A newly identified extrinsic input triggers a distinct gastric mill rhythm via activation of modulatory projection neurons

Journal of Experimental Biology

Volumn 211, Issue 6, 2008, Pages 1000-1011

  Blitz, Dawn M ^a   White, Rachel S ^a   Saideman, Shari R ^a,f   Cook, Aaron ^a   Christie, Andrew E ^b,c   Nadim, Farzan ^d,e   Nusbaum, Michael P ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

^d NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

^e RUTGERS UNIVERSITY   (United States)

^f Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Cancer borealis; Central pattern generator; Neuromodulation; Neuropeptide; Projection neurons

Indexed keywords

NEUROPEPTIDE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BRACHYURA; ELECTROSTIMULATION; HISTOLOGY; IN VITRO STUDY; INNERVATION; INTESTINE INNERVATION; MALE; MASTICATION; NERVE CELL; PHYSIOLOGY; STOMACH;

ANIMALS; BRACHYURA; ELECTRIC STIMULATION; ENTERIC NERVOUS SYSTEM; MALE; MASTICATION; MODELS, NEUROLOGICAL; NEURONS; NEUROPEPTIDES; STOMACH;

ANIMALIA; CANCER BOREALIS; DECAPODA (CRUSTACEA);

EID: 42549156687     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.015222     Document Type: Article

References (75)

1. Alexandrowicz, J. S. (1951). Muscle receptor organs in the abdomen of Homarus vulgaris and Palinurus vulgaris. Q. J. Microsc. Sci. 92, 163-199.
2. Bartos, M. and Nusbaum, M. P. (1997). Intercircuit control of motor pattern modulation by presynaptic inhibition. J. Neurosci. 17, 2247-2256.
3. Bartos, M., Manor, Y., Nadim, F., Marder, E. and Nusbaum, M. P. (1999). Coordination of fast and slow rhythmic neuronal circuits. J. Neurosci. 19, 6650-6660.
4. Beenhakker, M. P. and Nusbaum, M. P. (2004). Mechanosensory activation of a motor circuit by coactivation of two projection neurons. J. Neurosci. 24, 6741-6750.
5. Beenhakker, M. P., Blitz, D. M. and Nusbaum, M. P. (2004). Long-lasting activation of rhythmic neuronal activity by a novel mechanosensory system in the crustacean stomatogastric nervous system. J. Neurophysiol. 91, 78-91.
6. Blitz, D. M. and Nusbaum, M. P. (1997). Motor pattern selection via inhibition of parallel pathways. J. Neurosci. 17, 4965-4975.
7. Blitz, D. M. and Nusbaum, M. P. (1999). Distinct functions for cotransmitters mediating motor pattern selection. J. Neurosci. 19, 6774-6783.
8. Blitz, D. M., Christie, A. E., Coleman, M. J., Norris, B. J., Marder, E. and Nusbaum, M. P. (1999). Different proctolin neurons elicit distinct motor patterns from a multifunctional neuronal network. J. Neurosci. 19, 5449-5463.
9. Blitz, D. M., Beenhakker, M. P. and Nusbaum, M. P. (2004). Different sensory systems share projection neurons but elicit distinct motor patterns. J. Neurosci. 24, 11381-11390.
10. Bramble, D. M. and Carrier, D. R. (1983). Running and breathing in mammals. Science 219, 251-256.
11. Brocard, F., Bardy, C. and Dubuc, R. (2005). Modulatory effect of substance P to the brain stem locomotor command in lampreys. J. Neurophysiol. 93, 2127-2141.
12. Cardi, P. and Nagy, F. (1994). A rhythmic modulatory gating system in the stomatogastric nervous system of Homarus gammarus. III. Rhythmic control of the pyloric CPG. J. Neurophysiol. 71, 2503-2516.
13. Cattaert, D., Le Bon, M. and Le Ray, D. (2002). Efferent controls in crustacean mechanoreceptors. Microsc. Res. Tech. 58, 312-324.
14. Christie, A. E., Lundquist, C. T., Nassel, D. R. and Nusbaum, M. P. (1997). Two novel tachykinin-related peptides from the nervous system of the crab Cancer borealis. J. Exp. Biol. 200, 2279-2294.
15. Christie, A. E., Stein, W., Quinlan, J. E., Beenhakker, M. P., Marder, E. and Nusbaum, M. P. (2004). 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.
16. Clemens, S., Combes, D., Meyrand, P. and Simmers, J. (1998). Long term expression of two interacting motor pattern-generating networks in the stomatogastric system of freely behaving lobster. J. Neurophysiol. 79, 1396-1408.
17. Coleman, M. J. and Nusbaum, M. P. (1994). Functional consequences of compartmentalization of synaptic input. J. Neurosci. 11, 6544-6552.
18. Coleman, M. J., Nusbaum, M. P., Cournil, I. and Claiborne, B. J. (1992). Distribution of modulatory inputs to the stomatogastric ganglion of the crab, Cancer borealis. J. Comp. Neurol. 325, 581-594.
19. Coleman, M. J., Meyrand, P. and Nusbaum, M. P. (1995). A switch between two modes of synaptic transmission mediated by presynaptic inhibition. Nature 378, 502-505.
20. Combes, D., Simmers, A. J. and Moulins, M. (1995). Structural and functional characterization of a muscle tendon proprioceptor in lobster. J. Comp. Neurol. 363, 221-234.
21. Combes, D., Meyrand, P. and Simmers, J. (1999). Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster. J. Neurosci. 19, 3620-3628.
22. Di Prisco, G. V., Pearlstein, E., Robitaille, R. and Dubuc, R. (1997). Role of sensory-evoked NMDA plateau potentials in the initiation of locomotion. Science 278, 1122-1125.
23. Di Prisco, G. V., Pearlstein, E., Le Ray, D., Robitaille, R. and Dubuc, R. (2000). A cellular mechanism for the transformation of a sensory input into a motor command. J. Neurosci. 20, 8169-8176.
24. Fleischer, A. G. (1981). The effect of eyestalk hormones on the gastric mill in the intact lobster Panulirus interruptus. J. Comp. Physiol. 141, 363-368.
25. Fort, T. J., Brezina, V. and Miller, M. W. (2004). Modulation of an integrated central pattern generator-effector system: dopaminergic regulation of cardiac activity in the blue crab Callinectes sapidus. J. Neurophysiol. 92, 3455-3470.
26. Georgopoulos, A. P. (1995). Current issues in directional motor control. Trends Neurosci. 18, 506-510.
27. Goldberg, D., Nusbaum, M. P. and Marder, E. (1988). Substance P-like immunoreactivity in the stomatogastric nervous systems of the crab Cancer borealis and the lobsters Panulirus interruptus and Homarus americanus. Cell Tissue Res. 252, 515-522.
28. Gordon, I. T. and Whelan, P. J. (2006). Deciphering the organization and modulation of spinal locomotor central pattern generators. J. Exp. Biol. 209, 2007-2014.
29. Heinzel, H. G. (1988). Gastric mill activity in the lobster. I. Spontaneous modes of chewing. J. Neurophysiol. 59, 528-550.
30. Heinzel, H. G., Weimann, J. M. and Marder, E. (1993). The behavioral repertoire of the gastric mill in the crab, Cancer pagurus: an in situ endoscopic and electrophysiological examination. J. Neurosci. 13, 1793-1803.
31. Hooper, S. L. and Moulins, M. (1990). Cellular and synaptic mechanisms responsible for a long-lasting restructuring of the lobster pyloric network. J. Neurophysiol. 64, 1574-1589.
32. Horridge, G. A. (1965). Arthropoda: general anatomy. In Structure and Function in the Nervous System of Invertebrates (ed. T. H. Bullock and G. A. Horridge), pp. 801-964. San Francisco: W. H. Freeman.
33. Jorge-Rivera, J. C. and Marder, E. (1996). TNRNFLRFamide and SDRNFLRFamide modulate muscles of the stomatogastric system of the crab Cancer borealis. J. Comp. Physiol. A 179, 741-751.
34. Jung, L. J. and Scheller, R. H. (1991). Peptide processing and targeting in the neuronal secretory pathway. Science 251, 1330-1335.
35. Katz, P. S. and Harris-Warrick, R. M. (1990). Neuromodulation of the crab pyloric central pattern generator by serotonergic/cholinergic proprioceptive afferents. J. Neurosci. 10, 1495-1512.
36. Katz, P. S., Eigg, M. H. and Harris-Warrick, R. M. (1989) Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells. J. Neurophysiol. 62, 558-570.
37. Kawahara, K., Kumagai, S., Nakazono, Y. and Myamoto, Y. (1989). Coupling between respiratory and stepping rhythms during locomotion in decerebrate cats. J. Appl. Physiol. 67, 110-115.
38. Kiehn, O. (2006). Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci. 29, 279-306.
39. Kirby, M. S. and Nusbaum, M. P. (2007). Central nervous system projections to and from the commissural ganglion of the crab Cancer borealis. Cell Tissue Res. 328, 625-637.
40. Kristan, W. B. and Shaw, B. K. (1997). Population coding and behavioral choice. Curr. Opin. Neurobiol. 7, 826-831.
41. LeBeau, F. E., El Manira, A. and Grillner, S. (2005). Tuning the network: modulation of neuronal microcircuits in the spinal cord and hippocampus. Trends Neurosci. 28, 552-561.
42. Lewis, J. E. and Kristan, W. B. (1998). A neuronal network for computing population vectors in the leech. Nature 391, 76-79.
43. Liu, K. S. and Fetcho, J. R. (1999). Laser ablations reveal functional relationships of segmental hindbrain neurons. Neuron 23, 325-335.
44. Loechner, K. J. and Kaczmarek, L. K. (1994). Autoactive peptides act at three distinct receptors to depolarize the bag cell neurons of Aplysia. J. Neurophysiol. 71, 195-203.
45. Ludwig, M. and Pittman, Q. J. (2003). Talking back: dendritic neurotransmitter release. Trends Neurosci. 26, 255-261.
46. Marder, E. and Bucher, D. (2007). Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu. Rev. Physiol. 69, 291-316.
47. Marder, E., Bucher, D., Schulz, D. J. and Taylor, A. L. (2005). Invertebrate central pattern generation moves along. Curr. Biol. 15, R685-R699.
48. Mayeri, E. (1979). Local hormonal modulation of neural activity in Aplysia. Fed. Proc. 38, 2103-2108.
49. McLean, D. L. and Sillar, K. T. (2004). Metamodulation of a spinal locomotor network by nitric oxide. J. Neurosci. 24, 9561-9571.
50. Messinger, D. I., Kutz, K. K., Le T., Verley, D. R., Hsu, Y. W., Ngo, C. T., Cain, S. D., Birmingham, J. T., Li, L. and Christie, A. E. (2005). Identification and characterization of a tachykinin-containing neuroendocrine organ in the commissural ganglion of the crab Cancer productus. J. Exp. Biol. 208, 3303-3319.
51. Meyrand, P., Simmers, J. and Moulins, M. (1994). Dynamic construction of a neural network from multiple pattern generators in the lobster stomatogastric nervous system. J. Neurosci. 14, 630-644.
52. Morin, D. and Viala, D. (2002). Coordinations of locomotor and respiratory rhythms in vitro are critically dependent on hindlimb sensory inputs. J. Neurosci. 22, 4756-4765.
53. Norris, B. J., Coleman, M. J. and Nusbaum, M. P. (1994). 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.
54. Nusbaum, M. P. and Beenhakker, M. P. (2002). A small-systems approach to motor pattern generation. Nature 417, 343-350.
55. Nusbaum, M. P., Blitz, D. M., Swensen, A. M., Wood, D. and Marder, E. (2001). The roles of co-transmission in neural network modulation. Trends Neurosci. 24, 146-154.
56. Oliet, S. H., Baimoukhametova, D. V., Piet, R. and Bains, J. S. (2007). Retrograde regulation of GABA transmission by the tonic release of oxytocin and endocannabinoids governs postsynaptic firing. J. Neurosci. 27, 1325-1333.
57. Parker, D. and Grillner, S. (1999). Long-lasting substance-P-mediated modulation of NMDA-induced rhythmic activity in the lamprey locomotor network involves separate RNA- and protein-synthesis-dependent stages. Eur. J. Neurosci. 11, 1515-1522.
58. Saideman, S. R., Ma, M., Kutz-Naber, K. K., Cook, A., Torfs, P., Schoofs, L., Li, L. and Nusbaum, M. P. (2007a). Modulation of rhythmic motor activity by pyrokinin peptides. J. Neurophysiol. 97, 579-595.
59. Saideman, S. R., Blitz, D. M. and Nusbaum, M. P. (2007b). Convergent motor patterns from divergent circuits. J. Neurosci. 27, 6664-6674.
60. Saunders, S. W., Rath, D. and Hodges, P. W. (2004). Postural and respiratory activation of the trunk muscles changes with mode and speed of locomotion. Gait Posture 20, 280-290.
61. Sigvardt, K. A., Rothman, B. S., Brown, R. O. and Mayeri, E. (1986). The bag cells of Aplysia as a multitransmitter system: identification of alpha bag cell peptide as a second neurotransmitter. J. Neurosci. 6, 803-813.
62. Skiebe, P. and Schneider, H. (1994). Allatostatin peptides in the crab stomatogastric nervous system: inhibition of the pyloric motor pattern and distribution of allatostatin-like immunoreactivity. J. Exp. Biol. 194, 195-208.
63. Smarandache, C. R. and Stein, W. (2007). Sensory-induced modification of two motor patterns in the crab, Cancer pagurus. J. Exp. Biol. 210, 2912-2922.
64. Smetana, R. W., Alford, S. and Dubuc, R. (2007). Muscarinic receptor activation elicits sustained, recurring depolarizations in reticulospinal neurons. J. Neurophysiol. 97, 3181-3192.
65. Stein, W., DeLong, N. D., Wood, D. E. and Nusbaum, M. P. (2007). Divergent cotransmitter actions underlie motor pattern activation by a modulatory projection neuron. Eur. J. Neurosci. 26, 1148-1165.
66. Stemmler, E. A., Peguero, B., Bruns, E. A., Dickinson, P. S. and Christie, A. E. (2007). Identification, physiological actions, and distribution of TPSGFLGMRamide: a novel tachykinin-related peptide from the midgut and stomatogastric nervous system of Cancer crabs. J. Neurochem. 101, 1351-1366.
67. Syed, N. I. and Winlow, W. (1991). Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones. J. Exp. Biol. 158, 37-62.
68. Treptow, K., Oehme, P., Gäbler, E. and Bienert, M. (1983). Modulation of locomotor activity by substance P in rats. Regul. Pept. 5, 343-351.
69. Tryba, A. K., Pena, F. and Ramirez, J. M. (2006). Gasping activity in vitro: a rhythm dependent on 5-HT2A receptors. J. Neurosci. 26, 2623-2634.
70. Turrigiano, G. G. and Selverston, A. I. (1990). A cholecystokinin-like hormone activates a feeding-related neural circuit in lobster. Nature 344, 866-868.
71. Weimann, J. M. and Marder, E. (1994). Switching neurons are integral members of multiple oscillatory networks. Curr. Biol. 4, 896-902.
72. Weimann, J. M., Meyrand, P. and Marder, E. (1991). 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.
73. White, R. S., Nadim, F. and Nusbaum, M. P. (2005). Activation of a peripheral modulatory system elicits a distinct gastric mill rhythm. Abstr. Soc. Neurosci. 2005, 722.52.
74. Wood, D. E., Stein, W. and Nusbaum, M. P. (2000). Projection neurons with shared cotransmitters elicit different motor patterns from the same neural circuit. J. Neurosci. 20, 8943-8953.
75. Wood, D. E., Manor, Y., Nadim, F. and Nusbaum, M. P. (2004). Intercircuit control via rhythmic regulation of projection neuron activity. J. Neurosci. 24, 7455-7563.