Synaptic dynamics do not determine proper phase of activity in a central pattern generator

Journal of Neuroscience

Volumn 25, Issue 49, 2005, Pages 11269-11278

  Rabbah, Pascale ^a   Nadim, Farzan ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Dynamic clamp; Motor system; Pyloric rhythm; Stomatogastric; Synaptic depression; Synaptic plasticity

Indexed keywords

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL ACTIVITY; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; HYPOTHESIS; LOBSTER; MALE; MOLECULAR DYNAMICS; MOTOR SYSTEM; NERVE CELL PLASTICITY; NONHUMAN; PACEMAKER NERVE CELL; PATTERN GENERATOR; PRIORITY JOURNAL; SYNAPSE;

ANIMALS; BIOLOGICAL CLOCKS; MALE; NEURONS; PALINURIDAE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 30544453927     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3284-05.2005     Document Type: Article

References (88)

1. Abbott LF, Marder E, Hooper SL (1991) Oscillating networks: control of burst duration by electrically coupled neurons. Neural Comput 3:487-497.
2. Bose A, Manor Y, Nadim F (2004) The activity phase of postsynaptic neurons in a simplified rhythmic network. J Comput Neurosci 17:245-261.
3. Bucher D, Prinz AA, Marder E (2005) Animal-to-animal variability in motor pattern production in adults and during growth. J Neurosci 25:1611-1619.
4. Clemens S, Katz PS (2001) Identified serotonergic neurons in the Tritonia swim CPG activate both ionotropic and metabotropic receptors. J Neurophysiol 85:476-479.
5. Dicaprio R, Jordan G, Hampton T (1997) Maintenance of motor pattern phase relationships in the ventilatory system of the crab. J Exp Biol 200:963-974.
6. Eisen JS, Marder E (1982) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. III. Synaptic connections of electrically coupled pyloric neurons. J Neurophysiol 48:1392-1415.
7. Eisen JS, Marder E (1984) A mechanism for production of phase shifts in a pattern generator. J Neurophysiol 51:1375-1393.
8. el Manira A, Tegner J, Grillner S (1994) Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. J Neurophysiol 72:1852-1861.
9. Flamm RE, Harris-Warrick RM (1986a) Aminergic modulation in lobster stomatogastric ganglion. I. Effects on motor pattern and activity of neurons within the pyloric circuit. J Neurophysiol 55:847- 865.
10. Flamm RE, Harris-Warrick RM (1986b) Aminergic modulation in lobster stomatogastric ganglion. II. Target neurons of dopamine, octopamine, and serotonin within the pyloric circuit. J Neurophysiol 55:866-881.
11. Golowasch J, Buchholtz F, Epstein IR, Marder E (1992) Contribution of individual ionic currents to activity of a model stomatogastric ganglion neuron. J Neurophysiol 67:341-349.
12. Graubard K (1978) Synaptic transmission without action potentials: input-output properties of a nonspiking presynaptic neuron. J Neurophysiol 41:1014-1025.
13. Graubard K, Hartline DK (1991) Voltage clamp analysis of intact stomatogastric neurons. Brain Res 557:241-254.
14. Graubard K, Raper JA, Hartline DK (1980) Graded synaptic transmission between spiking neurons. Proc Natl Acad Sci USA 77:3733-3735.
15. Greenberg I, Manor Y (2005) Synaptic depression in conjunction with a-current channels promote phase constancy in a rhythmic network. J Neurophysiol 93:656-677.
16. Grillner S (1981) Control of locomotion in bipeds, tetrapods and fish. In: Handbook of physiology. The nervous system. Motor control, pp 1179-1236. Baltimore: Waverly.
17. Hancox JC, Pitman RM (1991) Plateau potentials drive axonal impulse bursts in insect motoneurons. Proc R Soc Lond B Biol Sci 244:33-39.
18. Harris-Warrick RM (1989) Forskolin reduces a transient potassium current in lobster neurons by a cAMP-independent mechanism. Brain Res 489:59-66.
19. Harris-Warrick RM, Flamm RE (1986) Chemical modulation of a small central pattern generator circuit. Trends Neurosci 9:432-437.
20. Harris-Warrick RM, Marder E (1991) Modulation of neural networks for behavior. Annu Rev Neurosci 14:39-57.
21. Harris-Warrick RM, Nagy F, Nusbaum MP (1992) Neuromodulation of stomatogastric networks by identified neurons and transmitters. In: Dynamic biological networks: the stomatogastric nervous system (Harris-Warrick RM, Marder E, Selverston AI, Moulins M, eds), pp 87-138. Cambridge, MA: MIT.
22. Harris-Warrick RM, Coniglio LM, Barazangi N, Guckenheimer J, Gueron S (1995a) Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network. J Neurosci 15:342-358.
23. Harris-Warrick RM, Coniglio LM, Levini RM, Gueron S, Guckenheimer J (1995b) Dopamine modulation of two subthreshold currents produces phase shifts in activity of an identified motoneuron. J Neurophysiol 74:1404-1420.
24. Harris-Warrick RM, Johnson BR, Peck JH, Kloppenburg P, Ayali A, Skarbinski J (1998) Distributed effects of dopamine modulation in the crustacean pyloric network. Ann NY Acad Sci 860:155-167.
25. Hartline DK (1979) Pattern generation in the lobster (Panulirus) stomatogastric ganglion. II. Pyloric network simulation. Biol Cybern 33:223-236.
26. Hartline DK, Gassie Jr DV (1979) Pattern generation in the lobster (Panulirus) stomatogastric ganglion. I. Pyloric neuron kinetics and synaptic interactions. Biol Cybern 33:209-222.
27. Hartline DK, Graubard K (1992) Cellular and synaptic properties in the crustacean stomatogastric nervous system. In: Dynamic biological networks: the stomatogastric nervous system (Harris-Warrick RM, Marder E, Selverston AI, Moulins M, eds), pp 31-86. Cambridge, MA: MIT.
28. Hartline DK, Gassie DV, Jones BR (1993) Effects of soma isolation on outward currents measured under voltage clamp in spiny lobster stomatogastric motor neurons. J Neurophysiol 69:2056-2071.
29. Hooper SL (1997a) Phase maintenance in the pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion. J Comput Neurosci 4:191-205.
30. Hooper SL (1997b) The pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion comprises two phase-maintaining subsets. J Comput Neurosci 4:207-219.
31. Jodkowski JS, Viana F, Dick TE, Berger AJ (1988) Repetitive firing properties of phrenic motoneurons in the cat. J Neurophysiol 60:687-702.
32. Johnson BR, Harris-Warrick RM (1990) Aminergic modulation of graded synaptic transmission in the lobster stomatogastric ganglion. J Neurosci 10:2066-2076.
33. Johnson BR, Peck JH, Harris-Warrick RM (1993) Amine modulation of electrical coupling in the pyloric network of the lobster stomatogastric ganglion. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 172:715-732.
34. Johnson BR, Peck JH, Harris-Warrick RM (1995) Distributed amine modulation of graded chemical transmission in the pyloric network of the lobster stomatogastric ganglion. J Neurophysiol 74:437-452.
35. Katz PS, Frost WN (1996) Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci 19:54-61.
36. Kiehn O, Harris-Warrick RM (1992) 5-HT modulation of hyperpolarization- activated inward current and calcium-dependent outward current in a crustacean motor neuron. J Neurophysiol 68:496-508.
37. King DG (1976a) Organization of crustacean neuropil. I. Patterns of synaptic connections in lobster stomatogastric ganglion. J Neurocytol 5:207-237.
38. King DG (1976b) Organization of crustacean neuropil. II. Distribution of synaptic contacts on identified motor neurons in lobster stomatogastric ganglion. J Neurocytol 5:239-266.
39. Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 29:169-195.
40. Kloppenburg P, Levini RM, Harris-Warrick RM (1999) Dopamine modulates two potassium currents and inhibits the intrinsic firing properties of an identified motor neuron in a central pattern generator network. J Neurophysiol 81:29-38.
41. Laurent G, Wehr M, Davidowitz H (1996) Temporal representations of odors in an olfactory network. J Neurosci 16:3837-3847.
42. LoFaro T, Kopell N, Marder E, Hooper SL (1994) Subharmonic coordination in networks of neurons with slow conductances. Neural Comp 6:69-84.
43. MacKay-Lyons M (2002) Central pattern generation of locomotion: a review of the evidence. Phys Ther 82:69-83.
44. Mamiya A, Nadim F (2004) Dynamic interaction of oscillatory neurons coupled with reciprocally inhibitory synapses acts to stabilize the rhythm period. J Neurosci 24:5140-5150.
45. Mamiya A, Nadim F (2005) Target-specific short-term dynamics are important for the function of synapses in an oscillatory neural network. J Neurophysiol 94:2590-2602.
46. Mamiya A, Manor Y, Nadim F (2003) Short-term dynamics of a mixed chemical and electrical synapse in a rhythmic network. J Neurosci 23:9557-9564.
47. Manor Y, Nadim F (2001) Synaptic depression mediates bistability in neuronal networks with recurrent inhibitory connectivity. J Neurosci 21:9460-9470.
48. Manor Y, Nadim F, Abbott LF, Marder E (1997) Temporal dynamics of graded synaptic transmission in the lobster stomatogastric ganglion. J Neurosci 17:5610-5621.
49. Manor Y, Bose A, Booth V, Nadim F (2003) Contribution of synaptic depression to phase maintenance in a model rhythmic network. J Neurophysiol 90:3513-3528.
50. Marder E (1984) Mechanisms underlying neurotransmitter modulation of neuronal circuit. Trends Neurosci 7:48-53.
51. Marder E (1987) Neurotransmitters and neuromodulators. In: The crustacean stomatogastric system (Selverston AI, Moulins M, eds), pp 263-300. Berlin: Springer.
52. Marder E (2000) Motor pattern generation. Curr Opin Neurobiol 10:691-698.
53. Marder E, Bucher D (2001) Central pattern generators and the control of rhythmic movements. Curr Biol 11:R986-R996.
54. Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687-717.
55. Marder E, Eisen JS (1984) Transmitter identification of pyloric neurons: electrically coupled neurons use different transmitters. J Neurophysiol 51:1345-1361.
56. Marder E, Hooper SL (1985) Neurotransmitter modulation of the stomatogastric ganglion of decopod crustaceans. In: Model neural networks and behavior (Selverston A, ed), pp 319-337. New York: Plenum.
57. Marder E, Paupardin-Tritsch D (1978) The pharmacological properties of some crustacean neuronal acetylcholine, gamma-aminobutyric acid, and L-glutamate responses. J Physiol (Lond) 280:213-236.
58. Marder E, Weimann JM (1992) Modulatory control of multiple task processing in the stomatogastric nervous system. In: Neurobiology of motor programme selection (Kien J, McCrohan C, Winlow B, eds), pp 3-19. New York: Pergamon.
59. Maynard DM (1972) Simpler networks. Ann NY Acad Sci 193:59-72.
60. Maynard DM, Selverston AI (1975) Organization of the stomatogastric ganglion of the spiny lobster. IV. The pyloric system. J Comp Physiol 100:161-182.
61. Maynard DM, Walton KD (1975) Effects of maintained depolarization of presynaptic neurons on inhibitory transmission in lobster neuropil. J Comp Physiol 97:215-243.
62. Miller JP (1987) Pyloric mechanisms. In: The crustacean stomatogastric system (Selverston AI, Moulins M, eds), pp 109-136. Berlin: Springer.
63. Miller JP, Selverston A (1979) Rapid killing of single neurons by irradiation of intracellularly injected dye. Science 206:702-704.
64. Miller JP, Selverston AI (1982a) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. II. Oscillatory properties of pyloric neurons. J Neurophysiol 48:1378-1391.
65. Miller JP, Selverston AI (1982b) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. IV. Network properties of pyloric system. J Neurophysiol 48:1416-1432.
66. Nadim F, Manor Y (2000) The role of short-term synaptic dynamics in motor control. Curr Opin Neurobiol 10:683-690.
67. Nassel DR (2000) Functional roles of neuropeptides in the insect central nervous system. Naturwissenschaften 87:439-449.
68. Nusbaum MP, Beenhakker MP (2002) A small-systems approach to motor pattern generation. Nature 417:343-350.
69. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
70. Olsen OH, Calabrese RL (1996) Activation of intrinsic and synaptic currents in leech heart interneurons by realistic waveforms. J Neurosci 16:4958-4970.
71. Pareti G, De Palma A (2004) Does the brain oscillate? The dispute on neuronal synchronization. Neurol Sci 25:41-47.
72. Peck JH, Nakanishi ST, Yaple R, Harris-Warrick RM (2001) Amine modulation of the transient potassium current in identified cells of the lobster stomatogastric ganglion. J Neurophysiol 86:2957-2965.
73. Rabbah P, Golowasch J, Nadim F (2005) Effect of electrical coupling on ionic current and synaptic potential measurements. J Neurophysiol 94:519-530.
74. Rabbah PM, Atamturktur S, Nadim F (2002) Distinct synaptic dynamics by pacemaker neurons of a rhythmic neural network. Soc Neurosci Abstr 28:752.5.
75. Ramirez JM, Pearson KG (1991) Octopamine induces bursting and plateau potentials in insect neurones. Brain Res 549:332-337.
76. Ramirez JM, Richter DW (1996) The neuronal mechanisms of respiratory rhythm generation. Curr Opin Neurobiol 6:817-825.
77. Raper JA (1979) Nonimpulse-mediated synaptic transmission during the generation of a cyclic motor program. Science 205:304-306.
78. Rezer E, Moulins M (1983) Expression of the crustacean pyloric pattern generator in the intact animal. J Comp Physiol 153:17-28.
79. Selverston AI, Moulins M (1985) Oscillatory neural networks. Annu Rev Physiol 47:29-48.
80. Selverston AI, Russell DF, Miller JP (1976) The stomatogastric nervous system: structure and function of a small neural network. Prog Neurobiol 7:215-290.
81. Sharp AA, O'Neil MB, Abbott LF, Marder E (1993) Dynamic clamp: computergenerated conductances in real neurons. J Neurophysiol 69:992-995.
82. Simmons PJ (2002) Presynaptic depolarization rate controls transmission at an invertebrate synapse. Neuron 35:749-758.
83. Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349-374.
84. Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70-74.
85. Tierney AJ, Harris-Warrick RM (1992) Physiological role of the transient potassium current in the pyloric circuit of the lobster stomatogastric ganglion. J Neurophysiol 67:599-609.
86. Tryba AK, Ritzmann RE (2000) Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. II. Extensor motor neuron pattern. J Neurophysiol 83:3337-3350.
87. Von Euler C (1983) On the origin and pattern control of breathing rhythmicity in mammals. Symp Soc Exp Biol 37:469-485.
88. Wolf H (1992) Reflex modulation in locusts walking on a treadwheel-intracellular recordings from motoneurons. J Comp Physiol 170:443-462.