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ARTICLE

Motor Pattern Specification by Dual Descending Pathways to a Lobster Rhythm-Generating Network

Denis Combes, Pierre Meyrand and John Simmers
Journal of Neuroscience 1 May 1999, 19 (9) 3610-3619; DOI: https://doi.org/10.1523/JNEUROSCI.19-09-03610.1999
Denis Combes
1Laboratoire de Neurobiologie des Réseaux, UniversitéBordeaux I and Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5816, 33405 Talence, France
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Pierre Meyrand
1Laboratoire de Neurobiologie des Réseaux, UniversitéBordeaux I and Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5816, 33405 Talence, France
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John Simmers
1Laboratoire de Neurobiologie des Réseaux, UniversitéBordeaux I and Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5816, 33405 Talence, France
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    Fig. 1.

    STNS of the lobster Homarus gammarus. A, Left lateral view of the foregut showing the STNS in situ and gastric mill muscles gm1–4, 6, and 9. B, STNS in vitro. The somata of gastric mill motoneurons (GM, LG, MG, DG, and LPG) are located in the STG, and their axons project caudally via the dorsal ventricular nerve (dvn) into their respective bilateral motor nerve roots. The two CoGs and the OG are connected to the STG via the bilateral inferior oesophageal nerves (ions), the superior oesophageal nerves (sons), and the single, mainly afferent stn.

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    Fig. 2.

    Gastric mill output patterns observed in an isolated STNS (A) and in vivo(B). A, Extracellular recordings of gastric mill motor nerves in vitro. GM motoneurons (medial tooth protraction) fire in antiphase with LPG motoneurons (lateral teeth opening; ellipse) and in phase with the MG motoneuron (lateral teeth closure). Icons on theright show teeth movements produced by each motoneuron subgroup (P, protraction; O, opening;C, closing). B, Electromyographic recordings of gastric mill muscles in vivo showing two distinct coordination patterns. B1 , Pattern similar to that seen in vitro (compare withA) in which muscles innervated by the LPG and GM motoneurons are alternately active (ellipse).B2 , Different animal in which the muscles innervated by the LPG and GM motoneurons are coordinately active (ellipse). In this pattern, protraction of the medial tooth (GM neurons) occurs with lateral teeth opening (LPG neurons).

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    Fig. 3.

    Gastric mill network of H. gammarus. A, Dual intrasomatic recordings that reveal probable monosynaptic inhibitory connections. Eachpanel shows superimposed oscilloscope sweeps triggered by impulses in the presynaptic LG neuron. B, Synaptic wiring diagram derived from recordings as in A.Stick and ball symbol, Chemical inhibitory synapse;resistor symbol, electrical coupling.Numbers denote the number of neurons of each type. Neurons of each functional group are electrically coupled, including the LG–MG neurons. Tooth movement driven by each neuron type is also indicated: O, C, opening and closing of lateral teeth, respectively; P, R, protraction and retraction of medial tooth, respectively.C, Anatomical evidence for 10 GM motoneurons after cobalt (CoCl2) backfill from their axons in the dagn; 10 STG somata are labeled.

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    Fig. 4.

    CG interneuron interactions with the gastric mill network. A, Superimposed sweeps showing CG neuron-derived EPSPs in the LPG and GM neurons but not in the LG neuron. Schema at top right shows the synaptic relationship between the CG neuron and the gastric mill network. B, Suprathreshold depolarization of the CG neuron excites the GM and LG neurons but inhibits the LPG neuron (left). However, when the LG neuron is continuously hyperpolarized by intracellular current injection (right), CG neuron stimulation now causes coordinated LPG and GM neuron excitation. Calibration: vertical bars, 10 mV; horizontal bar, 2 sec.

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    Fig. 5.

    Electrical coupling between GM and LG motoneurons. Depolarization of one (top left) or two (top right) GM neurons by current injection (arrows) depolarizes the LG neuron. Hyperpolarization of one (bottom left) or two (bottom right) GM neurons by current injection (arrows) hyperpolarizes the LG neuron. Note the increased postsynaptic response when both GM neurons are manipulated with current. Calibration: vertical bars, 20 mV; horizontal bar, 1 sec.

  • Fig. 6.
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    Fig. 6.

    The CG interneuron excites the LG neuron via the GM neurons. A, Stimulation of the CG neuron by intracellular current injection excites the LG neuron and, after a slight excitation (asterisk), inhibits an LPG neuron. Note that the smaller depolarizing transients in the CG neuron are action potentials, whereas the larger potentials are EPSPs (insets are CG neuron recordings on faster time base).B, After photoinactivation of Lucifer yellow-filled GM neurons by intense blue light illumination, CG neuron depolarization no longer activates the LG neuron and now excites the LPG neurons.C, LG neuron activation by current injection during CG neuron stimulation still causes LPG neuron inhibition. Calibration:vertical bars, 10 mV; horizontal bars, 1 sec.

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    Fig. 7.

    Identification of descending commissural GI interneuron. A, Camera lucida drawing of a Lucifer yellow-stained GI neuron in the right CoG; the GI neuron soma lies between the emergence of the ion and son through which its axon runs toward the stn. CG neuron soma position in the same CoG is also indicated. B, Each GI neuron spike is correlated 1:1 with an axonal spike recorded extracellularly in the son and then in the stn (5 superimposed oscilloscope sweeps). Calibration:vertical bar, 5 mV; horizontal bar, 2 msec. C, Geometry of GI neurons in the STNS; their somata are located one in each CoG and their axons project to the STG via the son and the stn.

  • Fig. 8.
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    Fig. 8.

    Synaptic relationship of the GI interneuron with the gastric mill network. A, Depolarization of the GI neuron inhibits the LG (top), MG (middle), and DG (bottom) neurons.B, Faster time base (5 sweeps in each recording). Each GI neuron spike is correlated 1:1 with a constant latency IPSP (arrows) in the MG, DG, and LG neurons. Diagram atright summarizes these synaptic relations. Calibration:vertical bars, A, 10 mV;B, 5 mV; horizontal bars,A, 2 sec; B, 10 msec.

  • Fig. 9.
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    Fig. 9.

    Different gastric mill patterns encounteredin vivo can be reproduced in vitro by activating the CG and GI interneurons. Schema summarizes synaptic relationships between descending CG and GI neurons and the gastric mill network. A, Periodic depolarization of a tonically active CG neuron alone generates a gastric mill pattern that resembles a type I pattern (LPG and GM neurons fire out of phase;ellipse) seen spontaneously in vivo.B, In the same preparation, rhythmic activation of the GI neuron alone also produces a pattern in which LPG and GM neuron bursts are in phase opposition. Here, however, the LPG neuron fires in phase with the stimulated interneuron. C, Simultaneous activation of the CG and GI interneurons organizes gastric mill activity into a type II-like pattern, similar to that spontaneously expressed in vivo; here, the LPG and GM neurons fire in phase (ellipse) and in antiphase with the MG neuron.

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The Journal of Neuroscience: 19 (9)
Journal of Neuroscience
Vol. 19, Issue 9
1 May 1999
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Motor Pattern Specification by Dual Descending Pathways to a Lobster Rhythm-Generating Network
Denis Combes, Pierre Meyrand, John Simmers
Journal of Neuroscience 1 May 1999, 19 (9) 3610-3619; DOI: 10.1523/JNEUROSCI.19-09-03610.1999

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Motor Pattern Specification by Dual Descending Pathways to a Lobster Rhythm-Generating Network
Denis Combes, Pierre Meyrand, John Simmers
Journal of Neuroscience 1 May 1999, 19 (9) 3610-3619; DOI: 10.1523/JNEUROSCI.19-09-03610.1999
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Keywords

  • crustacea
  • Homarus gammarus
  • stomatogastric nervous system
  • central pattern generator
  • projection interneurons
  • network reconfiguration

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