Ketamine administered to pregnant rats in the second trimester causes long-lasting behavioral disorders in offspring

Neurobiology of Disease

Volumn 68, Issue , 2014, Pages 145-155

  Zhao, Tianyun ^a   Li, Yuantao ^a   Wei, Wei ^b   Savage, Sinead ^c   Zhou, Libing ^d   Ma, Daqing ^c  

^a Nanfang Medical University   (China)

^b MEIZHOU HOSPITAL AFFILIATED TO SUN YAT SEN UNIVERSITY   (China)

^c CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^d JINAN UNIVERSITY   (China)

Author keywords

Brain development; Cognition; Depression; Ketamine; NMDA receptor; Pregnancy

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; POSTSYNAPTIC DENSITY PROTEIN 95; ANALGESIC AGENT;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR DISORDER; BRAIN DEVELOPMENT; CELL LOSS; CELL PROLIFERATION; CONTINUOUS INFUSION; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; DEPRESSION; DOWN REGULATION; FEMALE; HIPPOCAMPAL CA3 REGION; LEARNING DISORDER; MEMORY DISORDER; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PUP (RODENT); PYRAMIDAL NERVE CELL; RAT; SECOND TRIMESTER PREGNANCY; SPATIAL MEMORY; SUBVENTRICULAR ZONE; UPREGULATION; YOUNG ADULT; AGE; ANIMAL; BODY TEMPERATURE; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; FOOD PREFERENCE; GENE EXPRESSION REGULATION; GESTATIONAL AGE; GROWTH, DEVELOPMENT AND AGING; HIPPOCAMPUS; LATERAL BRAIN VENTRICLE; MALE; MAZE TEST; MENTAL DISORDERS; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

AGE FACTORS; ANALGESICS; ANIMALS; ANIMALS, NEWBORN; BODY TEMPERATURE; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEMALE; FOOD PREFERENCES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; HIPPOCAMPUS; KETAMINE; LATERAL VENTRICLES; MALE; MAZE LEARNING; MENTAL DISORDERS; NEURONS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84901338726     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.02.009     Document Type: Article

References (58)

1. Alladin A. The power of belief and expectancy in understanding and management of depression. Am. J. Clin. Hypn. 2013, 55:249-271.
2. Bambico F.R., et al. Decline in serotonergic firing activity and desensitization of 5-HT1A autoreceptors after chronic unpredictable stress. Eur. Neuropsychopharmacol. 2009, 19:215-228.
3. Brambrink A.M., et al. Ketamine-induced neuroapoptosis in the fetal and neonatal rhesus macaque brain. Anesthesiology 2012, 116:372-384.
4. Brocardo P.S., et al. Anxiety- and depression-like behaviors are accompanied by an increase in oxidative stress in a rat model of fetal alcohol spectrum disorders: protective effects of voluntary physical exercise. Neuropharmacology 2012, 62:1607-1618.
5. Castren E., Rantamaki T. The role of BDNF and its receptors in depression and antidepressant drug action: Reactivation of developmental plasticity. Dev. Neurobiol. 2010, 70:289-297.
6. Chao M.V. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 2003, 4:299-309.
7. Cheek T.G., Baird E. Anesthesia for nonobstetric surgery: maternal and fetal considerations. Clin. Obstet. Gynecol. 2009, 52:535-545.
8. Clancy B., et al. Translating developmental time across mammalian species. Neuroscience 2001, 105:7-17.
9. Craven R. Ketamine. Anaesthesia 2007, 62(Suppl. 1):48-53.
10. Crocker L.D., et al. Relationships among cognition, emotion, and motivation: implications for intervention and neuroplasticity in psychopathology. Front. Hum. Neurosci. 2013, 7:261.
11. Cryan J.F., et al. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci. Biobehav. Rev. 2005, 29:547-569.
12. Dargan P.I., Wood D.M. Recreational drug use in the Asia Pacific region: improvement in our understanding of the problem through the UNODC programmes. J. Med. Toxicol. 2012, 8:295-299.
13. David D.J., et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 2009, 62:479-493.
14. Day N.L., et al. The effects of prenatal marijuana exposure on delinquent behaviors are mediated by measures of neurocognitive functioning. Neurotoxicol. Teratol. 2011, 33:129-136.
15. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev. 2001, 36:60-90.
16. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 2006, 59:1116-1127.
17. Duman R.S., et al. Signaling pathways underlying the rapid antidepressant actions of ketamine. Neuropharmacology 2012, 62:35-41.
18. Famy C., et al. Mental illness in adults with fetal alcohol syndrome or fetal alcohol effects. Am. J. Psychiatry 1998, 155:552-554.
19. Femenia T., et al. Dysfunctional hippocampal activity affects emotion and cognition in mood disorders. Brain Res. 2012, 1476:58-70.
20. Feyissa A.M., et al. Reduced levels of NR2A and NR2B subunits of NMDA receptor and PSD-95 in the prefrontal cortex in major depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33:70-75.
21. Goodman S. Anesthesia for nonobstetric surgery in the pregnant patient. Semin. Perinatol. 2002, 26:136-145.
22. Green C.J., et al. Ketamine alone and combined with diazepam or xylazine in laboratory animals: a 10year experience. Lab. Anim. 1981, 15:163-170.
23. Hajszan T., et al. Short-term treatment with the antidepressant fluoxetine triggers pyramidal dendritic spine synapse formation in rat hippocampus. Eur. J. Neurosci. 2005, 21:1299-1303.
24. Hansen T.G., et al. Academic performance in adolescence after inguinal hernia repair in infancy: a nationwide cohort study. Anesthesiology 2011, 114:1076-1085.
25. Ikonomidou C., et al. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 2000, 287:1056-1060.
26. Ing C., et al. Long-term differences in language and cognitive function after childhood exposure to anesthesia. Pediatrics 2012, 130:e476-e485.
27. Iosifescu D.V. The relation between mood, cognition and psychosocial functioning in psychiatric disorders. Eur. Neuropsychopharmacol. 2012, 22(Suppl. 3):S499-S504.
28. Jevtovic-Todorovic V., et al. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J. Neurosci. 2003, 23:876-882.
29. Kalkman C.J., et al. Behavior and development in children and age at the time of first anesthetic exposure. Anesthesiology 2009, 110:805-812.
30. Karolewicz B., et al. Elevated levels of the NR2C subunit of the NMDA receptor in the locus coeruleus in depression. Neuropsychopharmacology 2005, 30:1557-1567.
31. Karolewicz B., et al. Elevated levels of NR2A and PSD-95 in the lateral amygdala in depression. Int. J. Neuropsychopharmacol. 2009, 12:143-153.
32. Kong F.J., et al. Fetal exposure to high isoflurane concentration induces postnatal memory and learning deficits in rats. Biochem. Pharmacol. 2012, 84:558-563.
33. Ladurelle N., et al. Agomelatine (S20098) modulates the expression of cytoskeletal microtubular proteins, synaptic markers and BDNF in the rat hippocampus, amygdala and PFC. Psychopharmacology (Berl.) 2012, 221:493-509.
34. Malberg J.E., Duman R.S. Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 2003, 28:1562-1571.
35. Masi G., Brovedani P. The hippocampus, neurotrophic factors and depression: possible implications for the pharmacotherapy of depression. CNS Drugs 2011, 25:913-931.
36. McEwen B.S., et al. Prevention of stress-induced morphological and cognitive consequences. Eur. Neuropsychopharmacol. 1997, 7(Suppl. 3):S323-S328.
37. McEwen B.S., et al. Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 2012, 62:3-12.
38. Nestler E.J., Hyman S.E. Animal models of neuropsychiatric disorders. Nat. Neurosci. 2010, 13:1161-1169.
39. O'Connor M.J., Paley B. The relationship of prenatal alcohol exposure and the postnatal environment to child depressive symptoms. J. Pediatr. Psychol. 2006, 31:50-64.
40. Olney J.W., et al. The enigma of fetal alcohol neurotoxicity. Ann. Med. 2002, 34:109-119.
41. Palanisamy A., et al. Rats exposed to isoflurane in utero during early gestation are behaviorally abnormal as adults. Anesthesiology 2011, 114:521-528.
42. Papazacharias A., Nardini M. The relationship between depression and cognitive deficits. Psychiatr. Danub. 2012, 24(Suppl. 1):S179-S182.
43. Pham K., et al. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 2003, 17:879-886.
44. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 2003, 463:3-33.
45. Richardson G.A., et al. Prenatal cocaine exposure: effects on mother- and teacher-rated behavior problems and growth in school-age children. Neurotoxicol. Teratol. 2011, 33:69-77.
46. Rofael H.Z., et al. Immunomodulation by cocaine and ketamine in postnatal rats. Toxicology 2003, 188:101-114.
47. Rygula R., et al. Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav. Brain Res. 2005, 162:127-134.
48. Satomoto M., et al. Neonatal exposure to sevoflurane induces abnormal social behaviors and deficits in fear conditioning in mice. Anesthesiology 2009, 110:628-637.
49. Shapiro M. Plasticity, hippocampal place cells, and cognitive maps. Arch. Neurol. 2001, 58:874-881.
50. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 1953, 87:387-406.
51. Slikker W.J., et al. Ketamine-induced neuronal cell death in the perinatal rhesus monkey. Toxicol. Sci. 2007, 98:145-158.
52. Smith D.M., Mizumori S.J. Hippocampal place cells, context, and episodic memory. Hippocampus 2006, 16:716-729.
53. Stewart M.G., et al. Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: a three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities. Neuroscience 2005, 131:43-54.
54. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res. Rev. 2007, 53:198-214.
55. Toro C., Deakin J.F. NMDA receptor subunit NRI and postsynaptic protein PSD-95 in hippocampus and orbitofrontal cortex in schizophrenia and mood disorder. Schizophr. Res. 2005, 80:323-330.
56. Viberg H., et al. Neonatal ketamine exposure results in changes in biochemical substrates of neuronal growth and synaptogenesis, and alters adult behavior irreversibly. Toxicology 2008, 249:153-159.
57. Watanabe Y., et al. Tianeptine attenuates stress-induced morphological changes in the hippocampus. Eur. J. Pharmacol. 1992, 222:157-162.
58. Zheng H., et al. Sevoflurane anesthesia in pregnant mice induces neurotoxicity in fetal and offspring mice. Anesthesiology 2013, 118:516-526.