Differential activation of projection neurons by two sensory pathways contributes to motor pattern selection

Journal of Neurophysiology

Volumn 102, Issue 5, 2009, Pages 2866-2879

  Hedrich, Ulrike B S ^a   Smarandache, Carmen R ^a   Stein, Wolfgang ^a  

^a UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CRAB; GANGLION; INFERIOR VENTRICULAR NEURON; MODULATORY COMMISSURAL NEURON 1; MODULATORY COMMISSURAL NEURON 5; MOTOR ACTIVITY; NERVE CELL; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; STOMATOGASTRIC NERVOUS SYSTEM;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANALYSIS OF VARIANCE; ANIMALS; BRACHYURA; MODELS, BIOLOGICAL; MOTOR ACTIVITY; NEURAL INHIBITION; PERIODICITY; PHYSICAL STIMULATION; SENSORY RECEPTOR CELLS; STOMATOGNATHIC SYSTEM;

EID: 70350606097     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00618.2009     Document Type: Article

References (54)

1. Barriere G, Simmers J, Combes D. Multiple mechanisms for integrating proprioceptive inputs that converge on the same motor pattern-generating network. J Neurosci 28: 8810-8820, 2008.
2. Bartos M, Manor Y, Nadim F, Marder E, Nusbaum MP. Coordination of fast and slow rhythmic neuronal circuits. J Neurosci 19: 6650-6660, 1999. (Pubitemid 29347465)
3. Bartos M, Nusbaum MP. Intercircuit control of motor pattern modulation by presynaptic inhibition. J Neurosci 17: 2247-2256, 1997. (Pubitemid 27137392)
4. Beenhakker MP, Blitz DM, Nusbaum MP. Long-lasting activation of rhythmic neuronal activity by a novel mechanosensory system in the crustacean stomatogastric nervous system. J Neurophysiol 91: 78-91, 2004.
5. Beenhakker MP, DeLong ND, Saideman SR, Nadim F, Nusbaum MP. Proprioceptor regulation of motor circuit activity by presynaptic inhibition of a modulatory projection neuron. J Neurosci 25: 8794-8806, 2005. (Pubitemid 41362058)
6. Beenhakker MP, Kirby MS, Nusbaum MP. Mechanosensory gating of proprioceptor input to modulatory projection neurons. J Neurosci 27: 14308-14316, 2007.
7. Beenhakker MP, Nusbaum MP. Mechanosensory activation of a motor circuit by coactivation of two projection neurons. J Neurosci 24: 6741-6750, 2004.
8. Blitz DM, Beenhakker MP, Nusbaum MP. Different sensory systems share projection neurons but elicit distinct motor patterns. J Neurosci 24: 11381-11390, 2004.
9. Blitz DM, Nusbaum MP. Motor pattern selection via inhibition of parallel pathways. J Neurosci 17: 4965-4975, 1997.
10. Blitz DM, Nusbaum MP. Distinct functions for cotransmitters mediating motor pattern selection. J Neurosci 19: 6774-6783, 1999.
11. Cabelguen JM, Bourcier-Lucas C, Dubuc R. Bimodal locomotion elicited by electrical stimulation of the midbrain in the salamander Notophthalmus viridescens. J Neurosci 23: 2434-2439, 2003.
12. Cazalets JR, Nagy F, Moulins M. Suppressive control of the crustacean pyloric network by a pair of identified interneurons. I. Modulation of the motor pattern. J Neurosci 10: 448-457, 1990. (Pubitemid 20089067)
13. Chevallier S, Jan Ijspeert A, Ryczko D, Nagy F, Cabelguen JM. Organisation of the spinal central pattern generators for locomotion in the salamander: biology and modelling. Brain Res Rev 57: 147-161, 2008. (Pubitemid 350213104)
14. Christie AE, Stein W, Quinlan JE, Beenhakker MP, Marder E, Nusbaum MP. Actions of a histaminergic/peptidergic projection neuron on rhythmic motor patterns in the stomatogastric nervous system of the crab Cancer borealis. J Comp Neurol 469: 153-169, 2004. (Pubitemid 38083867)
15. Coleman MJ, Meyrand P, Nusbaum MP. A switch between two modes of synaptic transmission mediated by presynaptic inhibition. Nature 378: 502-505, 1995.
16. Coleman MJ, Nusbaum MP. Functional consequences of compartmentalization of synaptic input. J Neurosci 14: 6544-6552, 1994.
17. Coleman MJ, Nusbaum MP, Cournil I, Claiborne BJ. Distribution of modulatory inputs to the stomatogastric ganglion of the crab, Cancer borealis. J Comp Neurol 325: 581-594, 1992.
18. Combes D, Meyrand P, Simmers J. Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster. J Neurosci 19: 3620-3628, 1999a. (Pubitemid 29203140)
19. Combes D, Meyrand P, Simmers J. Motor pattern specification by dual descending pathways to a lobster rhythm-generating network. J Neurosci 19: 3610-3619, 1999b. (Pubitemid 29203139)
20. Combes D, Simmers J, Moulins M. Structural and functional characterization of a muscle tendon proprioceptor in lobster. J Comp Neurol 363: 221-234, 1995.
21. Dubuc R, Brocard F, Antri M, Fenelon K, Gariepy JF, Smetana R, Menard A, Le Ray D, Viana Di Prisco G, Pearlstein E, Sirota MG, Derjean D, St-Pierre M, Zielinski B, Auclair F, Veilleux D. Initiation of locomotion in lampreys. Brain Res Rev 57: 172-182, 2008.
22. Elson RC, Panchin YV, Arshavsky YI, Selverston AI. Multiple effects of an identified proprioceptor upon gastric pattern generation in spiny lobsters. J Comp Physiol [A] 174: 317-329, 1994.
23. Esch T, Kristan WB Jr. Decision-making in the leech nervous system. Integr Comp Biol 42: 716, 2002.
24. Esch T, Mesce KA, Kristan WB. Evidence for sequential decision making in the medicinal leech. J Neurosci 22: 11045-11054, 2002. (Pubitemid 36005181)
25. Gutierrez GJ, Grashow RG. Cancer borealis stomatogastric nervous system dissection. JoVE. 25. http://www.jove.com/index/details.stp?id=1207, doi: 10.3791/1207.
26. Hedrich UB, Stein W. Characterization of a descending pathway: activation and effects on motor patterns in the brachyuran crustacean stomatogastric nervous system. J Exp Biol 211: 2624-2637, 2008.
27. Heinzel HG, Weimann JM, Marder E. The behavioral repertoire of the gastric mill in the crab, Cancer pagurus: an in situ endoscopic and electrophysiological examination. J Neurosci 13: 1793 - 1803, 1993.
28. Hess D, Büschges A. Sensorimotor pathways involved in interjoint reflex action of an insect leg. J Neurobiol 33: 891-913, 1997. (Pubitemid 27513681)
29. Hess D, Büschges A. Role of proprioceptive signals from an insect femur-tibia joint in patterning motoneuronal activity of an adjacent leg joint. J Neurophysiol 81: 1856-1865, 1999.
30. Katz PS. Neuromodulation and motor pattern generation in the crustacean stomatogastric nervous system. In: Neural Control of Movements, edited by Ferrell WR, Proske U. New York: Plenum Press, 1995, p. 277-283.
31. Katz PS, Harris-Warrick RM. Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. II. Rapid nicotinic and prolonged modulatory effects on neurons in the stomatogastric ganglion. J Neurophysiol 62: 571-581, 1989.
32. Katz PS, Harris-Warrick RM. Recruitment of crab gastric mill neurons into the pyloric motor pattern by mechanosensory afferent stimulation. J Neurophysiol 65: 1442-1451, 1991.
33. Marder E, Calabrese RL. Principles of rhythmic motor pattern generation. Physiol Rev 76: 687-717, 1996. (Pubitemid 26286076)
34. Meyrand P, Simmers J, Moulins M. Construction of a pattern-generating circuit with neurons of different networks. Nature 351: 60-63, 1991. (Pubitemid 21896534)
35. Meyrand P, Simmers J, Moulins M. Dynamic construction of a neural network from multiple pattern generators in the lobster stomatogastric nervous system. J Neurosci 14: 630-644, 1994. (Pubitemid 24043920)
36. Morgan PT, Jing J, Vilim FS, Weiss KR. Interneuronal and peptidergic control of motor pattern switching in Aplysia. J Neurophysiol 87: 49-61, 2002. (Pubitemid 34669929)
37. Mulloney B, Selverston AI. Organization of the stomatogastric ganglion of the spiny lobster. I. Neurons driving the lateral teeth. J Comp Physiol [A] Sens Neural Behav Physiol 91: 1-32, 1974.
38. Norris BJ, Coleman MJ, Nusbaum MP. Recruitment of a projection neuron determines gastric mill motor pattern selection in the stomatogastric nervous system of the crab, Cancer borealis. J Neurophysiol 72: 1451-1463, 1994.
39. Norris BJ, Coleman MJ, Nusbaum MP. Pyloric motor pattern modification by a newly identified projection neuron in the crab stomatogastric nervous system. J Neurophysiol 75: 97-108, 1996.
40. Nusbaum MP, Beenhakker MP. A small-systems approach to motor pattern generation. Nature 417: 343-350, 2002.
41. Nusbaum MP, Marder E. A modulatory proctolin-containing neuron (MPN). I. Identification and characterization. J Neurosci 9: 1591-1599, 1989a. (Pubitemid 19146255)
42. Nusbaum MP, Marder E. A modulatory proctolin-containing neuron (MPN). II. State-dependent modulation of rhythmic motor activity. J Neurosci 9: 1600-1607, 1989b. (Pubitemid 19146256)
43. Rossignol S, Dubuc R, Gossard JP. Dynamic sensorimotor interactions in locomotion. Physiol Rev 86: 89-154, 2006.
44. Selverston AI, Mulloney B. Organization of the stomatogastric ganglion of the spiny lobster. II. Neurons driving the medial tooth. J Comp Physiol [A]: Neuroethol Sens Neural Behav Physiol 91: 33-51, 1974.
45. Sigvardt KA, Mulloney B. Properties of synapses made by IVN command-interneurones in the stomatogastric ganglion of the spiny lobster Panulirus interruptus. J Exp Biol 97: 153-168, 1982a.
46. Sigvardt KA, Mulloney B. Sensory alteration of motor patterns in the stomatogastric nervous system of the spiny lobster Panulirus interruptus. J Exp Biol 97: 137-152, 1982b.
47. Simmers J, Moulins M. A disynaptic sensorimotor pathway in the lobster stomatogastric system. J Neurophysiol 59: 740-756, 1988a. (Pubitemid 18101394)
48. Simmers J, Moulins M. Nonlinear interneuronal properties underlie integrative flexibility in a lobster disynaptic sensorimotor pathway. J Neurophysiol 59: 757-777, 1988b. (Pubitemid 18101395)
49. Smarandache CR, Daur N, Hedrich U, Stein W. Regulation of motor pattern frequency by reversals in proprioceptive feedback. Eur J Neurosci 28: 460-474, 2008. (Pubitemid 352040420)
50. Smarandache CR, Stein W. Sensory-induced modification of two motor patterns in the crab, Cancer pagurus. J Exp Biol 210: 2912-2922, 2007. (Pubitemid 47401660)
51. Stein W, DeLong ND, Wood DE, Nusbaum MP. Divergent co-transmitter actions underlie motor pattern activation by a modulatory projection neuron. Eur J Neurosci 26: 1148-1165, 2007. (Pubitemid 47346762)
52. Stein W, Smarandache CR, Nickmann M, Hedrich UB. Functional consequences of activity-dependent synaptic enhancement at a crustacean neuromuscular junction. J Exp Biol 209: 1285-1300, 2006.
53. Takakusaki K. Forebrain control of locomotor behaviors. Brain Res Rev 57: 192-198, 2008.
54. Weimann JM, Meyrand P, Marder E. Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. J Neurophysiol 65: 111-122, 1991.