Complexities and uncertainties of neuronal network function

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 361, Issue 1465, 2006, Pages 81-99

  Parker, David ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Complexity; Lamprey; Neuromodulation; Neuronal network; Plasticity; Spinal cord

Indexed keywords

COMPLEXITY; FISH; NERVOUS SYSTEM; NETWORK ANALYSIS; PLASTICITY;

PETROMYZONTIDAE; VERTEBRATA;

ANIMAL; NERVE CELL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; PHYSIOLOGY; REVIEW; UNCERTAINTY;

ANIMALS; NERVE NET; NEURONAL PLASTICITY; NEURONS; UNCERTAINTY;

EID: 33646575642     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2005.1779     Document Type: Review

References (113)

1. Abraham, W. & Bear, M. 1996 Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19, 126-130. (doi:10.1016/S0166-2236(96) 80018-X)
2. Aradi, I. & Soltesz, I. 2002 Modulation of network behaviour by changes in variance in interneuronal properties. J. Physiol. 538, 227-251. (doi:10.1113/jphysiol.2001.013054)
3. Arshavsky, Y., Orlovsky, G., Panchin, Y., Roberts, A. & Soffe, S. 1993 Neuronal control of swimming locomotion: analysis of the pteropod mollusc clione and embryos of the amphibian Xenopus. TINS 16, 227-233.
4. Ayers, J., Carpenter, G., Currie, S. & Kinch, J. 1983 Which behavior does the lamprey central motor program mediate? Science 221, 1312-1314.
5. Barthe, J.-Y. & Clarac, F. 1997 Modulation of the spinal network for locomotion by substance P in the neonatal rat. Exp. Brain Res. 115, 485-492.
6. Bevan, S. & Parker, D. 2004 Metaplastic facilitation and ultrastructural changes in synaptic properties are associated with long-term modulation of the lamprey locomotor network. J. Neurosci. 24, 9458-9468. (doi:10.1523/JNEUROSCI.3391-04.2004)
7. Bienenstock, E., Cooper, L. & Munro, P. 1982 Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2, 32-48.
8. Blakemore, C. 2000 Achievements and challenges of the decade of the brain. Eurobrain 2, 1-4.
9. Breggin, P. 1993 Toxic psychiatry. New York: Fontana.
10. Brenner, S. 1999 Theoretical biology in the third millennium. Phil. Trans. R. Soc. B 354, 1963-1975. (doi:10.1098/rstb.1999.0535)
11. Brodin, L., Grillner, S. & Rovainen, C. 1985 N-methyl-D-aspartate (NMDA), kainate and quisqualate receptors and the generation of fictive locomotion in the lamprey spinal cord. Brain Res. 325, 302-306. (doi:10.1016/0006-8993(85)90328-2)
12. Brown, T. G. 1911 The intrinsic factors in the act of progression in the mammal. Proc. R. Soc. B 84, 308-319.
13. Buchanan, J. 1992 Neural network simulations of coupled locomotor oscillators in the lamprey spinal cord. Biol. Cybern. 66, 367-374. (doi:10.1007/BF00203673)
14. Buchanan, J. 1993 Electrophysiological properties of identified classes of lamprey spinal neurons. J. Neurophysiol. 70, 2313-2325.
15. Buchanan, J. 1999a The roles of interneurons and motoneurons in the lamprey locomotor network. Prog. Brain Res. 123, 311-321.
16. Buchanan, J. 1999b Commissural interneurons in rhythm generation and intersegmental coupling in the lamprey spinal cord. J. Neurophysiol. 81, 2037-2045.
17. Buchanan, J. 2001 Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology. Prog. Neurobiol. 63, 441-166.
18. Buchanan, J. & Grillner, S. 1987 Newly identified glutamate interneurones and their role in locomotion in the lamprey spinal cord. Science 236, 312-314.
19. Buchanan, J. & Grillner, S. 1988 A new class of small inhibitory interneurones in the lamprey spinal cord. Brain Res. 438, 404-407. (doi:10.1016/0006-8993(88)91373-X)
20. Buchman, T. 2002 The community of the self. Nature 420, 246-251. (doi:10.1038/nature01260)
21. Caplan, A. 2002 The brain revolution and ethics. The Scientist 16, 12-14.
22. Crick, F. 1994 The astonishing hypothesis. Sidney: Simon and Schuster.
23. Dietz, V. 2003 Spinal cord pattern generators for locomotion. Clin. Neurophysiol. 114, 1379-1389. (doi:10.1016/S1388-2457(03)00120-2)
24. Edgerton, V. & Roy, R. 2002 Paralysis recovery in humans and model systems. Curr. Opin. Neurobiol. 12, 658-667. (doi:10.1016/S0959-4388(02)00379-3)
25. Edgerton, V. et al. 2001 Retraining the injured spinal cord. J. Physiol. 533, 15-22. (doi:10.1111/j.1469-7793.2001.0015b.x)
26. Edwards, F. 1995 LTP-a structural model to explain the inconsistencies. Trends Neurosci. 18, 250-255. (doi:10.1016/0166-2236(95)80003-K)
27. El Manira, A., DiCaprio, R., Cattaert, D. & Clarac, F. 1991 Monosynaptic interjoint reflexes and their central modulation during fictive locomotion in crayfish. Eur. J. Neurosci. 3, 1219-1231.
28. Elson, R. C., Selverston, A. I., Abarbanel, H. D. I. & Rabinovich, M. I. 2002 Inhibitory synchronization of bursting in biological neurons: dependence on synaptic time constant. J. Neurophysiol. 88, 1166-1176.
29. Fawcett, J. 2002 Repair of spinal cord injuries: where are we, where are we going? Spinal Cord 40, 615-623. (doi:10.1038/sj.sc.3101328)
30. Feldman, D., Nicoll, R. & Malenka, R. 1999 Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. J. Neurobiol. 41, 92-101. (doi:10.1002/(SICI)1097-4695(199910) 41:1 〈92::AID-NEU12〉 3.0.CO;2-U)
31. Fields, R. D. & Stevens-Graham, B. 2002 New insights into neuron-glia communication. Science 298, 556-562. (doi:10.1126/science.298.5593.556)
32. Fitzsimonds, R., Song, H.-J. & Poo, M.-M. 1997 Propagation of activity-dependent synaptic depression in simple neural networks. Nature 388, 439-448. (doi:10.1038/41267)
33. Getting, P. 1988 Comparative analysis of invertebrate central pattern generators. In Neural control of rhythmic movements in vertebrates (ed. A. H. Cohen, S. Rossignol & S. Grillner), pp. 101-127. New York: Wiley.
34. Getting, P. 1989 Emerging principles governing the operation of neural networks. Ann. Rev. Neurosci. 12, 185-204.
35. Glanzman, D. 1995 The cellular basis of classical conditioning in Aplysia californica-it's less simple than you think. Trends Neurosci. 18, 30-36. (doi:10.1016/0166-2236(95) 93947-V)
36. Greenberg, B. 2002 Update on deep brain stimulation. J. ECT 18, 193-196. (doi:10.1097/00124509-200212000-00005)
37. Greenspan, R. 2001 The flexible genome. Nat. Rev. Genet. 2, 383-387. (doi:10.1038/35072018)
38. Grillner, S. 1985 Neurobiological basis of rhythmic motor acts in vertebrates. Science 228, 143-149.
39. Grillner, S. 2003 The motor infrastructure: from ion channel to neuronal networks. Nat. Rev. Neurosci. 4, 573-586. (doi:10.1038/nrn1137)
40. Grillner, S. & Matsushima, T. 1992 The neural network underlying locomotion in lamprey-synaptic and cellular mechanisms. Neuron 7, 1-15. (doi:10.1016/0896-6273(91)90069-C)
41. Grillner, S. & Wallèn, P. 1999 On the cellular basis of vertebrate locomotion. Prog. Brain Res. 123, 297-309.
42. Grillner, S., Buchanan, J. & Lansner, A. 1988 Simulation of the segmental burst generating network for locomotion in lamprey. Neurosci. Lett. 89, 31-35.
43. Grillner, S., Markram, H., Schutter, E. D., Silberberg, G. & Lebeau, F. 2005 Microcircuits in action - From CPGs to neocortex. TINS 28, 525-533.
44. Harris-Warrick, R. & Cohen, A. H. 1985 Serotonin modulates the central pattern generator for locomotion in the isolated lamprey spinal cord. J. Exp. Biol. 116, 27-46.
45. Harris-Warrick, R., Johnson, B., Peck, J., Kloppenburg, P., Ayali, A. & Skarbinski, J. 1998 Distributed effects of dopamine modulation in the crustacean pyloric network. Annal. NY Acad. Sci. 860, 155-167.
46. Hellgren, J., Grillner, S. & Lansner, A. 1992 Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons. Biol. Cybern. 68, 1-13. (doi:10.1007/BF00203132)
47. Hochman, S. & McCrea, D. 1994 Effects of chronic spinalization on ankle extensor motoneurons. II. Motoneuron electrical properties. J. Neurophysiol. 71, 1468-1479.
48. Hooper, S. & Moulins, M. 1989 Switching of a neuron from one network to another by sensory-induced changes in membrane properties. Science 244, 1587-1589.
49. Horn, C. C., Zhurov, Y., Orekhova, I. V., Proekt, A., Kupfermann, I., Weiss, K. R. & Brezina, V. 2004 Cycle-to-cycle variability of neuromuscular activity in Aplysia feeding behavior. J. Neurophysiol. 92, 157-180. (doi:10.1152/jn.01190.2003)
50. Horgan, J. 1999 The undiscovered mind. London: Widenfeld and Nicholson.
51. Kandel, E. 2001 The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030-1038. (doi:10.1126/science. 1067020)
52. Katz, P. 1999 In Beyond Neurotransmission (ed. P. Katz), pp. 1-28. New York: Oxford University Press.
53. Katz, P. & Edwards, D. 1999 Metamodulation: the control and modulation of neuromodulation. In Beyond neurotransmission (ed. P. Katz), pp. 349-381. New York: Oxford University Press.
54. Kiehn, O. & Kullander, K. 2004 Central pattern generators deciphered by molecular genetics. Neuron 41, 317-321. (doi:10.1016/S0896-6273(04)00042-X)
55. Kjaerulff, O. & Kiehn, O. 1997 Crossed rhythmic synaptic input to motoneurons during selective activation of the contralateral spinal locomotor network. J. Neurosci. 17, 9433-9447.
56. Kozlov, A., Hellgren-Kotaleski, J., Aurell, E., Grillner, S. & Lansner, A. 2001 Modeling of substance P and 5-HT induced synaptic plasticity in the lamprey spinal CPG: consequences for network pattern generation. J. Comput. Neurosci. 11, 183-200. (doi:10.1023/A:1012806018730)
57. Kuenzi, F., Fitzjohn, S., Morton, R., Collingridge, G. & Seabrook, G. 2000 Reduced long-term potentiation in hippocampal slices prepared using sucrose-based artificial cerebrospinal fluid. J. Neurosci. Meth. 100, 117-122. (doi:10.1016/S0165-0270(00)00239-9)
58. Leblond, H., L'Esperance, M., Orsal, D. & Rossignol, S. 2003 Treadmill locomotion in the intact and spinal mouse. J. Neurosci. 23, 11 411-11 419.
59. Levine, J. 1983 Materialism and qualia: the explanatory gap. Pac. Philos. Quart. 64, 354-361.
60. Lewontin, R. C. 1991 The doctrine of DNA. New York: Penguin Books.
61. Li, W.-C., Soffe, S. R. & Roberts, A. 2002 Spinal inhibitory neurons that modulate cutaneous sensory pathways during locomotion in a simple vertebrate. J. Neurosci. 22, 10924-10934.
62. Li, Y., Harvey, P. J., Li, X. & Bennett, D. J. 2004 Spastic long-lasting reflexes of the chronic spinal rat studied in vitro. J. Neurophysiol. 91, 2236-2246. (doi:10.1152/jn.01010.2003)
63. Malenka, R. & Nicoll, R. 1999 Long-term potentiation-a decade of progress? Science 285, 1870-1874. (doi:10. 1126/science.285.5435.1870)
64. Marder, E. 2002 Non-mammalian models for studying neural development and function. Nature 417, 318-321. (doi:10.1038/417318a)
65. Marder, E. & Calabrese, R. 1996 Principles of rhythmic motor pattern generation. Physiol. Rev. 76, 687-717.
66. McIntyre, C., Savasta, M., Kerkerian-Le Goff, L. & Vitek, J. 2004 Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin. Neurophysiol. 115, 1239-1248. (doi:10.1016/j.clinph. 2003.12.024)
67. Ohta, Y., Dubuc, R. & Grillner, S. 1991 A new population of neurons with crossed axons in the lamprey spinal cord. Brain Res. 564, 143-148. (doi:10.1016/0006-8993(91)91364-7)
68. Parker, D. 2000 Spinal-cord plasticity: independent and interactive effects of neuromodulator and activity-dependent plasticity. Mol. Neurobiol. 22, 55-80. (doi:10.1385/MN:22:1-3:055)
69. Parker, D. 2003a Activity-dependent feedforward inhibition modulates synaptic transmission in a spinal locomotor network. J. Neurosci. 23, 11 085-11 093.
70. Parker, D. 2003b Variable properties in a single class of excitatory spinal synapse. J. Neurosci. 23, 3154-3163.
71. Parker, D. & Grillner, S. 1999 Activity-dependent metaplasticity of inhibitory and excitatory synaptic transmission in the lamprey spinal cord locomotor network. J. Neurosci. 19, 1647-1656.
72. Parker, D., Zhang, W. & Grillner, S. 1998 Substance P modulates NMDA responses and causes long-term protein synthesis-dependent modulation of the lamprey locomotor network. J. Neurosci. 18, 4800-4813.
73. Pearlstein, E., Mabrouk, F. B., Pflieger, J. & Vinay, L. 2005 Serotonin refines the locomotor-related alternations in the in vitro neonatal rat spinal cord. Eur. J. Neurosci. 21, 1338-1346. (doi:10.1111/j.1460-9568.2005. 03971.x)
74. Quinlan, K. A., Placas, P. G. & Buchanan, J. T. 2004 Cholinergic modulation of the locomotor network in the lamprey spinal cord. J. Neurophysiol. 92, 1536-1548. (doi:10.1152/jn.01053.2003)
75. Roberts, A., Soffe, S., Wolf, E., Yoshida, M. & Zhao, F.-Y. 1998 Central circuits controlling locomotion in young frog tadpoles. Ann. NY Acad. Sci. 860, 19-34.
76. Robins, R., Gosling, S. & Craik, K. 1998 Psychological science at the crossroads. Am. Sci. July-August, 310-313.
77. Rose, S. P. R. 1997 Lifelines. London: Penguin Press.
78. Rose, S. P. R. 2002 'Smart Drugs': do they work? Are they ethical? Will they be legal? Nat. Rev. Neurosci. 3, 975-979. (doi:10.1038/nrn984)
79. Rossignol, S., Giroux, N., Chau, C., Marcoux, J., Brustein, E. & Reader, T. 2001 Pharmacological aids to locomotor training after spinal injury in the cat. J. Physiol. 533, 65-74. (doi:10.1111/j.1469-7793.2001.0065b.x)
80. Routenberg, A. 1995 Knockout mouse faultlines. Nature 374, 314-315. (doi:10.1038/374314b0)
81. Rovainen, C. 1979 Neurobiology of lampreys. Physiol. Rev. 59, 1007-1077.
82. Rovainen, C. 1983 Identified neurons in the lamprey spinal cord and their roles in fictive swimming. In Neural origin of rhythmic movements (ed. A. Roberts & B. L. Roberts), pp. 305-330. Cambride, UK: CUP.
83. Russell, B. 1935 Religion and science. New York: Oxford University Press.
84. Sagan, C. 1977 The Dragons of Eden: speculations on the evolution of human intelligence. New York: Ballantine Books.
85. Sapir, T., Geiman, E. J., Wang, Z., Velasquez, T., Mitsui, S., Yoshihara, Y., Frank, E., Alvarez, F. J. & Goulding, M. 2004 Pax6 and engrailed 1 regulate two distinct aspects of Renshaw cell development. J. Neurosci. 24, 1255-1264. (doi:10.1523/JNEUROSCI.3187-03.2004)
86. Schloss, P. & Henn, F. 2004 New insights into the mechanisms of antidepressant therapy. Pharmacol. Ther. 102, 47-60. (doi:10.1016/j.pharmthera. 2004.02.001)
87. Schwartz, E. J., Gerachshenko, T. & Alford, S. 2005 5-HT prolongs ventral root bursting via presynaptic inhibition of synaptic activity during fictive locomotion in lamprey. J. Neurophysiol. 93, 980-988. (doi:10.1152/jn.00669.2004)
88. Selverston, A. 1980 Are central pattern generators understandable. Behav. Brain Sci. 3, 535-571.
89. Sharma, K. & Peng, C. 2001 Spinal motor circuits: merging development and function. Neuron 29, 321-324. (doi:10.1016/S0896-6273(01)00208-2)
90. Silberberg, G., Grillner, S., Lebeau, F., Maex, R. & Markram, H. 2005 Synaptic pathways in neural microcircuits. TINS 28, 541-551.
91. Spira, M., Spray, D. & Bennett, M. 1976 Electrotonic coupling: effective sign reversal by inhibitory neurons. Science 194, 1065-1067.
92. Stent, G. 1969 The coining of the golden age. Garden City, NY: Natural History Press.
93. Sterling, P. 2004 Principles of allostasis: optimal design, predictive regulation, pathophysiology and rational therapeutics. In Allostasis, homeostasis, and the costs of adaptation (ed. J. Schulkin). Cambridge, UK: Cambridge University Press.
94. Suster, M. & Bate, M. 2002 Embryonic assembly of a central pattern generator without sensory input. Nature 416, 174-178. (doi:10.1038/416174a)
95. Tai, Q., Palazzolo, K., Mautes, A., Nacimiento, W., Kuhtz-Buschbeck, J., Nacimiento, A. & Goshgarian, H. 1997 Ultrastructural characteristics of glutamatergic and GABAergic terminals in cat lamina IX before and after spinal cord injury. J. Spinal Cord Med. 20, 311-318.
96. Teshiba, T., Shamsian, A., Yashar, B., Yeh, S., Edwards, D. & Krasne, F. 2001 Dual and opposing modulatory effects of serotonin on crayfish lateral giant escape command neurons. J. Neurosci. 21, 4523-4529.
97. Tillakaratne, N.J. K., de Leon, R. D., Hoang, T. X., Roy, R. R., Edgerton, V. R. & Tobin, A. J. 2002 Use-dependent modulation of inhibitory capacity in the feline lumbar spinal cord. J. Neurosci. 22, 3130-3143.
98. Trudeau, L.-E. & Castellucci, V. 1993 Sensitisation of the gill and siphon withdrawal reflex of Aplysia: multiple sites of change in the neuronal network. J. Neurophysiol. 10, 1210-1220.
99. Turrigiano, G. 1999 Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci. 22, 221-227. (doi:10.1016/S0166-2236(98)01341-1)
100. Van Dongen, P. A., Grillner, S. & Hökfelt, T. 1986 5-Hydroxytryptamine (serotonin) causes a reduction in the afterhyperpolarization following the action potential in lamprey motoneurons and premotor interneurons. Brain Res. 366, 320-325. (doi:10.1016/0006-8993(86)91310-7)
101. Verhage, M., McMahon, H., Ghijsen, W., Boomsa, F., Scholten, G., Wiegant, V. & Nicholls, D. 1991 Differential release of amino acids, neuropeptides and catecholamines from isolated nerve terminals. Neuron 6, 517-524. (doi:10.1016/0896-6273(91)90054-4)
102. Wallén, P. & Grillner, S. 1987 N-methyl-D-aspartate receptor-induced, inherent oscillatory activity in neurons active during fictive locomotion in the lamprey. J. Neurosci. 7, 2745-2755.
103. Wallén, P. & Lansner, A. 1984 Do the motoneurones constitute apart of the spinal network generating the swimming rhythm in the lamprey? J. Exp. Biol. 113, 493-497.
104. Wallèn, P. & Williams, T. 1984 Fictive locomotion in the lamprey spinal cord in vitro compared with swimming in the intact and spinal animal. J. Physiol. 347, 225-239.
105. Wallèn, P., Buchanan, J. T., Grillner, S., Hill, R. H., Christenson, J. & Hökfelt, T. 1989 Effects of 5-hydroxytryptamine on the afterhyperpolarization, spike frequency regulation, and oscillatory membrane properties in lamprey spinal cord neurons. J. Neurophysiol. 61, 759-768.
106. Wallén, P., Ekeberg, O., Lansner, A., Brodin, L., Traven, H. & Grillner, S. 1992 A computer-based model for realistic simulations of neural networks. II. The segmental network generating locomotor rhythmicity in the lamprey. J. Neurophysiol. 68, 1939-1950.
107. Watanabe, D. et al. 1998 Ablation of cerebellar Golgi cells disrupts synaptic integration involving GABA inhibition and NMDA receptor activation in motor coordination. Cell 95, 17-27. (doi:10.1016/S0092-8674(00)81779-1)
108. Willis, C. 1991 Exons, introns, and talking genes: the science behind the Human Genome Project. New York: Basic Books.
109. Wolpert, L. 1993 The unnatural nature of science. Cambridge, MA: Harvard University Press.
110. Wulff, P. & Wisden, W. 2005 Dissecting neural circuitry by combining genetics and pharmacology. Trends Neurosci. 28, 44-50. (doi:10.1016/j.tins.2004. 11.004)
111. Zecevic, D., Wu, J.-Y., Cohen, L., London, J., Hopp, H.-P. & Falk, C. 1989 Hundreds of neurons in the Aplysia abdominal ganglion are active during the gill-withdrawal reflex. J. Neurosci. 9, 3681-3689.
112. Zhang, W. & Grillner, S. 2000 The spinal 5-HT system contributes to the generation of fictive locomotion in lamprey. Brain Res. 879, 188-192.
113. Zucker, R. S. & Regehr, W. G. 2002 Short-term synaptic plasticity. Ann. Rev. Physiol. 64, 355-405. (doi:10.1146/annurev.physiol.64.092501.114547)