the initiation, generation and modulation of leech swimming. , 1983, Symposia of the Society for Experimental Biology.

[35]  P. S. Dickinson,et al.  Control of a central pattern generator by an identified modulatory interneurone in crustacea. II. Induction and modification of plateau properties in pyloric neurones. , 1983, The Journal of experimental biology.

[36]  D F Russell,et al.  Neural basis of teeth coordination during gastric mill rhythms in spiny lobsters, Panulirus interruptus. , 1985, The Journal of experimental biology.

[37]  J. Miller,et al.  Cooperative mechanisms for the production of rhythmic movements. , 1983, Symposia of the Society for Experimental Biology.

[38]  A. Selverston,et al.  The Crustacean Stomatogastric System , 1987, Springer Berlin Heidelberg.

[39]  E. Marder,et al.  Modulation of a central pattern generator by two neuropeptides, proctolin and FMRFamide , 1984, Brain Research.

[40]  Modulation of Central and Peripheral Rhythmicity in the Heartbeat System of the Leech , 1985 .

[41]  D. Hartline,et al.  Motor patterns in the stomatogastric ganglion of the lobster Panulirus argus. , 1975, The Journal of experimental biology.

[42]  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.

[43]  H. Chiel,et al.  Activity of an identified histaminergic neuron, and its possible role in arousal of feeding behavior in semi-intact Aplysia , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[45]  M. O'Shea,et al.  The identification of an octopaminergic neurone and the modulation of a myogenic rhythm in the locust. , 1978, The Journal of experimental biology.

[46]  Irving Kupfermann,et al.  NEURAL AND MOLECULAR MECHANISMS OF FOOD-INDUCED AROUSAL IN APLYSIA CALIFORNIA , 1981 .

[47]  D. F. Russell,et al.  Slow active potentials and bursting motor patterns in pyloric network of the lobster, Panulirus interruptus. , 1982, Journal of neurophysiology.

[48]  J. Truman,et al.  Hormonal control of the development and release of rhythmic ecdysis behaviours in insects. , 1983, Symposia of the Society for Experimental Biology.

[49]  M. Moulins,et al.  Control by an identified modulatory neuron of the sequential expression of plateau properties of, and synaptic inputs to, a neuron in a central pattern generator , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  S. Grillner Locomotion in the Spinal Cat , 1973 .

[51]  H Wachtel,et al.  Prolonged inhibition in burst firing neurons: synaptic inactivation of the slow regenerative inward current. , 1978, Science.

[52]  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.

[53]  H. Gainer,et al.  Peptide Regulation of Bursting Pacemaker Activity in a Molluscan Neurosecretory Cell , 1974, Science.

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

[55]  G. Augustine,et al.  The neuropeptide proctolin acts directly onLimulus cardiac muscle to increase the amplityde of contraction , 1981, Brain Research.