Lasting neurobehavioral abnormalities in rats after neonatal activation of serotonin 1A and 1B receptors: Possible mechanisms for serotonin dysfunction in autistic spectrum disorders

Psychopharmacology

Volumn 231, Issue 6, 2014, Pages 1191-1200

  Khatri, Nidhi ^a   Simpson, Kimberly L ^a,b   Lin, Rick C S ^a,b   Paul, Ian A ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

8 OH DPAT; Antidepressant; Autism; CGS 12066B; Citalopram; Development; GR 127935; Neonatal exposure; Selective serotonin reuptake inhibitor; Sensory systems; Serotonin; Social behavior; WAY 100635

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 4 (4 METHYL 1 PIPERAZINYL) 7 TRIFLUOROMETHYLPYRROLO[1,2 A]QUINOXALINE; CITALOPRAM; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; N [4 METHOXY 3 (4 METHYL 1 PIPERAZINYL)PHENYL] 2' METHYL 4' (5 METHYL 1,2,4 OXADIAZOL 3 YL)[1,1' BIPHENYL] 4 CARBOXAMIDE; SEROTONIN 1A RECEPTOR; SEROTONIN 1B RECEPTOR; SEROTONIN UPTAKE INHIBITOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; BEHAVIOR DISORDER; BRAIN DEVELOPMENT; CONTROLLED STUDY; FEMALE; LOCOMOTION; MALE; NEOPHOBIA; NONHUMAN; PRIORITY JOURNAL; PUPPY; RAT; SENSORY DYSFUNCTION; SEROTONIN SYNDROME; SOCIAL DISABILITY; SOCIAL INTERACTION; STEREOTYPY;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ANIMALS; ANIMALS, NEWBORN; BRAIN; CITALOPRAM; EXPLORATORY BEHAVIOR; FEMALE; FREEZING REACTION, CATALEPTIC; LOCOMOTION; MALE; OXADIAZOLES; PIPERAZINES; PYRIDINES; QUINOXALINES; RATS; RATS, LONG-EVANS; RECEPTOR, SEROTONIN, 5-HT1A; RECEPTOR, SEROTONIN, 5-HT1B; SEROTONIN ANTAGONISTS; SEROTONIN RECEPTOR AGONISTS; SEROTONIN UPTAKE INHIBITORS; SOCIAL BEHAVIOR;

EID: 84896717061     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-013-3242-2     Document Type: Article

References (66)

1. Aghajanian GK, Bloom FE (1967) The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study. Brain Res 6(4):716-727
2. Alzghoul L, Bortolato M, Delis F, Thanos PK, Darling RD, Godar SC, Zhang J, Grant S, Wang GJ, Simpson KL, Chen K, Volkow ND, Lin RC, Shih JC (2012) Altered cerebellar organization and function in monoamine oxidase A hypomorphic mice. Neuropharmacology 63(7):1208-17
3. Anderson GM, Horne WC, Chatterjee D, Cohen DJ (1990) The hyperserotonemia of autism. Ann. N.Y. Acad Sci 600:331-340
4. Azmitia EC (2001) Modern view on an ancient chemical: serotonin effects on proliferation, maturation, and apoptosis. Brain Res Bull 56:414-424
5. Bennett-Clarke CA, Leslie MJ, Chiaia NL, Rhoades RW (1993) Serotonin 1B receptors in the developing somatosensory and visual cortices are located on thalamocortical axons. Proc Natl Acad Sci U S A 90:153-157 (Pubitemid 23010268)
6. Bjerkenstedt L, Flyckt L, Overo KF, Lingjaerde O (1985) Relationship between clinical effects, serum drug concentration and serotonin uptake inhibition in depressed patients treated with citalopram. A double-blind comparison of three dose levels. Eur J Clin Pharmacol 28:553-557 (Pubitemid 15030781)
7. Bortolato M, Godar SC, Alzghoul L, Zhang J, Darling RD, Simpson KL, Bini V, Chen K, Wellman CL, Lin RC, Shih JC (2013) Monoamine oxidase A and A/B knockout mice display autistic-like features. Int J Neupsychopharmacology 16(4):869-88
8. Boschert U, Amara DA, Segu L, Hen R (1994) The mouse 5-hydroxytryptamine 1B receptor is localized predominantly on axon terminals. Neuroscience 58:167-182
9. Chugani HT (1998) A critical period of brain development: studies of cerebral glucose utilization with PET. Prev Med 27(2):184-188
10. Cohen LS, Nonacs R, Viguera AC, Reminick A (2004) Diagnosis and treatment of depression during pregnancy. CNS Spectr 9:209-216 (Pubitemid 44137114)
11. Cook EH, Arora RC, Anderson GM, Berry-Kravis EM, Yau S, Yeoh HC, Sklena PJ, Charak DA, Leventhal BL (1993) Platelet serotonin studies in familial hyperserotonemia of autism. Life Sci 52:2005-2015
12. Cook EH (1996) Brief report: pathophysiology of autism: neurochemistry. J Autism Dev Disord 26:221-215
13. Croen LA, Grether JK, Yoshida CK, Odouli R, Hendrick V (2011) Antidepressant use during pregnancy and childhood autism spectrum disorders. Arch Gen Psychiatry 68:1104-1112
14. Egaas B, Courchesne E, Saitoh O (1995) Reduced size of corpus callosum in autism. Arch Neurol 52:794-801
15. 1B receptors in knock-out mice lacking the 5-HT transporter. Eur J Neurosci 12:2299-2310
16. Fletcher PJ, Azampanah A, Korth KM (2002) Activation of 5-HT(1B) receptors in the nucleus accumbens reduces self-administration of amphetamine on a progressive ratio schedule. Pharmacol Biochem Behav 71:717-725 (Pubitemid 34219222)
17. Frambes NA, Kirstein CL, Moody CA, Spear LP (1990) 5-HT1A, 5-HT1B and 5-HT2 receptor agonists induce differential behavioral responses in preweanling rat pups. Eur J Pharmacol 182:9-17 (Pubitemid 20211578)
18. Frances H, Monier C (1991) Tolerance to the behavioural effect of serotonergic (5-HT1B) agonists in the isolation-induced social behavioural deficit test. Neuropharmacology 30:623-627
19. Fuller RW (1994) Minireview: uptake inhibitors increase extracellular serotonin concentration measured by brain microdialysis. Life Sci 55:163-167
20. Gendle MH, Strawderman MS, Mactutus CF, Booze RM, Levitsky DA, Strupp BJ (2003) Impaired sustained attention and altered reactivity to errors in an animalmodel of prenatal cocaine exposure. Dev Brain Res 147(12):85-96 (Pubitemid 38114700)
21. Gonzalez MI, Albonetti E, Siddiqui A, Farabollini F, Wilson CA (1996) Neonatal organizational effects of the 5-HT2 and 5-HT1A subsystems on adult behavior in the rat. Pharmacol Biochem Behav 54:195-203
22. Hansen HH, Sanchez C, Meier E (1997) 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 283:1333-1341 (Pubitemid 28016508)
23. Hansson SR, Mezey E, Hoffman BJ (1998) Serotonin transporter messenger RNA in the developing rat brain: early expression in serotonergic neurons and transient expression in non-serotonergic neurons. Neuroscience 83:1185-1201 (Pubitemid 28114210)
24. Harris SS, Maciag D, Simpson KL, Paul IA (2012) Dose dependent effects of neonatal SSRI exposure on adult behavior in the rat. Brain Res 1429:52-60
25. Hendrick V, Stowe ZN, Altshuler LL, Hwang S, Lee E, Haynes D (2003) Placental passage of antidepressant medications. Am J Psychiatry 160:993-996 (Pubitemid 41079587)
26. Hilakivi LA, Sinclair JD, Hilakivi IT (1984) Effects of neonatal treatment with clomipramine on adult ethanol related behavior in the rat. Brain Res 317:129-132 (Pubitemid 14097749)
27. 1A receptor mRNA and protein in rat embryonic brain stem cultures. Brain Res Dev Brain Res 79:195-202
28. Hjorth S, Westlin D, Bengtsson HJ (1997) WAY100635-induced augmentation of the 5-HT-elevating action of citalopram: relative importance of the dose of the 5-HT1A (auto) receptor blocker versus that of the 5-HT reuptake inhibitor. Neuropharmacology 36:461-465 (Pubitemid 27272091)
29. Hostetter A, Ritchie JC, Stowe ZN (2000) Amniotic fluid and umbilical cord blood concentrations of antidepressants in three women. Biol Psychiatry 48:1032-1034
30. Hoyer D, Hannon JP, Martin GR (2002) Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 71:533-54 (Pubitemid 34219205)
31. 1A receptors in the effects of acute and chronic fluoxetine on extracellular serotonin in the frontal cortex. Pharmacol Biochem Behav 54:143-147
32. Jacobson M (1991) Formation of dendrites and development of synaptic connections. Developmental neurobiology. Plenum Press, New York, pp 223-284
33. Kinney HC, Broadbelt KG, Haynes RL, Rognum IJ, Paterson DS (2011) The serotonergic anatomy of the developing human medulla oblongata: implications for pediatric disorders of homeostasis. J Chem Anat 41:182-189
34. Kiyasova V, Gaspar P (2011) Development of raphe serotonin neurons from specification to guidance. Eur J Neurosci 34(1553-1562):2011
35. Kugelberg FC, Apelqvist G, Carlsson B, Ahlner J, Bengtsson F (2001) In vivo steady-state pharmacokinetic outcome following clinical and toxic doses of racemic citalopramto rats. Br J Pharmacol 132:1683-1690 (Pubitemid 32401129)
36. Laine K, Heikkinen T, Ekblad U, Kero P (2003) Effects of exposure to selective serotonin reuptake inhibitors during pregnancy on serotonergic symptoms in newborns and cord blood monoamine and prolactin concentrations. Arch Gen Psychiatry 60:720-726 (Pubitemid 36818634)
37. Laurent A, Goaillard JM, Cases O, Lebrand C, Gaspar P, Ropert N (2002) Activity-dependent presynaptic effect of serotonin 1B receptors on the somatosensory thalamocortical transmission in neonatal mice. J Neurosci 22:886-900 (Pubitemid 34141769)
38. Lebrand C, Cases O, Adelbrecht C, Doye A, Alvarez C, El Mestikawy S, Seif I, Gaspar P (1996) Transient uptake and storage of serotonin in developing thalamic neurons. Neuron 17:823-835 (Pubitemid 26424011)
39. Lebrand C, Cases O, Wehrle R, Blakely RD, Edwards RH, Gaspar P (1998) Transient developmental expression of monoamine transporters in the rodent forebrain. J Comp Neurol 401:506-524 (Pubitemid 28509882)
40. Lu Y, Simpson KL, Weaver KJ, Lin RC (2012) Differential distribution patterns from medial prefrontal cortex and dorsal raphe to the locus coeruleus in rats. Anat Rec 295(7):1192-201
41. Maciag D, Simpson KL, Coppinger D, Lu Y, Wang Y, Lin RC, Paul IA (2006a) Neonatal antidepressant exposure has lasting effects on behavior and serotonin circuitry. Neuropsychopharmacology 31:47-57 (Pubitemid 43250940)
42. Maciag D, Williams L, Coppinger D, Paul IA (2006b) Neonatal citalopram exposure produces lasting changes in behavior which are reversed by adult imipramine treatment. Eur J Pharmacol 532:265-269
43. Malagié I, Trillat AC, Jacquot C, Gardier AM (1995) Effects of acute fluoxetine on extracellular serotonin levels in the raphe: an in vivo microdialysis study. Eur J Pharmacol 286:213-217
44. Mathews TA, Fedele DE, Coppelli FM, Avila AM, Murphy DL, Andrews AM (2004) Gene dose-dependent alterations in extraneuronal serotonin but not dopamine in mice with reduced serotonin transporter expression. J Neurosci Methods 140:169-181 (Pubitemid 39625865)
45. McLean JH, Shipley MT (1987a) Serotonergic afferents to the rat olfactory bulb: I. Origins and laminar specificity of serotonergic inputs in the adult rat. J Neurosci 7:3016-3028
46. McLean JH, Shipley MT (1987b) Serotonergic afferents to the rat olfactory bulb: II. Changes in fiber distribution during development. J Neurosci 7:3029-3039
47. McNamara IM, Borella AW, Bialowas LA, Whitaker-Azmitia PM (2008) Further studies in the developmental hyperserotonemia model (DHS) of autism: social, behavioral and peptide changes. Brain Res 1189:203-214
48. Mirmiran M, van de Poll NE, Corner MA, van Oyen HG, Bour HL (1981) Suppression of active sleep by chronic treatment with chlorimipramine during early postnatal development: effects upon adult sleep and behavior in the rat. Brain Res 204:129-146 (Pubitemid 11247494)
49. Neill D, Vogel G, Hagler M, Kors D, Hennessey A (1990) Diminished sexual activity in a new animal model of endogenous depression. Neurosci Biobehav Rev 14:73-76 (Pubitemid 20115615)
50. Nordeng H, Lindemann R, Perminov KV, Reikvam A (2001) Neonatal withdrawal syndrome after in utero exposure to selective serotonin reuptake inhibitors. Acta Paediatr 90:288-291 (Pubitemid 32299548)
51. Overstreet DH, Moy SS, Lubin DA, Lieberman JA, Johns JM (2000) Enduring effects of prenatal cocaine administration on emotional behavior in rats. Physiol Behav 70(12):149-156
52. Panksepp J, Siviy S, Normansell L (1984) The psychobiology of play: theoretical and methodological perspectives. Neurosci Biobehav Rev 8:465-492 (Pubitemid 15155159)
53. Pellis MS, Pellis VC (1998) Play fighting of rats in comparative perspective: a scheme for neurobehavioral analyses. Neurosci Biobehav Rev 23:87-101
54. Pineyro G, Blier P (1999) Autoregulation of serotonin neurons: role in antidepressant drug action. Pharmacol Rev 51:533-591 (Pubitemid 29420214)
55. Rodriguez-Porcel F, Green DL, Khatri N, Swilley S, Lin RCS, Paul IA (2011) Neonatal exposure of rats to antidepressants affects behavioral reactions to novelty and social interactions in a manner analogous to autistic spectrum disorders. Anat Rec 294:1726-1735
56. Salichon N, Gaspar P, Upton AL, Picaud S, Hanoun N, Hamon M et al (2001) Excessive activation of serotonin (5-HT) 1B receptors disrupted the formation of sensory maps in monoamine oxidase and 5-HT transporter knock-out mice. J Neurosci 21:884-896 (Pubitemid 32163130)
57. Sanz EJ, De-las-Cuevas C, Kiuru A, Bate A, Edwards R (2005) Selective serotonin reuptake inhibitors in pregnant women and neonatal withdrawal syndrome: a database analysis. Lancet 365:482-487 (Pubitemid 40215730)
58. Simpson KL, Weaver KJ, de Villers-Sidani E, Lu JY, Cai Z, Pang Y, Rodriguez-Porcel F, Paul IA, Merzenich M, Lin RC (2011) Perinatal antidepressant exposure alters cortical network function in rodents. Proc Natl Acad Sci U S A 108:18465-18470
59. Tohyama Y, Yamane F, Fikre Merid M, Blier P, Diksic M (2002) Effects of serotine receptors agonists, TFMPP and CGS12066B, on regional serotonin synthesis in the rat brain: an autoradiographic study. J Neurochem 80:788-98 (Pubitemid 34809231)
60. Veenstra-VanderWeele J, Kim SJ, Lord C, Courchesne R, Akshoomoff N, Leventhal BL, Courchesne E, Cook EH (2002) Transmission disequilibrium studies of the serotonin 5-HT2A receptor gene (HTR2A) in autism. Am J Med Genet 114:277-283 (Pubitemid 34258851)
61. Vogel G, Hartley P, Neill D, Hagler M, Kors D (1988) Animal depression model by neonatal clomipramine: reduction of shock induced aggression. Pharmacol Biochem Behav 31:103-106 (Pubitemid 19271189)
62. Weaver KJ, Paul IA, Lin RCS, Simpson KL (2010) Neonatal exposure to citalopram selectively alters the expression of the serotonin transporter in the hippocampus: dose-dependent effects. Anat Record 293:1920-1932
63. Whitaker-Azmitia PM, Zhang X, Clarke C (1994) Effects of gestational exposure to monoamine oxidase inhibitors in rats: preliminary behavioral and neurochemical studies. Neuropsychopharmacology 11(2):125-132 (Pubitemid 24334068)
64. Whitaker-Azmitia PM (2005) Behavioral and cellular consequences of increasing serotonergic activity during brain development: a role in autism? Int J Dev Neurosci 23:75-83
65. Wisner KL, Zarin DA, Holmboe ES, Appelbaum PS, Gelenberg AJ, Leonard HL et al (2000) Risk-benefit decision making for treatment of depression during pregnancy. Am J Psychiatry 157:1933-1940
66. Zhou FC, Sari Y, Zhang JK (2000) Expression of serotonin transporter protein in developing rat brain. Brain Res Dev Brain Res 119:33-45 (Pubitemid 30058380)