Parameter space analysis suggests multi-site plasticity contributes to motor pattern initiation in Tritonia

Journal of Neurophysiology

Volumn 98, Issue 4, 2007, Pages 2382-2398

  Calin Jageman, Robert J ^a,f   Tunstall, Mark J ^e   Mensh, Brett D ^b,c   Katz, Paul S ^a   Frost, William N ^d  

^a GEORGIA STATE UNIVERSITY   (United States)

^b Columbia University College of Physicians and Surgeons ^*  (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^e UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^f DOMINICAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL ACTIVITY; CIRCADIAN RHYTHM; EXCITATION; GASTROPOD; INTERNEURON; MEDICAL RESEARCH; MOTOR SYSTEM; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; OSCILLATOR; POLYSYNAPTIC REFLEX; PRIORITY JOURNAL; SWIMMING; TRITONIA SEA SLUG;

ACTION POTENTIALS; ANIMALS; COMPUTER SIMULATION; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; GASTROPODA; MEMBRANE POTENTIALS; MICROELECTRODES; MODELS, NEUROLOGICAL; NEURAL NETWORKS (COMPUTER); NEURONAL PLASTICITY; NEURONS; POTASSIUM CHANNELS, VOLTAGE-GATED; REFLEX, MONOSYNAPTIC; SEROTONIN; SWIMMING; SYNAPSES; TRITONIA SEA SLUG;

EID: 35348888375     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00572.2007     Document Type: Article

References (55)

1. Briggman KL, Kristan WB. Imaging dedicated and multifunction neural circuits generating distinct behaviors. J Neurosci 26: 10925-10933, 2006.
2. Calin-Jageman RJ, Katz PS. A distributed computing tool for generating neural simulation databases. Neural Computation 18: 1-5, 2006.
3. Calin-Jageman RJ, Katz PS, Frost WN. A computational analysis of neuromodulatory control of rhythmic neural activity in the Tritonia swim central pattern generator. Annual Meeting of the Organization for Computational Neuroscience, Edinburgh, Scotland, 2006.
4. Dale N, Gilday D. Regulation of rhythmic movements by purinergic neurotransmitters in frog embryos. Nature 383: 259-263, 1996.
5. Dorsett DA, Willows AO, Hoyle G. The neuronal basis of behavior in Tritonia. IV. The central origin of a fixed action pattern demonstrated in the isolated brain. J Neurobiol 4: 287-300, 1973.
6. Eisenhart FJ, Cacciatore TW, Kristan WB Jr. A central pattern generator underlies crawling in the medicinal leech. J Comp Physiol [A] 186: 631-643, 2000.
7. Fickbohm DJ, Katz PS. Paradoxical actions of the serotonin precursor 5-hydroxytryptophan on the activity of identified serotonergic neurons in a simple motor circuit. J Neurosci 20: 1622-1634, 2000.
8. Foster WR, Ungar LH, Schwaber JS. Significance of conductances in Hodgkin-Huxley models. J Neurophysiol 70: 2502-2518, 1993.
9. Fredman SM, Jahan-Parwar B. Role of pedal ganglia motor neurons in pedal wave generation in Aplysia. Brain Res Bull 5: 179-193, 1980.
10. Frost WN, Brandon CL, Mongeluzi DL. Sensitization of the Tritonia escape swim. Neurobiol Learn Mem 69: 126-135, 1998.
11. Frost WN, Hoppe TA, Wang J, Tian LM. Swim initiation neurons in Tritonia diomedea. Am Zool 41: 952-961, 2001.
12. Frost WN, Katz PS. Single neuron control over a complex motor program. Proc Natl Acad Sci USA 93: 422-426, 1996.
13. Frost WN, Lieb JR Jr, Tunstall MJ, Mensh BD, Katz PS. Integrate-and-fire simulations of two molluscan neural circuits. In: Neurons, Networks, and Motor Behavior, edited by Stein PSG, Selverston AI, Stuart DG, Grillner S. Cambridge, MA: MIT Press, 1997, p. 173-179.
14. Frost WN, Wang J, Brandon CJ. A stereo-compound hybrid microscope for combined intracellular and optical recording of invertebrate neural network activity. J Neurosci Methods 162: 148-154, 2007.
15. Getting PA. Mechanisms of pattern generation underlying swimming in Tritonia. I. Neuronal network formed by monosynaptic connections. J Neurophysiol 46: 65-79, 1981.
16. Getting PA. Mechanisms of pattern generation underlying swimming in Tritonia. II. Network reconstruction. J Neurophysiol 49: 1017-1035, 1983a.
17. Getting PA. Mechanisms of pattern generation underlying swimming in Tritonia. III. Intrinsic and synaptic mechanisms for delayed excitation. J Neurophysiol 49: 1036-1050, 1983b.
18. Getting PA. A network oscillator underlying swimming in Tritonia. In: Neuronal and Cellular Oscillators, edited by Jacklet JW. New York: Marcel Dekker, 1989a, p. 215-236.
19. Getting PA. Reconstruction of small neural networks. In: Methods in Neural Modeling, edited by Koch C, Segev I. Cambridge, MA: MIT Press, 1989b, p. 171-196.
20. Getting PA, Dekin MS. Mechanisms of pattern generation underlying swimming in Tritonia. IV. Gating of central pattern generator. J Neurophysiol 53: 466-480, 1985.
21. Getting PA, Lennard PR, Hume RI. Central pattern generator mediating swimming in Tritonia. I. Identification and synaptic interactions. J Neurophysiol 44:151- 64, 1980.
22. Goldman MS, Golowasch J, Marder E, Abbott LF. Global structure, robustness, and modulation of neuronal models. J Neurosci 21: 5229-5238, 2001.
23. Hines ML, Carnevale NT. The NEURON simulation environment. Neural Comput 9: 1179-1209, 1997.
24. Hines ML, Carnevale NT. NEURON: a tool for neuroscientists. Neuroscientist 7: 123-135, 2001.
25. Hines ML, Morse T, Migliore M, Carnevale NT, Shepherd GM. ModelDB: a database to support computational neuroscience. J Comput Neurosci 17: 7-11, 2004.
26. Jing J, Gillette R. Neuronal elements that mediate escape swimming and suppress feeding behavior in the predatory sea slug Pleurobranchaea. J Neurophysiol 74: 1900-1910, 1995.
27. Johnson RA, Wichern DW. Applied Multivariate Statistical Analysis. Englewood Cliffs, NJ: Prentice Hall, 1992.
28. Jordan LM. Initiation of locomotion in mammals. Ann NY Acad Sci 860: 83-93, 1998.
29. Katz PS, Frost WN. Intrinsic neuromodulation in the Tritonia swim CPG: serotonin mediates both neuromodulation and neurotransmission by the dorsal swim interneurons. J Neurophysiol 74: 2281-2294, 1995a.
30. Katz PS, Frost WN. Intrinsic neuromodulation in the Tritonia swim CPG: the serotonergic dorsal swim interneurons act presynaptically to enhance transmitter release from interneuron C2. J Neurosci 15: 6035-6045, 1995b.
31. Katz PS, Frost WN. Removal of spike frequency adaptation via neuromodulation intrinsic to the Tritonia escape swim central pattern generator. J Neurosci 17: 7703-7713, 1997.
32. Katz PS, Getting PA, Frost WN. Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature 367: 729-731, 1994.
33. Katz PS, Sakurai A, Clemens S, Davis D. Cycle period of a network oscillator is independent of membrane potential and spiking activity in individual central pattern generator neurons. J Neurophysiol 92: 1904-1917, 2004.
34. Lennard PR, Getting PA, Hume RI. Central pattern generator mediating swimming in Tritonia. II. Initiation, maintenance, and termination. J Neurophysiol 44: 165-173, 1980.
35. Lieb JR Jr, Frost WN. Realistic simulation of the Aplysia siphon-withdrawal reflex circuit: roles of circuit elements in producing motor output. J Neurophysiol 77: 1249-1268, 1997.
36. Lytonn WW. Neural query system: data mining from within the NEURON simulator. Neuroinformatics 4: 163-76, 2006.
37. Matsugu M, Duffin J, Poon C. Entrainment, instability, quasi-periodicity, and chaos in a compound neural oscillator. J Comp Neurosci 5: 35-51, 1998.
38. McClellan AD, Brown GD, Getting PA. Modulation of swimming in Tritonia: excitatory and inhibitory effects of serotonin. J Comp Physiol [A] 174: 257-266, 1994.
39. Morton DW, Chiel HJ, Cohen L, Wu JY. Optical methods can be utilized to map the location and activity of putative motor neurons and interneurons during rhythmic patterns of activity in the buccal ganglion of Aplysia. Brain Res 564: 45-55, 1991.
40. Nagy F, Cardi P, Cournil I. A rhythmic modulatory gating system in the stomatogastric nervous system of Homarus gammarus. I. Pyloric-related neurons in the commissural ganglia. J Neurophysiol 71: 2477-2489, 1994.
41. Nusbaum MP, Kristan WB Jr. Swim initiation in the leech by serotonincontaining interneurones, cells 21 and 61. J Exp Biol 122: 277-302, 1986.
42. Peterson BE, Healy MD, Nadkarni PM, Miller PL, Shepherd GM. ModelDB: an environment for running and storing computational models and their results applied to neuroscience. J Am Med Inform Assoc 3: 389-398, 1996.
43. Popescu IR, Frost WN. Highly dissimilar behaviors mediated by a multifunctional network in the marine mollusk Tritonia diomedea. J Neurosci 22: 1985-1993, 2002.
44. Prinz AA, Billimoria CP, Marder E. Alternative to hand-tuning conductance-based models: construction and analysis of databases of model neurons. J Neurophysiol 90: 3998-4015, 2003a.
45. Prinz AA, Thirumalai V, Marder E. The functional consequences of changes in the strength and duration of synaptic inputs to oscillatory neurons. J Neurosci 23: 943-954, 2003b.
46. Rosen SC, Teyke T, Miller MW, Weiss KR, Kupfermann I. Identification and characterization of cerebral-to-buccal interneurons implicated in the control of motor programs associated with feeding in Aplysia. J Neurosci 11: 3630-3655, 1991.
47. Sakurai A, Calin-Jageman RJ, Katz PS. The potentiation phase of spike timing-dependent neuromodulation by a serotonergic interneuron involves an increase in the fraction of transmitter release. J Neurophysiol In press.
48. Sakurai A, Darghouth NR, Butera RJ, Katz PS. Serotonergic enhancement of a 4-AP-sensitive current mediates the synaptic depression phase of spike timing-dependent neuromodulation. J Neurosci 26: 2010-2021, 2007.
49. Sakurai A, Katz PS. Spike timing-dependent serotonergic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. J Neurosci 23: 10745-10755, 2003.
50. Shaw BK, Kristan WB. The neuronal basis of the behavioral choice between swimming and shortening in the leech: control is not selectively exercised at higher circuit levels. J Neurosci 17: 786-795, 1997.
51. Shik ML, Severin FV, Orlovskii GN. Control of walking and running by means of electrical stimulation of the mid-brain. Biofizika 11: 659-666, 1966.
52. Staras K, Kemenes I, Benjamin PR, Kemenes G. Loss of self-inhibition is a cellular mechanism for episodic rhythmic behavior. Curr Biol 13: 116-124, 2003.
53. Taylor AL, Hickey TJ, Prinz AA, Marder E. Structure and visualization of high-dimensional conductance spaces. J Neurophysiol 96: 891-905, 2006.
54. Willows AO, Hoyle G. Correlation of behavior with the activity of single identifiable neurons in the brain of Tritonia. In: Neurobiology of Invertebrates, edited by Salanki J. New York: Plenum, 1967, p. 443-461.
55. Willows AO, Hoyle G. Neuronal network triggering a fixed action pattern. Science 166: 1549-1550, 1969.