Mechanosensory gating of proprioceptor input to modulatory projection neurons

Journal of Neuroscience

Volumn 27, Issue 52, 2007, Pages 14308-14316

  Beenhakker, Mark P ^a,b   Kirby, Matthew S ^a   Nusbaum, Michael P ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Central pattern generator; Convergence; Gastric mill circuit; Rhythms; State dependent; Stomatogastric

Indexed keywords

ANIMAL TISSUE; ARTICLE; CRAB; MECHANORECEPTOR; MOTOR ACTIVITY; NERVE PROJECTION; NEUROMODULATION; NONHUMAN; PATTERN GENERATOR; PRIORITY JOURNAL; PROPRIOCEPTION; SENSORIMOTOR FUNCTION;

ANALYSIS OF VARIANCE; ANIMALS; BRACHYURA; DIGESTIVE SYSTEM; GANGLIA, INVERTEBRATE; MALE; MECHANORECEPTORS; MEMBRANE POTENTIALS; MOTOR NEURONS; NERVE NET; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONS, AFFERENT; PERIODICITY; PHYSICAL STIMULATION;

EID: 37549058038     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4404-07.2007     Document Type: Article

References (51)

1. Bartos M, Nusbaum MP (1997) Intercircuit control of motor pattern modulation by presynaptic inhibition. J Neurosci 17:2247-2256.
2. Beenhakker MP, Nusbaum MP (2004) Mechanosensory activation of a motor circuit by coactivation of two projection neurons. J Neurosci 24:6741-6750.
3. Beenhakker MP, Blitz DM, Nusbaum MP (2004) Long-lasting activation of rhythmic neuronal activity by a novel mechanosensory system in the crustacean stomatogastric nervous system. J Neurophysiol 91:78-91.
4. Beenhakker MP, DeLong ND, Saideman SR, Nadim F, Nusbaum MP (2005) Proprioceptor regulation of motor circuit activity by presynaptic inhibition of a modulatory projection neuron. J Neurosci 25:8794-8806.
5. Blitz DM, Nusbaum MP (1997) Motor pattern selection via inhibition of parallel pathways. J Neurosci 17:4965-4975.
6. Blitz DM, Nusbaum MP (2007) Mechanosensory regulation of invertebrate motor systems. In: Invertebrate Neurobiology (eds North G, Greenspan RJ), pp185-208. Cold Spring Harbor Laboratory Press: NY.
7. Blitz DM, Christie AE, Coleman MJ, Norris BJ, Marder E, Nusbaum MP (1999) Different proctolin neurons elicit distinct motor patterns from a multifunctional neuronal network. J Neurosci 19:5449-5463.
8. Blitz DM, Beenhakker MP, Nusbaum MP (2004) Different sensory systems share projection neurons but elicit distinct motor patterns. J Neurosci 24:11381-11390.
9. Briggman KL, Abarbanel HD, Kristan WB (2005) Optical imaging of neuronal populations during decision-making. Science 307:896-901.
10. Buschges A, El Manira A (1998) Sensory pathways and their modulation in the control of locomotion. Curr Opin Neurobiol 8:733-739.
11. Cattaert D, Le Bon M, Le Ray D (2002) Efferent controls in crustacean mechanoreceptors. Microsc Res Tech 58:312-324.
12. Christie AE, Stein W, Quinlan JE, Beenhakker MP, Marder E, Nusbaum MP (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.
13. Coleman MJ, Nusbaum MP (1994) Functional consequences of compartmentalization of synaptic input. J Neurosci 14:6544-6552.
14. Coleman MJ, Nusbaum MP, Cournil I, Claiborne BJ (1992) Distribution of modulatory inputs to the stomatogastric ganglion of the crab, Cancer borealis. J Comp Neurol 325:581-594.
15. Coleman MJ, Meyrand P, Nusbaum MP (1995) A switch between two modes of synaptic transmission mediated by presynaptic inhibition. Nature 378:502-505.
16. Combes D, Simmers AJ, Moulins M (1995) Structural and functional characterization of a muscle tendon proprioceptor in lobster. J Comp Neurol 363:221-234.
17. Combes D, Meyrand P, Simmers J (1999) Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster. J Neurosci 19:3620-3628.
18. DeLong ND, Nusbaum MP (2006) Comparable sensory influence on related rhythmic motor patterns via distinct synaptic mechanisms. Soc Neurosci Abstr 350.6.
19. DiCaprio RA (1999) Gating of afferent input by a central pattern generator. J Neurophysiol 81:950-953.
20. El Manira A, Clarac F (1994) Presynaptic inhibition is mediated by histamine and GABA in the crustacean escape reaction. J Neurophysiol 71:1088-1095.
21. El Manira A, Tegner J, Grillner S (1997a) Locomotor-related presynaptic modulation of primary afferents in the lamprey. Eur J Neurosci 9:696-705.
22. El Manira A, Zhang W, Svensson E, Bussieres N (1997b) 5-HT inhibits calcium current and synaptic transmission from sensory neurons in lamprey. J Neurosci 17:1786-1794.
23. Evans CG, Jing J, Rosen SC, Cropper EC (2003) Regulation of spike initiation and propagation in an Aplysia sensory neuron: gating-in via central depolarization. J Neurosci 23:2920-2931.
24. Frost WN, Tian LM, Hoppe TA, Mongeluzi DL, Wang J (2003) A cellular mechanism for prepulse inhibition. Neuron 40:991-1001.
25. Katz PS (2003) Synaptic gating: the potential to open closed doors. Curr Biol 13:R554-R556.
26. Katz PS, Harris-Warrick RM (1989) 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.
27. Katz PS, Harris-Warrick RM (1991) Recruitment of crab gastric mill neurons into the pyloric motor pattern by mechanosensory afferent stimulation. J Neurophysiol 65:1442-1451.
28. Katz PS, Eigg MH, Harris-Warrick RM (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.
29. Lomeli J, Quevedo J, Linares P, Rudomin P (1998) Local control of information flow in segmental and ascending collaterals of single afferents. Nature 395:600-604.
30. Marder E, Bucher D (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu Rev Physiol 69:291-316.
31. Meyrand P, Simmers J, Moulins M (1994) Dynamic construction of a neural network from multiple pattern generators in the lobster stomatogastric nervous system. J Neurosci 14:630-644.
32. Norris BJ, Coleman MJ, Nusbaum MP (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.
33. Norris BJ, Coleman MJ, Nusbaum MP (1996) Pyloric motor pattern modification by a newly identified projection neuron in the crab stomatogastric nervous system. J Neurophysiol 75:97-108.
34. Nusbaum MP, Beenhakker MP (2002) A small-systems approach to motor pattern generation. Nature 417:343-350.
35. Nusbaum MP, Contreras D (2004) Sensorimotor gating: startle submits to presynaptic inhibition. Curr Biol 14:R247-R249.
36. Nusbaum MP, El Manira A, Gossard JP, Rossignol S (1997) Presynaptic mechanisms during rhythmic activity in vertebrates and invertebrates. In: Neurons, Networks and Motor Behav (eds Stein PSG, Grillner S, Selverston A, Stuart DG), pp. 237-253. Cambridge, MA: MIT Press.
37. Parker D, Grillner S (1996) Tachykinin-mediated modulation of sensory neurons, interneurons, and synaptic transmission in the lamprey spinal cord. J Neurophysiol 76:4031-4039.
38. Perrins R, Walford A, Roberts A (2002) Sensory activation and role of inhibitory reticulospinal neurons that stop swimming in hatchling frog tadpoles. J Neurosci 22:4229-4240.
39. Pieroni JP, Byrne JH (1992) Differential effects of serotonin, FMRFamide, and small cardioactive peptide on multiple, distributed processes modulating sensorimotor synaptic transmission in Aplysia. J Neurosci 12:2633-2647.
40. Rossignol S, Dubuc R, Gossard JP (2006) Dynamic sensorimotor interactions in locomotion. Physiol Rev 86:89-154.
41. Rudomin P (2002) Central control of information transmission through the intraspinal arborizations of sensory fibers examined 100 years after Ramon y Cajal. Prog Brain Res 136:409-421.
42. Rudomin P, Lomeli J, Quevedo J (2004) Differential modulation of primary afferent depolarization of segmental and ascending intraspinal collaterals of single muscle afferents in the cat spinal cord. Exp Brain Res 156:377-391.
43. Saideman SR, Ma M, Kutz-Naber KK, Cook A, Torfs P, Schoofs L, Li L, Nusbaum MP (2007a) Modulation of rhythmic motor activity by pyrokinin peptides. J Neurophysiol 97:579-595.
44. Saideman SR, Blitz DM, Nusbaum MP (2007b) Convergent motor patterns from divergent circuits. J Neurosci 27:6664-6674.
45. Smarandache CR, Stein W (2007) Sensory-induced modification of two motor patterns in the crab, Cancer pagurus. J Exp Biol 210:2912-2922.
46. Stein W, DeLong ND, Wood DE, Nusbaum MP (2007) Divergent cotransmitter actions underlie motor pattern activation by a modulatory projection neuron. Eur J Neurosci 26:1148-1165.
47. Swensen AM, Marder E (2000) Multiple peptides converge to activate the same voltage-dependent current in a central pattern-generating circuit. J Neurosci 20:6752-6759.
48. Swensen AM, Marder E (2001) Modulators with convergent cellular actions elicit distinct circuit outputs. J Neurosci 21:4050-4058.
49. Viana di Prisco G, Pearlstein E, Le Ray D, Robitaille R, Dubuc R (2000) A cellular mechanism for the transformation of a sensory input into a motor command. J Neurosci 20:8169-8176.
50. Weimann JM, Meyrand P, Marder E (1991) Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric nervous system. J Neurophysiol 65:111-122.
51. Wood DE, Manor Y, Nadim F, Nusbaum MP (2004) Intercircuit control via rhythmic regulation of projection neuron activity. J Neurosci 24:7455-7463.