Self-injurious behaviour in intellectual disability syndromes: Evidence for aberrant pain signalling as a contributing factor

Journal of Intellectual Disability Research

Volumn 56, Issue 5, 2012, Pages 441-452

  Peebles, K A ^a   Price, T J ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Central sensitisation; Diffuse noxious inhibitory control; Fragile X; Pain; Rett syndrome; Self injury

Indexed keywords

ARTICLE; AUTOMUTILATION; CHRONIC PAIN; DATA BASE; DIFFUSE NOXIOUS INHIBITORY CONTROL; FRAGILE X MENTAL RETARDATION; GASTROESOPHAGEAL REFLUX; HUMAN; LONG TERM POTENTIATION; MUTATION; NOCICEPTION; NONHUMAN; RETT SYNDROME; VISCERAL PAIN; X LINKED MENTAL RETARDATION;

AFFERENT PATHWAYS; ANIMALS; HUMANS; INTELLECTUAL DISABILITY; NOCICEPTORS; PAIN; SELF-INJURIOUS BEHAVIOR; SIGNAL TRANSDUCTION;

EID: 84859642836     PISSN: 09642633     EISSN: 13652788     Source Type: Journal    
DOI: 10.1111/j.1365-2788.2011.01484.x     Document Type: Article

References (94)

1. Apkarian A. V., Bushnell M. C., Treede R. D. & Zubieta J. K. (2005) Human brain mechanisms of pain perception and regulation in health and disease. European Journal of Pain 9, 463-84.
2. Asiedu M. N., Tillu D. V., Melemedjian O. K., Shy A., Sanoja R., Bodell B. etal. (2011) Spinal protein kinase M {zeta} underlies the maintenance mechanism of persistent nociceptive sensitization. Journal of Neuroscience 31, 6646-53.
3. Bagni C. & Greenough W. T. (2005) From mRNP trafficking to spine dysmorphogenesis: the roots of fragile X syndrome. Nature Reviews. Neuroscience 6, 376-87.
4. Bassell G. J. & Warren S. T. (2008) Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60, 201-14.
5. Bear M. F., Huber K. M. & Warren S. T. (2004) The mGluR theory of fragile X mental retardation. Trends in Neurosciences 27, 370-7.
6. Berry-Kravis E., Goetz C. G., Leehey M. A., Hagerman R. J., Zhang L., Li L. etal. (2007) Neuropathic features in fragile X premutation carriers. American Journal of Medical Genetics. Part A 143, 19-26.
7. Berry-Kravis E., Hessl D., Coffey S., Hervey C., Schneider A., Yuhas J. etal. (2009) A pilot open label, single dose trial of fenobam in adults with fragile X syndrome. Journal of Medical Genetics 46, 266-71.
8. Bosch J., Van Dyke C., Smith S. M. & Poulton S. (1997) Role of medical conditions in the exacerbation of self-injurious behavior: an exploratory study. Mental Retardation 35, 124-30.
9. Boureau F., Willer J. C. & Dauthier C. (1978) Study of naloxone in normal awake man: effects on spinal reflexes. Neuropharmacology 17, 565-8.
10. Breau L. M., Camfield C. S., Symons F. J., Bodfish J. W., Mackay A., Finley G. A. etal. (2003a) Relation between pain and self-injurious behavior in nonverbal children with severe cognitive impairments. The Journal of Pediatrics 142, 498-503.
11. Breau L. M., MacLaren J., McGrath P. J., Camfield C. S. & Finley G. A. (2003b) Caregivers' beliefs regarding pain in children with cognitive impairment: relation between pain sensation and reaction increases with severity of impairment. The Clinical Journal of Pain 19, 335-44.
12. Brega A. G., Reynolds A., Bennett R. E., Leehey M. A., Bounds L. S., Cogswell J. B. etal. (2009) Functional status of men with the fragile X premutation, with and without the tremor/ataxia syndrome (FXTAS). International Journal of Geriatric Psychiatry 24, 1101-9.
13. Cates M., Billmire D. F., Bull M. J. & Grosfeld J. L. (1989) Gastroesophageal dysfunction in Cornelia de Lange syndrome. Journal of Pediatric Surgery 24, 248-50.
14. Chang Q., Khare G., Dani V., Nelson S. & Jaenisch R. (2006) The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49, 341-8.
15. Coffey S. M., Cook K., Tartaglia N., Tassone F., Nguyen D. V., Pan R. etal. (2008) Expanded clinical phenotype of women with the FMR1 premutation. American Journal of Medical Genetics. Part A 146A, 1009-16.
16. De Broucker T., Cesaro P., Willer J. C. & Le Bars D. (1990) Diffuse noxious inhibitory controls in man. Involvement of the spinoreticular tract. Brain 113(Pt 4), 1223-34.
17. Defrin R., Pick C. G., Peretz C. & Carmeli E. (2004) A quantitative somatosensory testing of pain threshold in individuals with mental retardation. Pain 108, 58-66.
18. Dent J. (1998) Gastro-oesophageal reflux disease. Digestion 59, 433-45.
19. Dickenson A. H. & Sullivan A. F. (1987) Evidence for a role of the NMDA receptor in the frequency dependent potentiation of deep rat dorsal horn nociceptive neurones following C fibre stimulation. Neuropharmacology 26, 1235-8.
20. Downs J., Geranton S. M., Bebbington A., Jacoby P., Bahi-Buisson N., Ravine D. etal. (2010) Linking MECP2 and pain sensitivity: the example of Rett syndrome. American Journal of Medical Genetics. Part A 152A, 1197-205.
21. Frisby C. L., Mattsson J. P., Jensen J. M., Lehmann A., Dent J. & Blackshaw L. A. (2005) Inhibition of transient lower esophageal sphincter relaxation and gastroesophageal reflux by metabotropic glutamate receptor ligands. Gastroenterology 129, 995-1004.
22. Géranton S. M., Morenilla-Palao C. & Hunt S. P. (2007) A role for transcriptional repressor methyl-CpG-binding protein 2 and plasticity-related gene serum- and glucocorticoid-inducible kinase 1 in the induction of inflammatory pain states. Journal of Neuroscience 27, 6163-73.
23. Géranton S. M., Fratto V., Tochiki K. K. & Hunt S. P. (2008) Descending serotonergic controls regulate inflammation-induced mechanical sensitivity and methyl-CpG-binding protein 2 phosphorylation in the rat superficial dorsal horn. Molecular Pain 4, 35.
24. Gössler A., Schalamon J., Huber-Zeyringer A. & Höllwarth M. E. (2007) Gastroesophageal reflux and behavior in neurologically impaired children. Journal of Pediatric Surgery 42, 1486-90.
25. Hagerman R. J. & Hagerman P. J. (2002) The fragile X premutation: into the phenotypic fold. Current Opinion in Genetics & Development 12, 278-83.
26. Hall S. S., Lightbody A. A. & Reiss A. L. (2008) Compulsive, self-injurious, and autistic behavior in children and adolescents with fragile x syndrome. American Journal of Mental Retardation 113, 44-53.
27. Hennequin M., Morin C. & Feine J. S. (2000) Pain expression and stimulus localisation in individuals with Down's syndrome. Lancet 356, 1882-7.
28. Herrero J. F., Laird J. M. & Lopez-Garcia J. A. (2000) Wind-up of spinal cord neurones and pain sensation: much ado about something? Progress in Neurobiology 61, 169-203.
29. Hessl D., Tassone F., Loesch D. Z., Berry-Kravis E., Leehey M. A., Gane L. W. etal. (2005) Abnormal elevation of FMR1 mRNA is associated with psychological symptoms in individuals with the fragile X premutation. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics 139, 115-21.
30. Holloway R. H. & Dent J. (1990) Pathophysiology of gastroesophageal reflux. Lower esophageal sphincter dysfunction in gastroesophageal reflux disease. Gastroenterology Clinics of North America 19, 517-35.
31. Hu H., Qin Y., Bochorishvili G., Zhu Y., van Aelst L. & Zhu J. J. (2008) Ras signaling mechanisms underlying impaired GluR1-dependent plasticity associated with fragile X syndrome. Journal of Neuroscience 28, 7847-62.
32. Ikeda H., Stark J., Fischer H., Wagner M., Drdla R., Jager T. etal. (2006) Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science 312, 1659-62.
33. Jacquemont S., Curie A., des Portes V., Torrioli M. G., Berry-Kravis E., Hagerman R. J. etal. (2011) Epigenetic modification of the FMR1 gene in fragile X syndrome is associated with differential response to the mGluR5 antagonist AFQ056. Science Translational Medicine 3, 64ra1.
34. Jensen J., Lehmann A., Uvebrant A., Carlsson A., Jerndal G., Nilsson K. etal. (2005) Transient lower esophageal sphincter relaxations in dogs are inhibited by a metabotropic glutamate receptor 5 antagonist. European Journal of Pharmacology 519, 154-7.
35. Ji R. R., Kohno T., Moore K. A. & Woolf C. J. (2003) Central sensitization and LTP: do pain and memory share similar mechanisms? Trends in Neurosciences 26, 696-705.
36. Kelleher R. J. 3rd, Govindarajan A. & Tonegawa S. (2004) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44, 59-73.
37. Keywood C., Wakefield M. & Tack J. (2009) A proof-of-concept study evaluating the effect of ADX10059, a metabotropic glutamate receptor-5 negative allosteric modulator, on acid exposure and symptoms in gastro-oesophageal reflux disease. Gut 58, 1192-9.
38. Klein T., Magerl W., Hopf H.-C., Sandkühler J. & Treede R.-D. (2004) Perceptual correlates of nociceptive long-term potentiation and long-term depression in humans. Journal of Neuroscience 24, 964-71.
39. Klein T., Stahn S., Magerl W. & Treede R. (2008) The role of heterosynaptic facilitation in long-term potentiation (LTP) of human pain sensation. Pain 139, 507-19.
40. Lang S., Klein T., Magerl W. & Treede R.-D. (2007) Modality-specific sensory changes in humans after the induction of long-term potentiation (LTP) in cutaneous nociceptive pathways. Pain 128, 254-63.
41. Larson J., Jessen R. E., Kim D., Fine A. K. & du Hoffmann J. (2005) Age-dependent and selective impairment of long-term potentiation in the anterior piriform cortex of mice lacking the fragile X mental retardation protein. Journal of Neuroscience 25, 9460-9.
42. Latremoliere A. & Woolf C. J. (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. The Journal of Pain 10, 895-926.
43. Latremoliere A. & Woolf C. J. (2010) Synaptic plasticity and central sensitization: author reply. The Journal of Pain 11, 801-3.
44. Le Bars D., Dickenson A. H. & Besson J. M. (1979a) Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain 6, 283-304.
45. Le Bars D., Dickenson A. H. & Besson J. M. (1979b) Diffuse noxious inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications. Pain 6, 305-27.
46. Le Bars D., Chitour D., Kraus E., Dickenson A. H. & Besson J. M. (1981) Effect of naloxone upon diffuse noxious inhibitory controls (DNIC) in the rat. Brain Research 204, 387-402.
47. Li J., Pelletier M. R., Perez Velazquez J. L. & Carlen P. L. (2002) Reduced cortical synaptic plasticity and GluR1 expression associated with fragile X mental retardation protein deficiency. Molecular and Cellular Neurosciences 19, 138-51.
48. Luzzani S., Macchini F., Valadè A., Milani D. & Selicorni A. (2003) Gastroesophageal reflux and Cornelia de Lange syndrome: typical and atypical symptoms. American Journal of Medical Genetics. Part A 119A, 283-7.
49. Mailis A. (1996) Compulsive targeted self-injurious behaviour in humans with neuropathic pain: a counterpart of animal autonomy? Four case reports and literature review. Pain 64, 569-78.
50. Martin K. C., Casadio A., Zhu H., Yaping E., Rose J. C., Chen M. etal. (1997) Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91, 927-38.
51. Matson J. L., Dempsey T. & Wilkins J. (2008) Rett syndrome in adults with severe intellectual disability: exploration of behavioral characteristics. European Psychiatry 23, 460-5.
52. Melemedjian O. K., Asiedu M. N., Tillu D. V., Peebles K. A., Yan J., Ertz N. etal. (2010) IL-6- and NGF-induced rapid control of protein synthesis and nociceptive plasticity via convergent signaling to the eIF4F complex. Journal of Neuroscience 30, 15113-23.
53. Melzack R. & Wall P. D. (1965) Pain mechanisms: a new theory. Science 150, 971-9.
54. Mittal R. K., Holloway R. H., Penagini R., Blackshaw L. A. & Dent J. (1995) Transient lower esophageal sphincter relaxation. Gastroenterology 109, 601-10.
55. Moretti P., Levenson J. M., Battaglia F., Atkinson R., Teague R., Antalffy B. etal. (2006) Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. Journal of Neuroscience 26, 319-27.
56. Motil K. J., Schultz R. J., Browning K., Trautwein L. & Glaze D. G. (1999) Oropharyngeal dysfunction and gastroesophageal dysmotility are present in girls and women with Rett syndrome. Journal of Pediatric Gastroenterology and Nutrition 29, 31-7.
57. Newell K. M., Challis J. H., Boros R. L. & Bodfish J. W. (2002a) Further evidence on the dynamics of self-injurious behaviors: impact forces and limb motions. American Journal of Mental Retardation 107, 60-8.
58. Newell K. M., Challis J. H., Boros R. L. & Bodfish J. W. (2002b) Further evidence on the dynamics of self-injurious behaviors: impact forces and limb motions. American Journal of Mental Retardation 107, 60-8.
59. Ossipov M. H., Dussor G. O. & Porreca F. (2010) Central modulation of pain. The Journal of Clinical Investigation 120, 3779-87.
60. Pastalkova E., Serrano P., Pinkhasova D., Wallace E., Fenton A. A. & Sacktor T. C. (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313, 1141-4.
61. Pertovaara A., Kemppainen P., Johansson G. & Karonen S. L. (1982) Ischemic pain nonsegmentally produces a predominant reduction of pain and thermal sensitivity in man: a selective role for endogenous opioids. Brain Research 251, 83-92.
62. Price D. D. (1972) Characteristics of second pain and flexion reflexes indicative of prolonged central summation. Experimental Neurology 37, 371-87.
63. Price D. D., Hu J. W., Dubner R. & Gracely R. H. (1977) Peripheral suppression of first pain and central summation of second pain evoked by noxious heat pulses. Pain 3, 57-68.
64. Price T. J. & Geranton S. M. (2009) Translating nociceptor sensitivity: the role of axonal protein synthesis in nociceptor physiology. The European Journal of Neuroscience 29, 2253-63.
65. Price T. J., Flores C. M., Cervero F. & Hargreaves K. M. (2006) The RNA binding and transport proteins staufen and fragile X mental retardation protein are expressed by rat primary afferent neurons and localize to peripheral and central axons. Neuroscience 141, 2107-16.
66. Price T. J., Rashid M. H., Millecamps M., Sanoja R., Entrena J. M. & Cervero F. (2007) Decreased nociceptive sensitization in mice lacking the fragile X mental retardation protein: role of mGluR1/5 and mTOR. Journal of Neuroscience 27, 13958-67.
67. Roby-Brami A., Bussel B., Willer J. C. & Le Bars D. (1987) An electrophysiological investigation into the pain-relieving effects of heterotopic nociceptive stimuli. Probable involvement of a supraspinal loop. Brain 110(Pt 6), 1497-508.
68. Samaco R. C., Fryer J. D., Ren J., Fyffe S., Chao H. T., Sun Y. etal. (2008) A partial loss of function allele of methyl-CpG-binding protein 2 predicts a human neurodevelopmental syndrome. Human Molecular Genetics 17, 1718-27.
69. Sandkuhler J. (2007) Understanding LTP in pain pathways. Molecular Pain 3, 9.
70. Sandkuhler J. (2010) Central sensitization versus synaptic long-term potentiation (LTP): a critical comment. The Journal of Pain 11, 798-800.
71. Sansom D., Krishnan V. H., Corbett J. & Kerr A. (1993) Emotional and behavioural aspects of Rett syndrome. Developmental Medicine and Child Neurology 35, 340-5.
72. Shema R., Sacktor T. C. & Dudai Y. (2007) Rapid erasure of long-term memory associations in the cortex by an inhibitor of PKM zeta. Science 317, 951-3.
73. Silverman J. L., Tolu S. S., Barkan C. L. & Crawley J. N. (2010) Repetitive self-grooming behavior in the BTBR mouse model of autism is blocked by the mGluR5 antagonist MPEP. Neuropsychopharmacology 35, 976-89.
74. Sondheimer J. M. & Morris B. A. (1979) Gastroesophageal reflux among severely retarded children. The Journal of Pediatrics 94, 710-14.
75. Spitz L., Roth K., Kiely E. M., Brereton R. J., Drake D. P. & Milla P. J. (1993) Operation for gastro-oesophageal reflux associated with severe mental retardation. Archives of Disease in Childhood 68, 347-51.
76. Swender S. L., Matson J. L., Mayville S. B., Gonzalez M. L. & Mcdowell D. (2006) A functional assessment of handmouthing among persons with severe and profound intellectual disability. Journal of Intellectual & Developmental Disability 31, 95-100.
77. Symons F. J. & Danov S. E. (2005) A prospective clinical analysis of pain behavior and self-injurious behavior. Pain 117, 473-7.
78. Symons F. J., Clark R. D., Hatton D. D., Skinner M. & Bailey D. B. Jr (2003) Self-injurious behavior in young boys with fragile X syndrome. American Journal of Medical Genetics. Part A 118, 115-21.
79. Symons F. J., Thompson A. & Rodriguez M. C. (2004) Self-injurious behavior and the efficacy of naltrexone treatment: a quantitative synthesis. Mental Retardation and Developmental Disabilities Research Reviews 10, 193-200.
80. Symons F. J., Harper V., Shinde S. K., Clary J. & Bodfish J. W. (2010) Evaluating a sham-controlled sensory-testing protocol for nonverbal adults with neurodevelopmental disorders: self-injury and gender effects. The Journal of Pain 11, 773-81.
81. The Dutch-Belgian Fragile X Consortium (1994) Fmr1 knockout mice: a model to study fragile X mental retardation. The Dutch-Belgian Fragile X Consortium. Cell 78, 23-33.
82. Turner G., Webb T., Wake S. & Robinson H. (1996) Prevalence of fragile X syndrome. American Journal of Medical Genetics 64, 196-7.
83. Van den Veyver I. B. & Zoghbi H. Y. (2000) Methyl-CpG-binding protein 2 mutations in Rett syndrome. Current Opinion in Genetics & Development 10, 275-9.
84. Whitlock J. R., Heynen A. J., Shuler M. G. & Bear M. F. (2006) Learning induces long-term potentiation in the hippocampus. Science 313, 1093-7.
85. Willer J. C., Roby A., Boulu P. & Boureau F. (1982) Comparative effects of electroacupuncture and transcutaneous nerve stimulation on the human blink reflex. Pain 14, 267-78.
86. Willer J. C., Roby A. & Le Bars D. (1984) Psychophysical and electrophysiological approaches to the pain-relieving effects of heterotopic nociceptive stimuli. Brain 107(Pt 4), 1095-112.
87. Willer J. C., Le Bars D. & De Broucker T. (1990) Diffuse noxious inhibitory controls in man: involvement of an opioidergic link. European Journal of Pharmacology 182, 347-55.
88. Wilson B. M. & Cox C. L. (2007) Absence of metabotropic glutamate receptor-mediated plasticity in the neocortex of fragile X mice. Proceedings of the National Academy of Sciences of the United States of America 104, 2454-9.
89. Woolf C. J. (2010) Central sensitization: implications for the diagnosis and treatment of pain. Pain 152(3 Suppl.), S2-S15.
90. Woolf C. J. & Salter M. W. (2000) Neuronal plasticity: increasing the gain in pain. Science 288, 1765-9.
91. Young R. L., Page A. J., O'Donnell T. A., Cooper N. J. & Blackshaw L. A. (2007) Peripheral versus central modulation of gastric vagal pathways by metabotropic glutamate receptor 5. American Journal of Physiology. Gastrointestinal and Liver Physiology 292, G501-11.
92. Zerbib F., Keywood C. & Strabach G. (2010) Efficacy, tolerability and pharmacokinetics of a modified release formulation of ADX10059, a negative allosteric modulator of metabotropic glutamate receptor 5: an esophageal pH-impedance study in healthy subjects. Neurogastroenterology and Motility 22, 859-65.
93. Zerbib F., Bruley des Varannes S., Roman S., Tutuian R., Galmiche J. P., Mion F. etal. (2011) Randomised clinical trial: effects of monotherapy with ADX10059, a mGluR5 inhibitor, on symptoms and reflux events in patients with gastro-oesophageal reflux disease. Alimentary Pharmacology & Therapeutics 33, 911-21.
94. Zhao M. G., Toyoda H., Ko S. W., Ding H. K., Wu L. J. & Zhuo M. (2005) Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. Journal of Neuroscience 25, 7385-92.