Behavioural outcomes of perinatal maternal fluoxetine treatment

Neuroscience

Volumn 226, Issue , 2012, Pages 356-366

  McAllister, B B ^a,b   Kiryanova, V ^a,b   Dyck, R H ^a,b,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

Anxiety; Depression; Neurodevelopment; Pregnancy; Serotonin; SSRI exposure

Indexed keywords

FLUOXETINE;

ADULTHOOD; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DEPRESSION; EMOTION; FEMALE; MALE; MOUSE; NEUROPSYCHOLOGICAL TEST; NONHUMAN; PERINATAL DRUG EXPOSURE; PREGNANCY; PRIORITY JOURNAL; WEIGHT REDUCTION;

ANIMALS; ANIMALS, NEWBORN; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; BEHAVIOR, ANIMAL; BODY WEIGHT; FEAR; FEMALE; FLUOXETINE; LITTER SIZE; MAZE LEARNING; MEMORY; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; POSTURAL BALANCE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEROTONIN UPTAKE INHIBITORS; SEX CHARACTERISTICS; SEX RATIO; STARTLE REACTION; SWIMMING;

EID: 84867413986     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.024     Document Type: Article

References (60)

1. Alwan S., Friedman J.M. Safety of selective serotonin reuptake inhibitors in pregnancy. CNS Drugs 2009, 2:493-509.
2. Ansorge M.S., Morelli E., Gingrich J.A. Inhibition of serotonin but not norepinephrine transport during development produces delayed, persistent perturbations of emotional behaviors in mice. J Neurosci 2008, 28:199-207.
3. Ansorge M.S., Zhou M., Lira A., Hen R., Gingrich J.A. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 2004, 306:879-881.
4. Azmitia E.C. Modern views on an ancient chemical: serotonin effects on cell proliferation, maturation, and apoptosis. Brain Res Bull 2001, 56:413-424.
5. Bairy K.L., Madhyastha S., Ashok K.P., Bairy I., Malini S. Developmental and behavioral consequences of prenatal fluoxetine. Pharmacology 2007, 79:1-11.
6. Blazevic S., Colic L., Culig L., Hranilovic D. Anxiety-like behavior and cognitive flexibility in adult rats perinatally exposed to increased serotonin concentrations. Behav Brain Res 2012, 230:175-181.
7. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 1998, 95:5335-5340.
8. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behaviour: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005, 29:1193-1205.
9. Cases O., Seit I., Grimsby J., Gaspar P., Chen K., Pournin S., Müller U., Aguet M., Babinet C., Shih J.C., De Maeyer E. Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 1995, 268:1763-1766.
10. Cases O., Vitalis T., Seit I., De Maeyer E., Sotelo C., Gaspar P. Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: role of serotonin excess during the critical period. Neuron 1996, 16:297-307.
11. Casper R.C., Fleisher B.E., Lee-Ancajas J.C., Gilles A., Gaylor E., DeBattista A., Hoyme H.E. Follow-up of children of depressed mothers exposed or not exposed to antidepressant drugs during pregnancy. J Pediatr 2003, 142:402-408.
12. Castagné V., Porsolt R.D., Moser P. Use of latency to immobility improves detection of antidepressant-like activity in the behavioral despair test in the mouse. Eur J Pharmacol 2009, 616:128-133.
13. Chambers C.D., Hernandez-Diaz S., Van Marter L.J., Werler M.M., Louik C., Jones K.L., Mitchell A.A. Selective serotonin-reuptake inhibitors and risk of persistent pulmonary hypertension of the newborn. N Engl J Med 2006, 354:579-597.
14. Chambers C.D., Johnson K.A., Dick L.M., Felix R.J., Jones K.L. Birth outcomes in pregnant women taking fluoxetine. N Engl J Med 1996, 335:1010-1015.
15. Choleris E., Thomas A.W., Kavaliers M., Prato F.S. A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neurosci Biobehav Rev 2001, 25:235-260.
16. Detke M.J., Rickels M., Lucki I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology 1995, 121:66-72.
17. Farr T.D., Liu L., Colwell K.L., Whishaw I.Q., Metz G.A. Bilateral alteration in stepping pattern after unilateral motor cortex injury: a new test strategy for analysis of skilled limb movements in neurological mouse models. J Neurosci Methods 2005, 153:104-113.
18. Freeman-Daniels E., Beck S.G., Kirby L.G. Cellular correlates of anxiety in CA1 hippocampal pyramidal cells of 5-HT1A receptor knockout mice. Psychopharmacology 2011, 213:453-463.
19. Gaspar P., Cases O., Maroteaux L. The developmental role of serotonin: new from mouse molecular genetics. Nat Rev Neurosci 2003, 4:1002-1012.
20. Gavin N.I., Gaynes B.N., Lohr K.N., Meltzer-Brody S., Gartlehner G., Swinson T. Perinatal depression: a systematic review of prevalence and incidence. Obstet Gynecol 2005, 106:1071-1083.
21. Gouvêa T.A., Morimoto H.K., de Faria M.J., Moreira E.G., Gerardin D.C. Maternal exposure to the antidepressant fluoxetine impairs sexual motivation in adult male mice. Pharmacol Biochem Behav 2008, 90:416-419.
22. Hansen H.H., Sánchez C., Meier E. Neonatal administration of the selective serotonin reuptake inhibitor Lu 10-134-C increases forced swimming-induced immobility in adult rats: a putative animal model of depression?. J Pharmacol Exp Ther 1997, 283:1333-1341.
23. Heikkinen T., Ekblad U., Palo P., Laine K. Pharmacokinetics of fluoxetine and norfluoxetine in pregnancy and lactation. Clin Pharmacol Ther 2003, 73:330-337.
24. Hendrick V., Stowe Z.N., Altshuler L.L., Hwang S., Lee E., Haynes D. Placental passage of antidepressant medications. Am J Psychiatry 2003, 160:993-996.
25. Hendrick V., Stowe Z.N., Altshuler L.L., Mintz J., Hwang S., Hostetter A., Suri R., Leight K., Fukuchi A. Fluoxetine and norfluoxetine concentrations in nursing infants and breast milk. Biol Psychiatry 2001, 50:775-782.
26. Hoffman H.S., Ison J.R. Reflex modification in the domain of startle: I. Some empirical findings and their implications for how the nervous system processes sensory input. Psychol Rev 1980, 87:175-189.
27. Holmes A., Murphy D.L., Crawley J.N. Reduced aggression in mice lacking the serotonin transporter. Psychopharmacology 2002, 161:160-167.
28. Holmes A., Yang R.J., Lesch K.P., Crawley J.N., Murphy D.L. Mice lacking the serotonin transporter exhibit 5-HT1A receptor-mediated abnormalities in tests for anxiety-like behavior. Neuropsychopharmacology 2003, 28:2077-2088.
29. Holmes A., Yang R.J., Murphy D.L., Crawley J.N. Evaluation of antidepressant-related behavioral responses in mice lacking the serotonin transporter. Neuropsychopharmacology 2002, 27:914-923.
30. Ishiwata H., Shiga T., Okado N. Selective serotonin reuptake inhibitor treatment of early postnatal mice reverses their prenatal stress-induced brain dysfunction. Neuroscience 2005, 133:893-901.
31. Karpova N.N., Lindholm J., Pruunsild P., Timmusk T., Castrén E. Long-lasting behavioural and molecular alterations induced by early postnatal fluoxetine exposure are restored by chronic fluoxetine treatment in adult mice. Eur Neuropsychopharmacol 2009, 19:97-108.
32. Kiryanova V, Smith VM, Dyck RH, Antle MC (in press) The effects of perinatal fluoxetine treatment on the circadian system of the adult mouse. Psychopharmacology, http://dx.doi.org/10.1007/s00213-012-2861-3.
33. Lee L.-J. Neonatal fluoxetine exposure affects the neuronal structure in the somatosensory cortex and somatosensory-related behaviors in adolescent rats. Neurotox Res 2009, 15:212-223.
34. Lisboa S.F., Oliveira P.E., Costa L.C., Venân E.J., Moreira E.G. Behavioral evaluation of male and female mice pups exposed to fluoxetine during pregnancy and lactation. Pharmacology 2007, 80:49-56.
35. Maciag D., Williams L., Coppinger D., Paul I.A. Neonatal citalopram exposure produces lasting changes in behaviour which are reversed by adult imipramine treatment. Eur J Pharmacol 2006, 532:265-269.
36. Meziane H., Ouagazzal A.-M., Aubert L., Wietrzych M., Krezel W. Estrous cycle effects on behavior of C57BL/6J and BALB/cByJ female mice: implications for phenotyping strategies. Genes Brain Behav 2007, 6:192-200.
37. Miyagawa K., Tsuji M., Fujimori K., Saito Y., Takeda H. Prenatal stress induces anxiety-like behavior together with the disruption of central serotonin neurons in mice. Neurosci Res 2011, 70:111-117.
38. Morrison J.L., Riggs K.W., Rurak D.W. Fluoxetine during pregnancy: impact on fetal development. Reprod Fertil Dev 2005, 17:641-650.
39. Nagano M., Liu M., Inagaki H., Kawada T., Suzuki H. Early intervention with fluoxetine reverses abnormalities in the serotonergic system and behaviour or rats exposed prenatally to dexamethasone. Neuropharmacology 2012, 63:292-300.
40. Noorlander C.W., Ververs F.T., Nikkels P.G., van Echteld C.J., Visser G.H., Smidt M.P. Modulation of serotonin transporter function during fetal development causes dilated heart cardiomyopathy and lifelong behavioral abnormalities. PLoS One 2008, 3:e2782.
41. Nulman I., Rovet J., Stewart D.E., Wolpin J., Pace-Asciak P., Shuhaiber S., Koren G. Child development following exposure to tricyclic antidepressants or fluoxetine throughout fetal life: a prospective, controlled study. Am J Psychiatry 2002, 159:1889-1895.
42. Oberlander T.F., Warburton W., Misri A., Aghajanian J., Hertzman C. Effects of timing and duration of gestational exposure to serotonin reuptake inhibitor antidepressants: population-based study. Br J Psychiatry 2008, 192:338-343.
43. Olivier J.D., Vallès A., van Heesch F., Afrasiab-Middelman A., Roelofs J.J., Jonkers M., Peeters E.J., Korte-Bouws G.A., Dederen J.P., Kiliaan A.J., Martens G.J., Schubert D., Homberg J.R. Fluoxetine administration to pregnant rats increases anxiety-related behaviour in the offspring. Psychopharmacology 2011, 217:419-432.
44. Pawluski J.L., Charlier T.D., Fillet M., Houbart V., Crispin H.T., Steinbusch H.W., Van den Hove D.L. Chronic fluoxetine treatment and maternal adversity differentially alter neurobehavioral outcomes in the rat dam. Behav Brain Res 2011, 228:159-168.
45. Pawluski J.L., Rayen I., Niessen N.A., Kristensen S., van Donkelaar E.L., Balthazart J., Steinbusch H.W., Charlier T.D. Developmental fluoxetine exposure differentially alters central and peripheral measures of the HPA system in adolescent male and female offspring. Neuroscience 2012, 220:131-141.
46. Persico A.M., Mengual E., Moessner R., Hall S.F., Revay R.S., Sora I., Arellano J., DeFelipe J., Girnénez-Amaya J.M., Conciatori M., Marino R., Baldi A., Cabib S., Pascucci T., Uhl G.R., Murphy D.L., Lesch K.P., Keller F. Barrel pattern formation requires serotonin uptake by thalamocortical afferents, and not vesicular monoamine release. J Neurosci 2001, 21:6826-6873.
47. Popa D., Léna C., Alexandre C., Adrien J. Lasting syndrome of depression produced by reduction in serotonin uptake during postnatal development: evidence from sleep, stress, and behavior. J Neurosci 2008, 28:3546-3554.
48. Ralph-Williams R.J., Lehmann-Masten V., Otero-Corchon V., Low M.J., Geyer M.A. Differential effects of direct and indirect dopamine agonists on prepulse inhibition: a study in D1 and D2 receptor knock-out mice. J Neurosci 2002, 22:9604-9611.
49. Rao U., Chen L.-A. Characteristics, correlates, and outcomes of childhood and adolescent depressive disorders. Dialogues Clin Neurosci 2009, 11:45-62.
50. Rayen I., Van den Hove D.L., Prickaerts J., Steinbusch H.W., Pawluski J.L. Fluoxetine during development reverses the effects of prenatal stress on depressive-like behavior and hippocampal neurogenesis in adolescence. PLoS One 2011, 6:e24003.
51. Romjin H.J., Hofman M.A., Gramsbergen A. At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby?. Early Hum Dev 1991, 26:61-67.
52. Saxe M.D., Battaglia F., Wang J.-W., Malleret G., David D.J., Monckton J.E., Garcia A.D., Sofroniew M.V., Kandel E.R., Santarelli L., Hen R., Drew M.R. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA 2006, 103:17501-17506.
53. Schellinck H.M., Cyr D.P., Brown R.E. How many ways can mouse behavioral experiments go wrong? Confounding variables in mouse models of neurodegenerative diseases and how to control them. Adv Study Behav 2010, 41:255-366.
54. Smit-Rigter L.A., Noorlander C.W., von Oerthel L., Chameau P., Smidt M.P., van Hooft J.A. Prenatal fluoxetine exposure induces life-long serotonin 5-HT3 receptor-dependent cortical abnormalities and anxiety-like behaviour. Neuropharmacology 2012, 62:865-875.
55. Upton A.L., Ravary A., Salichon N., Moessner R., Lesch K.-P., Hen R., Seif I., Gaspar P. Lack of 5-HT1B receptor and of serotonin transporter have different effects on the segregation of retinal axons in the later geniculate nucleus compared to the superior colliculus. Neuroscience 2002, 111:587-610.
56. Upton A.L., Salichon N., Lebrand C., Ravary A., Blakely R., Seif I., Gaspar P. Excess of serotonin (5-HT) alters the segregation of ipsilateral and contralateral retinal projections in monoamine oxidase A knock-out mice: possible role of 5-HT uptake in retinal ganglion cells during development. J Neurosci 1999, 19:7007-7024.
57. Van den Hove D.L., Steinbusch H.W., Scheepens A., Van de Berg W.D., Kooiman L.A., Boosten B.J., Prickaerts J., Blanco C.E. Prenatal stress and neonatal rat brain development. Neuroscience 2006, 13:145-155.
58. 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.
59. Wellman C.L., Izquierdo A., Garrett J.E., Martin K.P., Carroll J., Millstein R., Lesch K.-P., Murphy D.L., Holmes A. Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J Neurosci 2007, 27:684-691.
60. Zheng J., Xu D.-F., Li K., Wang H.-T., Shen P.-C., Lin M., Cao X.H., Wang R. Neonatal exposure to fluoxetine and fluvoxamine alters spine density in mouse hippocampal CA1 pyramidal neurons. Int J Clin Exp Pathol 2011, 4:162-168.