Evidence that long-term hyperexcitability of the sensory neuron soma induced by nerve injury in Aplysia is adaptive

Journal of Neurophysiology

Volumn 94, Issue 3, 2005, Pages 2218-2230

  Gasull, Xavier ^a   Liao, Xiaogang ^a   Dulin, Michael F ^a   Phelps, Cynthia ^a   Walters, Edgar T ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; APLYSIA; ARTICLE; CONTROLLED STUDY; HYPERALGESIA; LONG TERM HYPEREXCITABILITY; NERVE CELL EXCITABILITY; NERVE FIBER TRANSECTION; NERVE INJURY; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; SENSORY DYSFUNCTION; SENSORY NERVE CELL;

ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; APLYSIA; AXOTOMY; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; LONG-TERM POTENTIATION; MEMBRANE POTENTIALS; NERVE REGENERATION; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; RECOVERY OF FUNCTION; SENSORY THRESHOLDS; TIME FACTORS; TRAUMA, NERVOUS SYSTEM;

EID: 23944519999     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00169.2005     Document Type: Article

References (71)

1. Abdulla FA and Smith PA. Axotomy- and autotomy-induced changes in the excitability of rat dorsal root ganglion neurons. J Neurophysiol 85: 630-643, 2001.
2. Ambron RT, Dulin MF, Zhang X-P, Schmied R, and Walters ET. Axoplasm enriched in a protein mobilized by nerve injury elicits memory-like alterations in Aplysia neurons. J Neurosci 15: 3440-3446, 1995.
3. Ambron RT, Zhang X-P, Gunstream JD, Povelones M, and Walters ET. Intrinsic injury signals enhance growth, survival, and excitability of Aplysia neurons. J Neurosci 16: 7469-7477, 1996.
4. Bedi SS and Glanzman DL. Axonal rejoining inhibits injury-induced long-term changes in Aplysia sensory neurons in vitro. J Neurosci 21: 9667-9677, 2001.
5. Bedi SS, Salim A, Chen S, and Glanzman DL. Long-term effects of axotomy on excitability and growth of isolated Aplysia sensory neurons in cell culture: potential role of cAMP. J Neurophysiol 79: 1371-1383, 1998.
6. Billy AJ and Walters ET. Long-term expansion and sensitization of mechanosensory receptive fields in Aplysia support an activity-dependent model of whole-cell sensory plasticity. J Neurosci 9: 1254-1262, 1989.
7. Bittner GD. Long-term survival of anucleate axons and its implications for nerve regeneration. Trends Neurosci 14: 188-193, 1991.
8. Carew TJ, Walters ET, and Kandel ER. Classical conditioning in a simple withdrawal reflex in Aplysia californica. J Neurosci 1: 1426-1437, 1981.
9. Chase R. Behavior and Its Neural Control in Gastropod Molluscs. Oxford. UK: Oxford Univ. Press. 2002.
10. Clatworthy AL, Castro GA, Budelmann BU, and Walters ET. Induction of a cellular defense reaction is accompanied by an increase in sensory neuron excitability in Aplysia. J Neurosci 14: 3263-3270, 1994.
11. Clatworthy AL and Walters ET. Rapid amplification and facilitation of mechanosensory discharge in Aplysia by noxious stimulation. J Neurophysiol 70: 1181-1194, 1993.
12. Clatworthy AL and Walters ET. Comparative analysis of hyperexcitability and synaptic facilitation induced by nerve injury in two populations of mechanosensory neurones of Aplysia californica. J Exp Biol 190: 217-238, 1994.
13. Cleary LJ and Byrne JH. Identification and characterization of a multifunctional neuron contributing to defensive arousal in Aplysia. J Neurophysiol 70: 1767-1776, 1993.
14. Cleary LJ, Lee WL, and Byrne JH. Cellular correlates of long-term sensitization in Aplysia. J Neurosci 18: 5988-5998, 1998.
15. Cohen-Armon M, Visochek L, Katzoff A, Levitan D, Susswein AJ, Klein R, Valbrun M, and Schwartz JH. Long-term memory requires poly ADP-ribosylation. Science 304: 1820-1822, 2004.
16. Daoudal G and Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 10: 456-465, 2003.
17. Dulin MF, Steffensen I, Morris CE, and Walters ET. Recovery of function, peripheral sensitization, and sensory neurone activation by novel pathways following axonal injury in Aplysia. J Exp Biol 198: 2055-2066, 1995.
18. Erixon NJ, Demartini LJ, and Wright WG. Dissociation between sensitization and learning-related neuromodulation in an aplysiid species. J Comp Neurol 408: 506-514, 1999.
19. Farr M, Mathews J, Zhu DF, and Ambron RT. Inflammation causes a long-term hyperexcitability in the nociceptive sensory neurons of Aplysia. Learn Mem 6: 331-340, 1999.
20. Farr M, Zhu DF, Povelones M, Valcich D, and Ambron RT. Direct interactions between immunocytes and neurons after axotomy in Aplysia. J Neurobiol 46: 89-96, 2001.
21. Gallego R, Ivorra I, and Morales A. Effects of central or peripheral axotomy on membrane properties of sensory neurones in the petrosal ganglion of the cat. J Physiol 391: 39-56, 1987.
22. Gordon T, Kelly ME, Sanders EJ, Shapiro J, and Smith PA. The effects of axotomy on bullfrog sympathetic neurones. J Physiol 392: 213-229, 1987.
23. Gorodetskaya N, Constantin C, and Janig W. Ectopic activity in cutaneous regenerating afferent nerve fibers following nerve lesion in the rat. Eur J Neurosci 18: 2487-2497, 2003.
24. Gunstream JD, Castro GA, and Walters ET. Retrograde transport of plasticity signals in Aplysia sensory neurons following axonal injury. J Neurosci 15: 439-448, 1995.
25. Gurtu S and Smith PA. Electrophysiological characteristics of hamster dorsal root ganglion cells and their response to axotomy. J Neurophysiol 59: 408-423, 1988.
26. Illich PA and Walters ET. Mechanosensory neurons innervating Aplysia siphon encode noxious stimuli and display nociceptive sensitization. J Neurosci 17: 459-469, 1997.
27. Ishikawa K, Tanaka M, Black JA, and Waxman SG. Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve 22: 502-507, 1999.
28. Kim YI, Na HS, Kim SH, Han HC, Yoon YW, Sung B, Nam HJ, Shin SL, and Hong SK. Cell type-specific changes of the membrane properties of peripherally-axotomized dorsal root ganglion neurons in a rat model of neuropathic pain. Neuroscience 86: 301-309, 1998.
29. Lai J, Porreca F, Hunter JC, and Gold MS. Voltage-gated sodium channels and hyperalgesia. Annu Rev Pharmacol Toxicol 44: 371-397, 2004.
30. Lewin MR and Walters ET. Cyclic GMP pathway is critical for inducing long-term sensitization of nociceptive sensory neurons. Nat Neurosci 2: 18-23, 1999.
31. Lin H, Bao J, Ju-Sung Y, Walters ET, and Ambron RT. Rapid electrical and delayed molecular signals regulate the serum response element after nerve injury: convergence of injury and learning signals. J Neurobiol 57: 204-220, 2003.
32. Ma C, Shu Y, Zheng Z, Chen Y, Yao H, Greenquist KW, White FA, and LaMotte RH. Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons. J Neurophysiol 89: 1588-1602, 2003.
33. Manseau F, Sossin WS, and Castellucci VF. Long-term changes in excitability induced by protein kinase C activation in Aplysia sensory neurons. J Neurophysiol 79: 1210-1218, 1998.
34. Marinesco S, Duran KL, and Wright WG. Evolution of learning in three aplysiid species: differences in heterosynaptic plasticity contrast with conservation in serotonergic pathways. J Physiol 550: 241-253, 2003.
35. 2+ from different sources in mouse sympathetic neurones. J Physiol 527: 249-264, 2000.
36. Michaelis M, Liu X, and Janig W. Axotomized and intact muscle afferents but no skin afferents develop ongoing discharges of dorsal root ganglion origin after peripheral nerve lesion. J Neurosci 20: 2742-2748, 2000.
37. Nordin M, Nystrom B, Wallin U, and Hagbarth KE. Ectopic sensory discharges and paresthesiae in patients with disorders of peripheral nerves, dorsal roots and dorsal columns. Pain 20: 231-245, 1984.
38. Nystrom B and Hagbarth KE. Microelectrode recordings from transected nerves in amputees with phantom limb pain. Neurosci Lett 27: 211-216, 1981.
39. Purves D. Body and Brain: A Trophic Theory of Neural Connections. Cambridge, MA: Harvard Univ. Press, 1988.
40. + currents in cutaneous afferent dorsal root ganglion neurones following axotomy. Neurobiol Dis 2: 87-96, 1995.
41. Scholz KP and Byrne JH. Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science 235: 685-687, 1987.
42. + currents. Science 240: 1664-1666, 1988.
43. Song XJ, Vizcarra C, Xu DS, Rupert RL, and Wong ZN. Hyperalgesia and neural excitability following injuries to central and peripheral branches of axons and somata of dorsal root ganglion neurons. J Neurophysiol 89: 2185-2193, 2003.
44. Stebbing MJ, Eschenfelder S, Habler HJ, Acosta MC, Janig W, and McLachlan EM. Changes in the action potential in sensory neurones after peripheral axotomy in vivo. Neuroreport 10: 201-206, 1999.
45. Steffensen I, Dulin MF, Walters ET, and Morris CE. Peripheral regeneration and central sprouting of sensory neurone axons in Aplysia californica following nerve injury. J Exp Biol 198: 2067-2078, 1995.
46. Study RE and Kral MG. Spontaneous action potential activity in isolated dorsal root ganglion neurons from rats with a painful neuropathy. Pain 65: 235-242, 1996.
47. Sung YJ and Ambron RT. Pathways that elicit long-term changes in gene expression in nociceptive neurons following nerve injury: contributions to neuropathic pain. Neurol Res 26: 195-203, 2004.
48. Sung YJ, Povelones M, and Ambron RT. RISK-1: a novel MAPK homologue in axoplasm that is activated and retrogradely transported after nerve injury. J Neurobiol 47: 67-79, 2001.
49. Sung YJ, Walters ET, and Ambron RT. A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear import to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons. J Neurosci 24: 7583-7595, 2004.
50. Suzuki R and Dickenson AH. Neuropathic pain: nerves bursting with excitement. Neuroreport 11: R17-R21, 2000.
51. Titmus MJ and Faber DS. Axotomy-induced alterations in the electrophysiological characteristics of neurons. Prog Neurobiol 35: 1-51, 1990.
52. Ungless MA, Gasull X, and Walters ET. Long-term alteration of S-type potassium current and passive membrane properties in Aplysia sensory neurons following axotomy. J Neurophysiol 87: 2408-2420, 2002.
53. Wall PD and Devor M. Sensory afferent impulses originate from dorsal root ganglia as well as from the periphery in normal and nerve injured rats. Pain 17: 321-339, 1983.
54. Walters ET. Multiple sensory neuronal correlates of site-specific sensitization in Aplysia. J Neurosci 1: 408-417, 1987a.
55. Walters ET. Site-specific sensitization of defensive reflexes in Aplysia: a simple model of long-term hyperalgesia. J Neurosci 7: 400-407, 1987b.
56. Walters ET. A functional, cellular, and evolutionary model of nociceptive plasticity m Aplysia. Biol Bull 180: 241-251, 1991.
57. Walters ET. Injury-related behavior and neuronal plasticity: an evolutionary perspective on sensitization, hyperalgesia and analgesia. Int Rev Neurobiol 36: 325-427, 1994.
58. Walters ET, Alizadeh H, and Castro GA. Similar neuronal alterations induced by axonal injury and learning in Aplysia. Science 253: 797-799, 1991.
59. Walters ET, Bodnarova M, Billy AJ, Dulin MF, Diaz-Rios M, Miller MW, and Moroz LL. Somatotopic organization and functional properties of mechanosensory neurons expressing sensorin-A mRNA in Aplysia californica. J Comp Neurol 471: 219-240, 2004.
60. Walters ET, Byrne JH, Carew TJ, and Kandel ER. Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. J Neurophysiol 50: 1522-1542, 1983a.
61. Walters ET, Byrne JH, Carew TJ, and Kandel ER. Mechanoafferent neurons innervating tail of Aplysla. II. Modulation by sensitizing stimulation. J Neurophysiol 50: 1543-1559, 1983b.
62. Walters ET, Carew TJ, Hawkins RD, and Kandel ER. Classical conditioning in Aplysla: analysis of involved neural circuits. In: Conditioning: Representation of Involved Neural Functions, edited by Woody CD. New York: Plenum, 1982, p. 677-695.
63. Walters ET, Carew TJ, and Kandel ER. Associative learning in Aplysia: evidence for conditioned fear in an invertebrate. Science 211: 504-506, 1981.
64. Walters ET and Erickson MT. Directional control and the functional organization of defensive responses in Aplysia. J Comp Physiol A Sens Neural Behav Physiol 159: 339-351, 1986.
65. Walters ET, Illich PA, and Hickie C. Inking and siphon response plasticity in Aplysia: anti-predator and alarm signal functions. Soc Neurosci Abstr 19: 578, 1993.
66. Weragoda RM, Ferrer E, and Walters ET. Memory-like alterations in Aplysia axons after nerve injury or localized depolarization. J Neurosci 24: 10393-10401, 2004.
67. Wu W, Mathew TC, and Miller FD. Evidence that the loss of homeostatic signals induces regeneration-associated alterations in neuronal gene expression. Dev Biol 158: 456-466, 1993.
68. Yang EK, Takimoto K, Hayashi Y, de Groat WC, and Yoshimura N. Altered expression of potassium channel subunit mRNA and alpha-dendrotoxin sensitivity of potassium currents in rat dorsal root ganglion neurons after axotomy. Neuroscience 123: 867-874, 2004.
69. Zhang JM, Donnelly DF, Song XJ, and Lamotte RH. Axotomy increases the excitability of dorsal root ganglion cells with unmyelinated axons. J Neurophysiol 78: 2790-2794, 1997.
70. Zhang W and Linden DJ. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4: 885-900, 2003.
71. Zhang ZS, Fang B, Marshak DW, Byrne JH, and Cleary LJ. Serotoninergic varicosities make synaptic contacts with pleural sensory neurons of Aplysia. J Comp Neurol 311: 259-270, 1991.