Neonatal ventral hippocampal lesions modify pain perception and evoked potentials in rats

Behavioural Brain Research

Volumn 234, Issue 2, 2012, Pages 167-174

  Sandner, Guy ^a   Meyer, Laurence ^a   Angst, Marie Josée ^a   Guignard, Blandine ^a   Guiberteau, Thierry ^a   Mensah Nyagan, Ayikoe Guy ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Audition; Schizophrenia; Sensory gating; Tactile; Vision

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; AUDITORY THRESHOLD; CONTROLLED STUDY; EVOKED AUDITORY RESPONSE; EVOKED VISUAL RESPONSE; MALE; MECHANICAL STIMULATION; NOCICEPTION; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; RAT; RESPONSE TIME; SCHIZOPHRENIA; SENSORY DYSFUNCTION; SENSORY GATING; TACTILE STIMULATION; THERMAL STIMULATION; VISUAL STIMULATION;

ACOUSTIC STIMULATION; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; AUDITORY THRESHOLD; CEREBRAL CORTEX; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, AUDITORY; EXTREMITIES; HIPPOCAMPUS; HYPERALGESIA; MAGNETIC RESONANCE IMAGING; MALE; PAIN MEASUREMENT; PAIN PERCEPTION; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SENSORY GATING;

EID: 84864056566     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.06.026     Document Type: Article

References (74)

1. Harrison P.J. Schizophrenia: a disorder of neurodevelopment. Current Opinion in Neurobiology 1997, 7:285-289.
2. Schultz S.K., Andreasen N.C. Schizophrenia. Lancet 1999, 353:1425-1430.
3. Lewis D.A., Lieberman J.A. Catching up on schizophrenia: natural history and neurobiology. Neuron 2000, 28:325-334.
4. Ashe P.C., Berry M.D., Boulton A.A. Schizophrenia, a neurodegenerative disorder with neurodevelopmental antecedents. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2001, 25:691-707.
5. Mechri A., Bourdel M.C., Slama H., Gourion D., Gaha L., Krebs M.O. Neurological soft signs in patients with schizophrenia and their unaffected siblings: frequency and correlates in two ethnic and socioeconomic distinct populations. European Archives of Psychiatry and Clinical Neuroscience 2009, 259:218-226.
6. Van Os J. Are psychiatric diagnoses of psychosis scientific and useful? The case of schizophrenia. Journal of Mental Health 2010, 19:305-317.
7. Silverstein S.M., Keane B.P. Perceptual organization impairment in schizophrenia and associated brain mechanisms: review of research from 2005 to 2010. Schizophrenia Bulletin 2011, 37:690-699.
8. Posner M.I. Attention: the mechanisms of consciousness. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:7398-7403.
9. Baddeley A. Working memory: theories, models, and controversies. Annual Review of Psychology 2012, 63:1-29.
10. Lalanne L., Dufour A., Després O., Giersch A. Attention and masking in schizophrenia. Biological Psychiatry 2012, 71:162-168.
11. Salamé P., Danion J.M., Peretti S., Cuervo C. The state of functioning of working memory in schizophrenia. Schizophrenia Research 1998, 30:11-29.
12. Ikuda T., Furuda N., Kihara S., Okura M., Nagamine I., Nakayama H., et al. Differences in waveforms of cerebral evoked potentials among healthy subjects, schizophrenics, manic-depressives and epileptics. Journal of Medical Investigation 2007, 54:303-315.
13. Potvin S., Marchand S. Hypoalgesia in schizophrenia is independent of antipsychotic drugs: a systematic quantitative review of experimental studies. Pain 2009, 138:70-78.
14. De la Fuente-Sandoval C., Favila R., Gómez-Martin D., Pellicer F., Graff-Guerrero A. Functional magnetic resonance imaging response to experimental pain in drug-free patients with schizophrenia. Psychiatry Research 2010, 183:99-104.
15. Lipska B.K. Using animal models to test a neurodevelopmental hypothesis of schizophrenia. Journal of Psychiatry and Neuroscience 2004, 29:282-286.
16. Tseng K.Y., Chambers R.A., Lipska B.K. Neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia. Behavioural Brain Research 2009, 204:295-305.
17. O'Donnell P. Cortical disinhibition in the neonatal ventral hippocampal lesion model of schizophrenia: new vistas on possible therapeutic approaches. Pharmacology & Therapeutics 2012, 133:19-25.
18. Angst M.J., Macedo C.E., Guiberteau T., Sandner G. Alteration of conditioned emotional response and conditioned taste aversion after neonatal ventral hippocampus lesions in rats. Brain Research 2007, 1143:183-192.
19. Macedo C.E., Sandner G., Angst M.J., Guiberteau T. Rewarded associative and instrumental conditioning after neonatal ventral hippocampus lesions in rats. Brain Research 2008, 215:190-199.
20. Macedo C.E., Angst M.J., Guiberteau T., Brasse D., O'Brien T., Sandner G. Acoustic hypersensitivity in adult rats after neonatal ventral hippocampus lesions. Behavioural Brain Research 2009, 207:161-168.
21. Bertrand J.B., Langlois J.B., Bégou M., Volle J., Brun P., d'Amato T., et al. Longitudinal MRI monitoring of brain damage in the neonatal ventral hippocampal lesion rat model of schizophrenia. Hippocampus 2010, 20:264-278.
22. Halim N.D., Swerdlow N.R. Distributed neurodegenerative changes 2-28 days after ventral hippocampal excitotoxic lesions in rats. Brain Research 2000, 873:60-74.
23. Meyer L., Patte-Mensah C., Taleb O., Mensah-Nyagan A.G. Cellular and functional evidence for a protective action of neurosteroids against vincristine chemotherapy-induced painful neuropathy. Cellular and Molecular Life Sciences 2010, 67:3017-3034.
24. Meyer L., Patte-Mensah C., Taleb O., Mensah-Nyagan A.G. Allopregnanolone prevents and suppresses oxaliplatin-evoked painful neuropathy: multi-parametric assessment and direct evidence. Pain 2011, 152:170-181.
25. Patte-Mensah C., Meyer L., Schaeffer V., Mensah-Nyagan A.G. Selective regulation of 3 alpha-hydroxysteroid oxido-reductase expression in dorsal root ganglion neurons: a possible mechanism to cope with peripheral nerve injury-induced chronic pain. Pain 2010, 150:522-534.
26. Schaeffer V., Meyer L., Patte-Mensah C., Mensah-Nyagan A.G. Progress in dorsal root ganglion neurosteroidogenic activity: basic evidence and pathophysiological correlation. Progress in Neurobiology 2010, 92:33-41.
27. Iwamura Y., Fujii Y., Kamei C. The effects of selective serotonin-reuptake inhibitor on visual evoked potential in rats. Journal of Pharmacological Sciences 2004, 94:271-276.
28. Agrawal G., Thakor N.V., All A.H. Evoked potential versus behavior to detect minor insult to the spinal cord in a rat model. Journal of Clinical Neuroscience 2009, 16:1052-1055.
29. Breier M.R., Lewis B., Shoemaker J.M., Light G.A., Swerdlow N.R. Sensory and sensorimotor gating-disruptive effects of apomorphine in Sprague Dawley and Long Evans rats. Behavioural Brain Research 2010, 208:560-565.
30. Broberg B.V., Oranje B., Glenthøj B.Y., Fejgin K., Plath N., Bastlund J.F. Assessment of auditory sensory processing in a neurodevelopmental animal model of schizophrenia: gating of auditory-evoked potentials and prepulse inhibition. Behavioural Brain Research 2010, 213:142-147.
31. Miyasato H., Skinner R.D., Garcia-Rill E. Locus coeruleus involvement in the effects of immobilization stress on the P13 midlatency auditory evoked potential in the rat. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2000, 24:1177-1201.
32. Vohs J.L., Chambers R.A., Krishnan G.P., O'Donnell B.F., Hetrick W.P., Kaiser S.T., et al. Auditory sensory gating in the neonatal ventral hippocampal lesion model of schizophrenia. Neuropsychobiology 2009, 60:12-22.
33. Takahashi H., Nakao M., Kaga K. Multiple neural origins of early auditory evoked potential of rats. Neuroscience 2007, 148:845-856.
34. Sandner G., Angst M.J., Guiberteau T., Guignard B., Brasse D. MRI and X-ray scanning images of the brain of 3-, 6- and 9-month-old rats with bilateral neonatal ventral hippocampus lesions. Neuroimage 2010, 53:44-50.
35. Sandner G., Host L., Angst M.J., Guiberteau T., Guignard B., Zwiller J. The HDAC inhibitor phenylbutyrate reverses effects of neonatal ventral hippocampal lesion in rats. Front Psychiatry 2011, 1:153.
36. Al Amin H.A., Atweh S.F., Jabbur S.J., Saade N.E. Effects of ventral hippocampal lesion on thermal and mechanical nociception in neonates and adult rats. European Journal of Neuroscience 2004, 0:3027-3034.
37. Shaw F.Z., Chen R.F., Yen C.T. Dynamic changes of touch- and laser heat-evoked field potentials of primary somatosensory cortex in awake and pentobarbital-anesthetized rats. Brain Research 2001, 911:105-115.
38. Park Y.M., Lee S.H., Kim S., Bae S.M. The loudness dependence of the auditory evoked potential (LDAEP) in schizophrenia, bipolar disorder, major depressive disorder, anxiety disorder, and healthy controls. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2010, 34:313-316.
39. Klein A.H., Sawyer C.M., Carstens M.L., Tsagareli M.G., Tsiklauri N., Carstens N. Topical application of l-menthol induces heat analgesia, mechanical allodynia, and a biphasic effect on cold sensitivity in rats. Behavioural Brain Research 2010, 212:179-186.
40. Cavanaugh D.J., Lee H., Lo L., Shields S.D., Zylka M.J., Basbaum A.I., et al. Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:9075-9080.
41. Fernando A.B.P., Robbins T.W. Animal models of neuropsychiatric disorders. Annul Review of Clinical Psychology 2011, 7:39-61.
42. Becker A., Grecksch G., Schröder H. Pain sensitivity is altered in animals after subchronic ketamine treatment. Psychopharmacology (Berlin) 2006, 189:237-247.
43. Meng Q., Li N., Han X., Shao F., Wang W. Peri-adolescence isolation rearing alters social behavior and nociception in rats. Neuroscience Letters 2010, 480:25-29.
44. Charlet A., Muller A.H., Laux A., Kemmel V., Schweitzer A., Deloulme J.C., et al. Abnormal nociception and opiate sensitivity of STOP null mice exhibiting elevated levels of the endogenous alkaloid morphine. Molecular Pain 2010, 6:96.
45. Walsh J., Tighe O., Lai D., Harvey R., Karayiorgou M., Gogos J.A., et al. Disruption of thermal nociceptive behaviour in mice mutant for the schizophrenia-associated genes NRG1, COMT and DISC. Brain Research 2010, 1348:114-119.
46. Morgan M.J. Franklin KBJ.6-hydroxydopamine lesions of the ventral tegmentum abolish d-amphetamine and morphine analgesia in the formalin test but not in the tail flick test. Brain Research 1990, 519:144-149.
47. Dalal S., Melzack R. Psychostimulant drugs potentiate morphine analgesia in the formalin test. Journal of Pain and Symptom Management 1998, 16:230-239.
48. Hetem L.A., Danion J.M., Diemunsch P., Brandt C. Effect of a subanesthetic dose of ketamine on memory and conscious awareness in healthy volunteers. Psychopharmacology (Berlin) 2000, 152:283-288.
49. Manahan-Vaughan D., von Haebler D., Winter C., Juckel G., Heinemann U. A single application of MK801 causes symptoms of acute psychosis, deficits in spatial memory, and impairment of synaptic plasticity in rats. Hippocampus 2008, 18:125-134.
50. Murthy B.V.S., Narayan B., Nayagam S. Reduced perception of pain in schizophrenia: its relevance to the clinical diagnosis of compartment syndrome. Injury 2004, 35:1192-1193.
51. Virit O., Savas H.A., Altindag A. Lack of pain in schizophrenia: a patient whose arm was burned and amputated. General Hospital Psychiatry 2008, 30:384-385.
52. Murakami H., Tamasawa N., Yamashita M., Takayasu S., Nigawara T., Matsui J., et al. Altered pain perception in schizophrenia. Lancet 2010, 375:864.
53. Dworkin R.H. Pain insensitivity in schizophrenia: a neglected phenomenon and some implications. Schizophrenia Bulletin 1994, 2:235-248.
54. Bonnot O., Anderson G.M., Cohen D., Willer J.C., Tordjman S. Are patients with schizophrenia insensitive to pain? A reconsideration of the question. Clinical Journal of Pain 2009, 25:244-252.
55. Blumensohn Rl Ringler D., Eli I. Pain perception in patients with schizophrenia. Journal of Nervous and Mental Disease 2002, 190:481-483.
56. Jochum T., Letzsch A., Greiner W., Wagner G., Sauer H., Bär K.J. Influence of antipsychotic medication on pain perception in schizophrenia. Psychiatry Research 2006, 142:151-156.
57. Rabinowicz E.F., Silipo G., Goldman R., Javitt D.C. Auditory sensory dysfunction in schizophrenia: imprecision or distractibility. Archives of General Psychiatry 2000, 57:1149-1155.
58. Bramon E., Rabe-Hesketh S., Sham P., Murray R.M., Frangou S. Meta-analysis of the P300 and P50 waveforms in schizophrenia. Schizophrenia Research 2004, 70:315-329.
59. Butler P.D., Martinez A., Foxe J.J., Kim D., Zemon V., Silipo G., et al. Subcortical visual dysfunction in schizophrenia drives secondary cortical impairments. Brain 2007, 130:417-430.
60. Yeap S., Kelly S.P., Sehatpour P., Magno E., Garavan H., Thakore J.H., et al. Visual sensory processing deficits in schizophrenia and their relationship to disease state. European Archives of Psychiatry and Clinical Neuroscience 2008, 258:305-316.
61. Koychev I., El-Deredy W., Haenschel C., Deakin J.F.W. Visual information processing deficits as biomarkers of vulnerability to schizophrenia: an event-related potential study in schizotypy. Neuropsychologia 2010, 48:2205-2214.
62. Neuhaus A.H., Trempler N.R., Hahn E., Luborzewski A., Karl C., Hahn C., et al. Evidence of specificity of a visual P3 amplitude modulation deficit in schizophrenia. Schizophrenia Research 2010, 124:119-126.
63. Shi W.X. The auditory cortex in schizophrenia. Biological Psychiatry 2007, 61:829-830.
64. Sweet R.A., Fish K.N., Lewis D.A. Mapping synaptic pathology within cerebral cortical circuits in subjects with schizophrenia. Frontiers in Human Neuroscience 2010, 4:44.
65. Tress K.H., Caudrey D.J., Mehta B. Tactile-evoked potentials in schizophrenia. Interhemispheric transfer and drug effects. British Journal of Psychiatry 1983, 143:156-164.
66. Reite M., Teale P., Rojas D.C., Benkers T.L., Carlson J. Anomalous somatosensory cortical localization in schizophrenia. American Journal of Psychiatry 2003, 160:2148-2153.
67. Joy B., McMahon R.P., Shepard P.D. Effects of acute and chronic clozapine on d-amphetamine-induced disruption of auditory gating in the rat. Psychopharmacology 2004, 174:274-282.
68. Keedy S.K., Marlow-O'Connor M., Beenken B., Dorflinger J., Abel M., Erwin R.J. Noradrenergic antagonism of the P13 and N40 components of the rat auditory evoked potential. Psychopharmacology 2007, 190:117-125.
69. Jansen B.H., Hu L., Boutros N.N. Auditory evoked potential variability in healthy and schizophrenia subjects. Clinical Neurophysiology 2010, 121:1233-1239.
70. Mazhari S., Price G., Waters F., Dragović M., Jablensky A. Evidence of abnormalities in mid-latency auditory evoked responses (MLAER) in cognitive subtypes of patients with schizophrenia. Psychiatry Research 2011, 187:317-323.
71. Battaglia A. Sensory impairment in mental retardation: a potential role for NGF. Archives Italiennes de Biologie 2011, 149:193-203.
72. Cascio C.J. Somatosensory processing in neurodevelopmental disorders. Journal of Neurodevelopmental Disorders 2010, 2:62-69.
73. Nyakas C., Buwalda B., Luiten P.G. Hypoxia and brain development. Progress in Neurobiology 1996, 49:1-51.
74. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, London.