Long-lasting effects of perinatal asphyxia on exploration, memory and incentive downshift

International Journal of Developmental Neuroscience

Volumn 29, Issue 6, 2011, Pages 609-619

  Galeano, Pablo ^a   Blanco Calvo, Eduardo ^b,c   Madureira de Oliveira, Diêgo ^d   Cuenya, Lucas ^e   Kamenetzky, Giselle Vanesa ^e   Mustaca, Alba Elisabeth ^e   Barreto, George Emilio ^f   Giraldez Alvarez, Lisandro Diego ^d   Milei, José ^a   Capani, Francisco ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSITY OF MÁLAGA   (Spain)

^c HOSPITAL REGIONAL UNIVERSITARIO DE MÁLAGA   (Spain)

^d FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^e INSTITUTO DE INVESTIGACIONES MÉDICAS ALFREDO LANARI   (Argentina)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anxiety; Exploration; Incentive downshift; Perinatal asphyxia; Reference memory; Spatial working memory

Indexed keywords

SUCROSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BEHAVIOR DISORDER; BIRTH; CESAREAN SECTION; CONTROLLED STUDY; EMOTION; EXPERIMENTAL TEST; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; FEMALE; INCENTIVE DOWNSHIFT; MALE; MAZE TEST; MEMORY DISORDER; MORRIS WATER MAZE TEST; MOTOR PERFORMANCE; NONHUMAN; OPEN FIELD TEST; PERINATAL ASPHYXIA; PRIORITY JOURNAL; RAT; REFERENCE MEMORY; REWARD; SPATIAL MEMORY; VAGINAL DELIVERY; WORKING MEMORY;

ANIMALS; ASPHYXIA NEONATORUM; BEHAVIOR, ANIMAL; COGNITION DISORDERS; EXPLORATORY BEHAVIOR; FEMALE; HUMANS; INFANT, NEWBORN; MALE; MEMORY; MEMORY DISORDERS; MOTIVATION; MOTOR ACTIVITY; NEUROPSYCHOLOGICAL TESTS; PREGNANCY; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA; RATTUS;

EID: 80052401819     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2011.05.002     Document Type: Article

References (70)

1. Adcock L.M., Papile L.A. Perinatal asphyxia. Manual of Neonatal Care 2008, 518-528. Lippincott Williams & Wilkins, Philadelphia, PA, USA. J.P. Cloherty, E.C. Eichenwald, A.R. Stark (Eds.).
2. Amsel A. Frustration Theory: An Analysis of Dispositional Learning and Memory 1992, Cambridge University Press, Cambridge.
3. Arteni N.S., Pereira L.O., Rodrigues A.L., Lavinsky D., Achaval M.E., Netto C.A. Lateralized and sex-dependent behavioral and morphological effects of unilateral neonatal cerebral hypoxia-ischemia in the rat. Behav. Brain Res. 2010, 210:92-98.
4. Azzopardi D.V., Strohm B., Edwards A.D., Dyet L., Halliday H.L., Juszczak E., Kapellou O., Levene M., Marlow N., Porter E., Thoresen M., Whitelaw A., Brocklehurst P. TOBY study group Moderate hypothermia to treat perinatal asphyxial encephalopathy. N. Engl. J. Med. 2009, 361:1349-1358.
5. Bentosela M., Ruetti E., Muzio R.N., Mustaca A.E., Papini M.R. Administration of corticosterone after the first downshift trial enhances consummatory successive negative contrast. Behav. Neurosci. 2006, 120:371-376.
6. Berger R., Garnier Y. Pathophysiology of perinatal brain damage. Brain Res. Brain Res. Rev. 1999, 30:107-134.
7. Bjelke B., Andersson K., Ogren S.O., Bolme P. Asphyctic lesion: proliferation of tyrosine hydroxylase-immunoreactive nerve cell bodies in the rat substantia nigra and functional changes in dopamine neurotransmission. Brain Res. 1991, 543:1-9.
8. Boksa P., El-Khodor B.F. Birth insult interacts with stress at adulthood to alter dopaminergic function in animal models: possible implications for schizophrenia and other disorders. Neurosci. Biobehav. Rev. 2003, 27:91-101.
9. Boksa P., Krishnamurthy A., Brooks W. Effects of a period of asphyxia during birth on spatial learning in the rat. Pediatr. Res. 1995, 37:489-496.
10. Boksa P., Krishnamurthy A., Sharma S. Hippocampal and hypothalamic type I corticosteroid receptor affinities are reduced in adult rats born by a caesarean procedure with or without an added period of anoxia. Neuroendocrinology 1996, 64:25-34.
11. Boksa P., Wilson D., Rochford J. Responses to stress and novelty in adult rats born vaginally, by cesarean section or by cesarean section with acute anoxia. Biol. Neonate 1998, 74:48-59.
12. Borg E. Perinatal asphyxia, hypoxia, ischemia and hearing loss. An overview. Scand. Audiol. 1997, 26:77-91.
13. Bradshaw J.L. Animal asymmetry and human heredity: dextrality, tool use and language in evolution-10 years after Walker (1980). Br. J. Psychol. 1991, 82:39-59.
14. Brake W.G., Sullivan R.M., Gratton A. Perinatal distress leads to lateralized medial prefrontal cortical dopamine hypofunction in adult rats. J. Neurosci. 2000, 20:5538-5543.
15. Cannon M., Jones P.B., Murray R.M. Obstetric complications and schizophrenia: historical and meta-analytic review. Am. J. Psychiatry 2002, 159:1080-1092.
16. Capani F., Loidl F., Lopez-Costa J.J., Selvin-Testa A., Saavedra J.P. Ultrastructural changes in nitric oxide synthase immunoreactivity in the brain of rats subjected to perinatal asphyxia: neuroprotective effects of cold treatment. Brain Res. 1997, 775:11-23.
17. Capani F., Loidl C.F., Aguirre F., Piehl L., Facorro G., Hager A., De Paoli T., Farach H., Pecci-Saavedra J. Changes in reactive oxygen species (ROS) production in rat brain during global perinatal asphyxia: an ESR study. Brain Res. 2001, 914:204-207.
18. Capani F., Loidl C.F., Piehl L.L., Facorro G., De Paoli T., Hager A. Long term production of reactive oxygen species during perinatal asphyxia in the rat central nervous system: effects of hypothermia. Int. J. Neurosci. 2003, 113:641-654.
19. Capani F., Saraceno G.E., Botti V., Aon-Bertolino L., de Oliveira D.M., Barreto G., Galeano P., Giraldez-Alvarez L.D., Coirini H. Protein ubiquitination in postsynaptic densities after hypoxia in rat neostriatum is blocked by hypothermia. Exp. Neurol. 2009, 219:404-413.
20. Carlini V.P., Monzón M.E., Varas M.M., Cragnolini A.B., Schiöth H.B., Scimonelli T.N., de Barioglio S.R. Ghrelin increases anxiety-like behavior and memory retention in rats. Biochem. Biophys. Res. Commun. 2002, 299:739-743.
21. Cassel J.C., Cassel S., Galani R., Kelche C., Will B., Jarrard L. Fimbria-fornix vs selective hippocampal lesions in rats: effects on locomotor activity and spatial learning and memory. Neurobiol. Learn. Mem. 1998, 69:22-45.
22. Cebral E., Capani F., Selvín-Testa A., Funes M.R., Coirini H., Loidl C.F. Neostriatal cytoskeleton changes following perinatal asphyxia: effect of hypothermia treatment. Int. J. Neurosci. 2006, 116:697-714.
23. Cebral E., Loidl C.F. Changes in neostriatal and hippocampal synaptic densities in perinatal asphyctic male and female young rats: Role of hypothermia. Brain Res. Bull. 2011, 84:31-38.
24. Chen Y., Ogren S.O., Bjelke B., Bolme P., Eneroth P., Gross J., Loidl F., Herrera-Marschitz M., Andersson K. Nicotine treatment counteracts perinatal asphyxia-induced changes in the mesostriatal/limbic dopamine systems and in motor behavior in the four-week-old male rat. Neuroscience 1995, 68:531-538.
25. Crofts B.J., King R., Johnson A. The contribution of low birth weight to severe vision loss in a geographically defined population. Br. J. Ophthalmol. 1998, 82:9-13.
26. de Haan M., Wyatt J.S., Roth S., Vargha-Khadem F., Gadian D., Mishkin M. Brain and cognitive-behavioral development after asphyxia at term birth. Dev. Sci. 2006, 9:350-358.
27. Engidawork E., Loidl F., Chen Y., Kohlhauser C., Stoeckler S., Dell'Anna E., Lubec B., Lubec G., Goiny M., Gross J., Andersson K., Herrera-Marschitz M. Comparison between hypothermia and glutamate antagonism treatments on the immediate outcome of perinatal asphyxia. Exp. Brain Res. 2001, 138:375-383.
28. Fernandes C., González M.I., Wilson C.A., File S.E. Factor analysis shows that female rat behavior is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol. Biochem. Behav. 1999, 64:731-738.
29. Flaherty C.F. Incentive Relativity 1996, Cambrige University Press, Cambridge, England.
30. Flaherty C.F., Grigson P.S., Rowan G.A. Chlordiazepoxide and the determinants of contrast. Anim. Learn. Behav. 1986, 14:315-321.
31. Hill A. Current concepts of hypoxic-ischemic cerebral injury in the term newborn. Pediatr. Neurol. 1991, 7:317-325.
32. Hill A., Volpe J.J. Seizures, hypoxic-ischemic brain injury, and intraventricular hemorrhage in the newborn. Ann. Neurol. 1981, 10:109-121.
33. Hoeger H., Engelmann M., Bernert G., Seidl R., Bubna-Littitz H., Mosgoeller W., Lubec B., Lubec G. Long term neurological and behavioral effects of graded perinatal asphyxia in the rat. Life Sci. 2000, 66:947-962.
34. Hoeger H., Engidawork E., Stolzlechner D., Bubna-Littitz H., Lubec B. Long-term effect of moderate and profound hypothermia on morphology, neurological, cognitive and behavioral functions in a rat model of perinatal asphyxia. Amino Acids 2006, 31:385-396.
35. Johnston A.L., File S.E. Sex differences in animal tests of anxiety. Physiol. Behav. 1991, 49:245-250.
36. Kamenetzky G.V., Mustaca A.E., Pedron V.T., Cuenya L., Papini M.R. Ethanol facilitates consummatory extinction. Behav. Processes 2009, 82:352-354.
37. Kohlhauser C., Kaehler S., Mosgoeller W., Singewald N., Kouvelas D., Prast H., Hoeger H., Lubec B. Histological changes and neurotransmitter levels three months following perinatal asphyxia in the rat. Life Sci. 1999, 64:2109-2124.
38. Lewis S.W., Murray R.M. Obstetric complications, neurodevelopmental deviance, and risk of schizophrenia. J. Psychiatr. Res. 1987, 21:413-421.
39. Loidl C.F., Gavilanes A.W., Van Dijk E.H., Vreuls W., Blokland A., Vles J.S., Steinbusch H.W., Blanco C.E. Effects of hypothermia and gender on survival and behavior after perinatal asphyxia in rats. Physiol. Behav. 2000, 68:263-269.
40. Lubec B., Dell'Anna E., Fang-Kircher S., Marx M., Herrera-Marschitz M., Lubec G. Decrease of brain protein kinase C, protein kinase A, and cyclin-dependent kinase correlating with pH precedes neuronal death in neonatal asphyxia. J. Investig. Med. 1997, 45:284-294.
41. McGuire W. Perinatal asphyxia. Clin. Evid. 2006, 511-519.
42. Miranda R., Blanco E., Begega A., Rubio S., Arias J.L. Hippocampal and caudate metabolic activity associated with different navigational strategies. Behav. Neurosci. 2006, 120:641-650.
43. Mitchell C., Flaherty C. Temporal dynamics of corticosterone elevation in successive negative contrast. Physiol. Behav. 1998, 64:287-292.
44. Morales P., Simola N., Bustamante D., Lisboa F., Fiedler J., Gebicke-Haerter P.J., Morelli M., Tasker R.A., Herrera-Marschitz M. Nicotinamide prevents the long-term effects of perinatal asphyxia on apoptosis, non-spatial working memory and anxiety in rats. Exp. Brain Res. 2010, 202:1-14.
45. Morris R.G.M. Spatial localisation does not depend on the presence of local cues. Learn. Motiv. 1981, 12:239-260.
46. Morris R.G.M., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
47. Mustaca A.E., Bentosela M., Papini M.R. Consummatory successive negative contrast in mice. Learn. Motiv. 2000, 31:272-282.
48. Papini M.R. Comparative psychology of surprising nonreward. Brain Behav. Evol. 2003, 62:83-95.
49. Pecoraro N., de Jong H., Dallman M.F. An unexpected reduction in sucrose concentration activates the HPA axis on successive post shift days without attenuation by discriminative contextual stimuli. Physiol. Behav. 2009, 96:651-661.
50. Pellow S., Chopin P., File S.E., Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 1985, 14:149-167.
51. Piazza P.V., Deminière J.M., Le Moal M., Simon H. Factors that predict individual vulnerability to amphetamine self-administration. Science 1989, 245:1511-1513.
52. Rodgers R.J., Johnson N.J. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacol. Biochem. Behav. 1995, 52:297-303.
53. Rubio S., Begega A., Santin L.J., Arias J.L. Improvement of spatial memory by (R)-alpha-methylhistamine, a histamine H(3)-receptor agonist, on the Morris water-maze in rat. Behav. Brain Res. 2002, 129:77-82.
54. Ruetti E., Justel N., Mustaca A.E., Papini M.R. Posttrial corticosteron administration enhances the effects of incentive downshift: exploring the boundaries of this effect. Behav. Neurosci. 2009, 123:137-144.
55. Santín L.J., Rubio S., Begega A., Arias J.L. Effects of mammillary body lesions on spatial reference and working memory tasks. Behav. Brain Res. 1999, 1999.
56. Saraceno G.E., Bertolino M.L., Galeano P., Romero J.I., Garcia-Segura L.M., Capani F. Estradiol therapy in adulthood reverses glial and neuronal alterations caused by perinatal asphyxia. Exp. Neurol. 2010, 223:615-622.
57. Sawaguchi T., Goldman-Rakic P.S. D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science 1991, 251:947-950.
58. Seamans J.K., Floresco S.B., Phillips A.G. D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat. J. Neurosci. 1998, 18:1613-1621.
59. Shankaran S., Laptook A.R., Ehrenkranz R.A., Tyson J.E., McDonald S.A., Donovan E.F., Fanaroff A.A., Poole W.K., Wright L.L., Higgins R.D., Finer N.N., Carlo W.A., Duara S., Oh W., Cotton C.M., Stevenson D.K., Stoll B.J., Lemons J.A., Guillet R., Jobe A.H. National Institute of Child Health and Human Development Neonatal Research Network Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N. Engl. J. Med. 2005, 353:1574-1584.
60. Simon H., Scatton B., Moal M.L. Dopaminergic A10 neurones are involved in cognitive functions. Nature 1980, 286:150-151.
61. Simola N., Bustamante D., Pinna A., Pontis S., Morales P., Morelli M., Herrera-Marschitz M. Acute perinatal asphyxia impairs non-spatial memory and alters motor coordination in adult male rats. Exp. Brain Res. 2008, 185:595-601.
62. Strackx E., Van den Hove D.L., Prickaerts J., Zimmermann L., Steinbusch H.W., Blanco C.E., Gavilanes A.W., Vles J.S. Fetal asphyctic preconditioning protects against perinatal asphyxia-induced behavioral consequences in adulthood. Behav. Brain Res. 2010, 208:343-351.
63. Van de Berg W.D., Kwaijtaal M., de Louw A.J., Lissone N.P., Schmitz C., Faull R.L., Blokland A., Blanco C.E., Steinbusch H.W. Impact of perinatal asphyxia on the GABAergic and locomotor system. Neuroscience 2003, 117:83-96.
64. van Handel M., Swaab H., de Vries L.S., Jongmans M.J. Long-term cognitive and behavioral consequences of neonatal encephalopathy following perinatal asphyxia: a review. Eur. J. Pediatr. 2007, 166:645-654.
65. Vannucci R.C. Experimental biology of cerebral hypoxia-ischemia: relation to perinatal brain damage. Pediatr. Res. 1990, 27:317-326.
66. Vorhees C.V., Williams M.T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 2006, 1:848-858.
67. Wakuda T., Matsuzaki H., Suzuki K., Iwata Y., Shinmura C., Suda S., Iwata K., Yamamoto S., Sugihara G., Tsuchiya K.J., Ueki T., Nakamura K., Nakahara D., Takei N., Mori N. Perinatal asphyxia reduces dentate granule cells and exacerbates methamphetamine-induced hyperlocomotion in adulthood. PLoS One 2008, 3:e3648.
68. Walsh R.N., Cummins R.A. The open-field test: a critical review. Psychol. Bull. 1976, 83:482-504.
69. Weitzdoerfer R., Pollak A., Lubec B. Perinatal asphyxia in the rat has lifelong effects on morphology, cognitive functions, and behavior. Semin. Perinatol. 2004, 28:249-256.
70. Younkin D.P. Hypoxic-ischemic brain injury of the newborn-statement of the problem and overview. Brain Pathol. 1992, 2:209-210.