A dynamic network simulation of the nematode tap withdrawal circuit: Predictions concerning synaptic function using behavioral criteria

Journal of Neuroscience

Volumn 16, Issue 12, 1996, Pages 4017-4031

  Wicks, Stephen R ^a   Roehrig, Chris J ^a   Rankin, Catharine H ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Caenorhabditis elegans; habituation; inhibition; lesion; mechanosensory; reflex

Indexed keywords

ARTICLE; ASCARIS; BEHAVIOR; CELL JUNCTION; INTEGRATED CIRCUIT; MOTONEURON; NEMATODE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROBABILITY; STEADY STATE; SYNAPTIC TRANSMISSION;

EID: 0029948031     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-12-04017.1996     Document Type: Article

References (66)

1. Achacoso TB, Yamamoto WS (1992) AY's neuroanatomy of C. elegans for computation. Boca Raton, FL: CRC.
2. Arena JP, Liu KK, Paress PS, Schaeffer JM, Cully DF (1992) Expression of a glutamate-activated chloride current in Xenopus oocytes injected with Caenorhabditis elegans RNA: evidence for modulation by avermectin. Mol Brain Res 15:339-348.
3. Avery L, Horvitz HR (1987) A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant. Cell 51:1071-1078.
4. Avery L, Horvitz HR (1989) Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron 3:473-485.
5. Avery L, Raizen D, Lockery S (1995) Electrophysiological methods. In: Caenorhabditis elegans: modern biological analysis of an organism (Epstein HF, Shakes DC, eds), pp 251-269. San Diego: Academic.
6. Bargmann CI, Horvitz HR (1991) Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7:729-742.
7. Bennett MVL (1972) A comparison of electrically and chemically mediated transmission. In: Structure and function of synapses (Pappas GD, Purpura DP, eds), pp 221-256. New York: Raven.
8. Blazis DEJ, Fischer TM, Carew TJ (1993) A neural network model of inhibitory information processing in Aplysia. Neural Comput 5:213-227.
9. Brenner S (1974) The genetics of the nematode Caenorhabditis elegans. Genetics 77:71-94.
10. Carew TJ, Pinsker HM, Kandel ER (1972) Long-term habituation of a defensive reflex in Aplysia. Science 175:451-454.
11. Chalfie M, Sulston J (1981) Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 82:358-370.
12. Chalfie M, White JG (1988) The nervous system. In: The nematode Caenorhabditis elegans (Wood WB, ed), pp 337-392. Cold Spring Harbor, NY: Cold Spring Harbor.
13. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S (1985) The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5:956-964.
14. Corfas G, Dudai Y (1990) Adaptation and fatigue of a mechanosensory neuron in wild-type Drosophila and in memory mutants. J Neurosci 10:491-499.
15. Davis RE, Stretton AOW (1989a) Passive membrane properties of motorneurons and their role in long-distance signaling in the nematode Ascaris. J Neurosci 9:403-414.
16. Davis RE, Stretton AOW (1989b) Signaling properties of Ascaris motorneurons: graded active responses, graded synaptic transmission, and tonic transmitter release. J Neurosci 9:415-425.
17. DeSchutter E, Angstadt JD, Calabrese RL (1993) A model of graded synaptic transmission for use in dynamic network simulations. J Neurophysiol 69:1225-1235.
18. du Lac S, Raymond JL, Sejnowski TJ, Lisberger SG (1995) Learning and memory in the vestibulo-ocular reflex. Annu Rev Neurosci 18:409-441.
19. Dusenbury DB (1974) Analysis of chemotaxis in the nematode Caenorhabditis elegans by countercurrent separation. J Exp Zool 188:41-47.
20. Erdös P, Niebur E (1993) Theory of locomotion of nematodes: control of the somatic motor neurons by interneurons. Math Biosci 118:51-82.
21. Fischer TM, Carew TJ (1993) Activity-dependent regulation of recurrent inhibition: a mechanism for dynamic gain control in the siphon withdrawal reflex of Aplysia. J Neurosci 13:1302-1314.
22. Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12:185-204.
23. Gross RE, Bagchi S, Lu X, Rubin CS (1990) Cloning, characterization, and expression of the gene for the catalytic subunit of cAMP-dependent protein kinase in Caenorhabditis elegans. J Biol Chem 265:6896-6907.
24. Groves PM, De Marco R, Thompson RF (1969) Habituation and sensitization of spinal interneuron activity in acute spinal cat. Brain Res 14:521-525.
25. Hall DH, Russell RL (1991) The posterior nervous system of the nematode Caenorhabditis elegans: serial reconstruction of identified neurons and complete pattern of synaptic interactions. J Neurosci 11:1-22.
26. Harris-Warrick RM, Nagy F, Nusbaum MP (1992) Neuromodulation of stomatogastric networks by identified neurons and neurotransmitters. In: Dynamic neural networks (Harris-Warrick RM, Marder E, Selverston AI, Moulins M, eds), pp 87-137. Cambridge, MA: MIT.
27. Horvitz HR, Chalfie M, Trent C, Sulston JE, Evans PD (1982) Serotonin and octopamine in the nematode C. elegans. Science 216:1012-1014.
28. Kandel ER, Schwartz JH (1982) Molecular biology of learning: modulation of transmitter release. Science 218:433-442.
29. Krasne FB (1969) Excitation of habituation of the crayfish escape reflex: the depolarizing response in lateral giant fibers in the isolated abdomen. J Exp Biol 50:29-46.
30. Lockery SR, Sejnowski TJ (1992) Distributed processing of sensory information in the leech. III. A dynamic neural network of the local bending reflex. J Neurosci 12:3877-3895.
31. Lockery SR, Nolan SJ, Sejnowski TJ (1993) Modeling chemotaxis in the nematode C. elegans. In: Computation and neural systems (Eeckman FH, Bower JM, eds), pp 249-254. Boston: Kluwer Academic.
32. Loer CM, Kenyon CJ (1994) Serotonin-deficient mutants and male mating-behavior in the nematode Caenorhabditis elegans. J Neurosci 13:5407-5417.
33. Lu X, Gross RE, Bagchi S, Rubin CS (1990) Cloning, structure, and expression of the gene for a novel regulatory subunit of cAMPdependent protein kinase in Caenorhabditis elegans. J Biol Chem 265:3293-3303.
34. McIntire SL, Jorgensen E, Kaplan J, Horvitz HR (1993) The GABAergic nervous system of Caenorhabditis elegans. Nature 364:337-341.
35. Mendel JE, Korswagen HC, Liu KS, Hajdu-Cronin YM, Simon MI, Plasterk RHA, Sternberg PW (1995) Participation of the protein G(o) in multiple aspects of behavior in C. elegans. Science 167:1652-1655.
36. Niebur E (1988) Théorie du système locomoteur et neuronal des nématodes. PhD thesis, University of Lausanne.
37. Niebur E, Erdös P (1991) Theory of the locomotion of nematodes: dynamics of undulatory progression on a surface. Biophys J 60:1132-1146.
38. Niebur E, Erdös P (1993) Theory of the locomotion of nematodes: control of the somatic motor neurons by interneurons. Math Biosci 118:51-82.
39. Nonet ML, Grundahl K, Meyer BJ, Rand JB (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73:1291-1305.
40. Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1988) Numerical recipes in C: the art of scientific computing. Cambridge, UK: Cambridge UP.
41. Raizen DM, Avery L (1994) Electrical activity and behavior in the pharynx of Caenorhabditis elegans. Neuron 12:483-495.
42. Rail WB (1977) Core conductor theory and cable properties of neurons. In: Handbook of physiology: the nervous system, Vol 1 (Kandel ER, ed), pp 39-97. Bethesda, MD: American Physiological Society.
43. Rail WB (1989) Cable theory for dendritic neurons. In: Methods in neuronal modeling: from synapses to networks (Kock C, Segev I, eds), pp 9-62. Cambridge MA: MIT.
44. Rankin CH (1991) Interactions between two antagonistic reflexes in the nematode Caenorhabditis elegans. J Comp Physiol [A] 169:59-67.
45. Rankin CH, Beck CDO, Chiba CM (1990) Caenorhabditis elegans: a new model system for the study of learning and memory. Behav Brain Res 37:89-92.
46. Roehrig C, Wicks SR, Rankin CH (1994) Determination of synaptic polarities using a computational cellular model of the nematode tap withdrawal reflex. Soc Neurosci Abstr 20:1201.
47. Savage C, Hamelin M, Culotti JG, Coulson A, Albertson DG, Chalfic M (1989) mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev 3:870-881.
48. Segalat L, Elkes DA, Kaplan JM (1995) Modulation of serotonincontrolled behaviors by G(o) in Caenorhabditis elegans. Science 267:1648-1651.
49. Segev I, Fleshman JW, Burke RE (1989) Compartmental models of complex neurons. In: Methods in neuronal modeling: from synapses to networks (Kock C, Segev I, eds), pp 63-96. Cambridge, MA:MIT.
50. Selverston AI (1985) Model neural networks and behavior. New York: Plenum.
51. Sherrington C (1906) The integrative action of the nervous system. New Haven, CT: Yale UP.
52. Siegal S (1956) Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill.
53. Steinmetz JE, Lavond DG, Ivkovich D, Logan CG, Thompson RF (1992) Disruption of classical eyelid conditioning after cerebellar lesions: damage to a memory trace system or a simple performance deficit. J Neurosci 12:4403-4426.
54. Stern MJ, DeVore DL (1994) Extending and connecting signaling pathways in C. elegans. Dev Biol 166:443-459.
55. Stretton A, Donmoyer J, Davis R, Meade J, Cowden C, Sithigorngul P (1992) Motor behavior and motor nervous system function in the nematode Ascaris suum. J Parasitol 78:206-214.
56. Sulston JE, White JG (1980) Regulation and cell autonomy during post-embryonic development of Caenorhabditis elegans. Dev Biol 78:577-597.
57. Sulston JE, Dew M, Brenner S (1975) Dopaminergic neurons in the nematode Caenorhabditis elegans. J Comp Neurol 163:215-226.
58. Vu ET, Lee SC, Krasne FB (1993) The mechanism of tonic inhibition of crayfish escape behavior: distal inhibition and its functional significance. J Neurosci 13:4379-4393.
59. Ward S, Thomson N, White JG, Brenner S (1975) Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J Comp Neurol 160:313-337.
60. Ware RW, Clark D, Crossland K, Russel RL (1975) The nerve ring of the nematode Caenorhabditis elegans: sensory input and motor output. J Comp Neurol 162:71-110.
61. Way JC, Chalfie M (1988) mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54:5-16.
62. White JG, Southgate E, Thomson JN, Brenner S (1976) The structure of the ventral cord of Caenorhabditis elegans. Philos Trans R Soc Lond Biol 275:327-384.
63. White JE, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond Biol 314:1-340.
64. Wicks SR, Rankin CH (1995a) Integration of mechanosensory stimuli in Caenorhabditis elegans. J Neurosci 15:2434-2444.
65. Wicks SR, Rankin CH (1995b) Recovery from habituation and habituation of spontaneous behavior in C. elegans: dependence on circuit characteristics. Soc Neurosci Abstr 21:1201.
66. Wood WB (1988) The nematode Caenorhabditis elegans. Cold Spring Harbor, NY: Cold Spring Harbor.