Deficits in development of synaptic plasticity in rat dorsal striatum following prenatal and neonatal exposure to low-dose bisphenol A

Neuroscience

Volumn 159, Issue 1, 2009, Pages 161-171

  Zhou, R ^a   Zhang, Z ^a   Zhu, Y ^a   Chen, L ^a,a,b   Sokabe, M ^b,c,d  

^a NANJING MEDICAL UNIVERSITY   (China)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

BPA; D1 receptor; D2 receptor; DL; striatum; synaptic plasticity

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; 8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; DOPAMINE 1 RECEPTOR; DOPAMINE 1 RECEPTOR BLOCKING AGENT; DOPAMINE 2 RECEPTOR; DOPAMINE 2 RECEPTOR BLOCKING AGENT; DOPAMINE 2 RECEPTOR STIMULATING AGENT; METABOTROPIC RECEPTOR; QUINPIROLE; SULPIRIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DEVELOPMENTAL DISORDER; FACILITATION; HYPERACTIVITY; LOCOMOTION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOTOR CONTROL; NERVE CELL PLASTICITY; NERVE STIMULATION; NEUROTOXICITY; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; RAT; SYNAPSE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BENZAZEPINES; CORPUS STRIATUM; DOPAMINE AGONISTS; ELECTRIC STIMULATION; EVOKED POTENTIALS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; MALE; NEURONAL PLASTICITY; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; VALINE;

EID: 60349131091     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.12.028     Document Type: Article

References (76)

1. Ade K.K., and Lovinger D.M. Anandamide regulates postnatal development of long-term synaptic plasticity in the rat dorsolateral striatum. J Neurosci 7 (2007) 2403-2409
2. Andrzejewski M.E., Spencer R.C., and Kelley A.E. Instrumental learning, but not performance, requires dopamine D1-receptor activation in the amygdala. Neuroscience 135 (2005) 335-345
3. Artola A., Hensch T., and Singer W. Calcium-induced long-term depression in the visual cortex of the rat in vitro. J Neurophysiol 76 (1996) 984-994
4. Barnes T.D., Kubota Y., Hu D., Jin D.Z., and Graybiel A.M. Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437 (2005) 1158-1161
5. Belcher S.M., Le H.H., Spurling L., and Wong J.K. Rapid estrogenic regulation of extracellular signal-regulated kinase 1/2 signaling in cerebellar granule cells involves a G protein- and protein kinase A-dependent mechanism and intracellular activation of protein phosphatase 2A. Endocrinology 146 (2005) 5397-5406
6. Bergman H., Feingold A., Nini A., Raz A., Slovin H., Abeles M., and Vaadia E. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci 21 (1998) 32-38
7. Brotons J.A., Olea-Serrano M.F., Villalobos M., Pedraza V., and Olea N. Xenoestrogens released from lacquer coatings in food cans. Environ Health Perspect 103 (1995) 608-612
8. Cai W.Y., Zhu Y., Furuya K., Li Z., Sokabe M., and Chen L. Two different molecular mechanisms underlying progesterone neuroprotection against ischemic brain damage. Neuropharmacology 55 (2008) 127-138
9. Calabresi P., Maj R., Mercuri N.B., and Bernardi G. Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum. Neurosci Lett 142 (1992) 95-99
10. Calabresi P., Maj R., Pisani A., Mercuri N.B., and Bernardi G. Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 12 (1992) 4224-4233
11. Calabresi P., Pisani A., Mercuri N.B., and Bernardi G. The corticostriatal projection: from synaptic plasticity to dysfunctions of the basal ganglia. Trends Neurosci 19 (1996) 19-24
12. Calabresi P., Saiardi A., Pisani A., Baik J.H., Centonze D., Mercuri N.B., Bernardi G., and Borrelli E. Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J Neurosci 15 (1997) 4536-4544
13. Centonze D., Grande C., Saulle E., Martin A.B., Gubellini P., Pavón N., Pisani A., Bernardi G., Moratalla R., and Calabresi P. Distinct roles of D1 and D5 dopamine receptors in motor activity and striatal synaptic plasticity. J Neurosci 23 (2003) 8506-8512
14. Centonze D., Picconi B., Gubellini P., Bernardi G., and Calabresi P. Dopaminergic control of synaptic plasticity in the dorsal striatum. Eur J Neurosci 13 (2001) 1071-1077
15. Centonze D., Usiello A., Costa C., Picconi B., Erbs E., Bernardi G., Borrelli E., and Calabresi P. Chronic haloperidol promotes corticostriatal long-term potentiation by targeting dopamine D2L receptors. J Neurosci 24 (2004) 8214-8222
16. Cepeda C., Buchwald N.A., and Levine M.S. Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. Proc Natl Acad Sci U S A 90 (1993) 9576-9580
17. Cepeda C., and Levine M.S. Dopamine and N-methyl-d-aspartate receptor interactions in the neostriatum. Dev Neurosci 20 (1998) 1-18
18. Charpier S., and Deniau J.M. In vivo activity-dependent plasticity at corticostriatal connections: evidence for physiological long-term potentiation. Proc Natl Acad Sci U S A 94 (1997) 7036-7040
19. Chen L., and Sokabe M. Perinatal BPA exposure influences synaptic functions in the dorsal striatum of offspring. J Physiol Sci 58 Suppl (2007) S84
20. Choi S., and Lovinger D.M. Decreased frequency but not amplitude of quantal synaptic responses associated with expression of corticostriatal long-term depression. J Neurosci 17 (1997) 8613-8620
21. Choi S., and Lovinger D.M. Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc Natl Acad Sci U S A 94 (1997) 2665-2670
22. Colwell C.S., Cepeda C., Crawford C., and Levine M.S. Postnatal development of glutamate receptor-mediated responses in the neostriatum. Dev Neurosci 20 (1998) 154-163
23. Costa R.M. Plastic corticostriatal circuits for action learning: what's dopamine got to do with it?. Ann N Y Acad Sci 1104 (2007) 172-191
24. Costa R.M., Cohen D., and Nicolelis M.A. Differential corticostriatal plasticity during fast and slow motor skill learning in mice. Curr Biol 14 (2004) 1124-1134
25. Dos Santos Villar F., and Walsh J.P. Modulation of long-term synaptic plasticity at excitatory striatal synapses. Neuroscience 90 (1999) 1031-1041
26. Emilien G., Maloteaux J.M., Geurts M., Hoogenberg K., and Cragg S. Dopamine receptors-physiological understanding to therapeutic intervention potential. Pharmacol Ther 84 (1999) 133-156
27. Faroon O.M., Keith S., Jones D., and De Rosa C. Carcinogenic effects of polychlorinated biphenyls. Toxicol Ind Health 17 (2001) 41-62
28. Featherstone R.E., and McDonald R.J. Lesions of the dorsolateral striatum impair the acquisition of a simplified stimulus-response dependent conditional discrimination task. Neuroscience 136 (2005) 387-395
29. Flores-Hernández J., Galarraga E., and Bargas J. Dopamine selects glutamatergic inputs to neostriatal neurons. Synapse 25 (1997) 185-195
30. Fonnum F., Mariussen E., and Reistad T. Molecular mechanisms involved in the toxic effects of polychlorinated biphenyls (PCBs) and brominated flame retardants (BFRs). J Toxicol Environ Health A 69 (2006) 21-35
31. Gerdeman G.L., Ronesi J., and Lovinger D.M. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5 (2002) 446-451
32. Gingrich J.A., and Caron M.G. Recent advances in the molecular biology of dopamine receptors. Annu Rev Neurosci 16 (1993) 299-321
33. Graybiel A.M., Aosaki T., Flaherty A.W., and Kimura M. The basal ganglia and adaptive motor control. Science 265 (1994) 1826-1831
34. Hruska R.E., and Nowak M.W. Estrogen treatment increases the density of D1 dopamine receptors in the rat striatum. Brain Res 442 (1988) 349-350
35. Ikemoto S., and Wise R.A. Mapping of chemical trigger zones for reward. Neuropharmacology 47 Suppl 1 (2004) 190-201
36. Ikezuki Y., Tsutsumi O., Takai Y., Kamei Y., and Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod 17 (2002) 2839-2841
37. Ishido M., Masuo Y., Kunimoto M., Oka S., and Morita M. Bisphenol A causes hyperactivity in the rat concomitantly with impairment of tyrosine hydroxylase immunoreactivity. J Neurosci Res 76 (2004) 423-433
38. Ito M. Long term depression. Annu Rev Neurosci 12 (1989) 85-102
39. Jacobson J.L., and Jacobson S.W. Dose-response in perinatal exposure to polychlorinated biphenyls (PCBs): the Michigan and North Carolina cohort studies. Toxicol Ind Health 12 (1996) 435-445
40. Kerr J.N., and Wickens J.R. Dopamine d-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro. J Neurophysiol 85 (2001) 117-124
41. Knowlton B.J., Mangels J.A., and Squire L.R. A neostriatal habit learning system in humans. Science 273 (1996) 1399-1402
42. Kreitzer A.C., and Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445 (2007) 643-647
43. Krishnan A.V., Stathis P., Permuth S.F., Tokes L., and Feldman D. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132 (1993) 2279-2286
44. Lammers C.H., D'souza U., Qin Z.H., Lee S.H., Yajima S., and Mouradian M.M. Regulation of striatal dopamine receptors by estrogen. Synapse 34 (1999) 222-227
45. Laws S.C., Carey S.A., Ferrell J.M., Bodman G.J., and Cooper R.L. Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicol Sci 54 (2000) 154-167
46. Linden D.J., and Connor J.A. Long-term synaptic depression. Annu Rev Neurosci 18 (1995) 319-357
47. Levine M.S., Li Z., Cepeda C., Cromwell H.C., and Altemus K.L. Neuromodulatory actions of dopamine on synaptically-evoked neostriatal responses in slices. Synapse 24 (1996) 65-78
48. Lovinger D.M., Tyler E.C., and Merritt A. Short- and long-term synaptic depression in rat neostriatum. J Neurophysiol 70 (1993) 1937-1949
49. Mariussen E., and Fonnum F. Neurochemical targets and behavioral effects of organohalogen compounds: an update. Crit Rev Toxicol 36 (2006) 253-289
50. Masuo Y., Ishido M., Morita M., and Oka S. Effects of neonatal treatment with 6-hydroxydopamine and endocrine disrupters on motor activity and gene expression in rats. Neural Plast 11 (2004) 59-76
51. McKee B.L., and Meshul C.K. Time-dependent changes in extracellular glutamate in the rat dorsolateral striatum following a single cocaine injection. Neuroscience 133 (2005) 605-613
52. Missale C., Nash S.R., Robinson S.W., Jaber M., and Caron M.C. Dopamine receptors: from structure to function. Physiol Rev 78 (1998) 189-225
53. Miyagawa K., Narita M., Narita M., Akama H., and Suzuki T. Memory impairment associated with a dysfunction of the hippocampal cholinergic system induced by prenatal and neonatal exposures to bisphenol-A. Neurosci Lett 418 (2007) 236-241
54. Miyatake M., Miyagawa K., Mizuo K., Narita M., and Suzuki T. Dynamic changes in dopaminergic neurotransmission induced by a low concentration of bisphenol-A in neurones and astrocytes. J Neuroendocrinol 18 (2006) 434-444
55. Mizuo K., Narita M., Yoshida T., Narita M., and Suzuki T. Functional changes in dopamine D3 receptors by prenatal and neonatal exposure to an endocrine disrupter bisphenol-A in mice. Addict Biol 9 (2004) 19-25
56. Nakamura K., Itoh K., Yaoi T., Fujiwara Y., Sugimoto T., and Fushiki S. Murine neocortical histogenesis is perturbed by prenatal exposure to low doses of bisphenol A. J Neurosci Res 84 (2006) 1197-1205
57. Nagel S.C., vom Saal F.S., Thayer K.A., Dhar M.G., Boechler M., and Welshons W.V. Relative binding affinity-serum modified access (RBASMA) assay predicts the relative in vivo bioactivity of the xenoestrogens bisphenol A and octylphenol. Environ Health Perspect 105 (1997) 70-76
58. Narita M., Miyagawa K., Mizuo K., Yoshida T., and Suzuki T. Prenatal and neonatal exposure to low-dose of bisphenol-A enhance the morphine-induced hyperlocomotion and rewarding effect. Neurosci Lett 402 (2006) 249-252
59. Partridge J.G., Apparsundaram S., Gerhardt G.A., Ronesi J., and Lovinger D.M. Nicotinic acetylcholine receptors interact with dopamine in induction of striatal long-term depression. J Neurosci 22 (2002) 2541-2549
60. Partridge J.G., Tang K.C., and Lovinger D.M. Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J Neurophysiol 84 (2000) 1422-1429
61. Petersen D.N., Tkalcevic G.T., Koza-Taylor P.H., Turi T.G., and Brown T.A. Identification of estrogen receptor β2, a functional variant of estrogen receptor β expressed in normal rat tissues. Endocrinology 139 (1998) 1082-1092
62. Reynolds J.N., and Wickens J.R. Substantia nigra dopamine regulates synaptic plasticity and membrane potential fluctuations in the rat neostriatum in vivo. Neuroscience 99 (2000) 199-203
63. Ronesi J., and Lovinger D.M. Induction of striatal long-term synaptic depression by moderate frequency activation of cortical afferents in rat. J Physiol 562 (2005) 245-256
64. Schönfelder G., Wittfoht W., Hopp H., Talsness C.E., Paul M., and Chahoud I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 10 (2002) A703-A707
65. Self D.W. Regulation of drug-taking and -seeking behaviors by neuroadaptations in the mesolimbic dopamine system. Neuropharmacology 47 Suppl 1 (2004) 242-255
66. Surmeier D.J., Song W.-J., and Zhen Y. Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci 15 (1996) 6579-6591
67. Suzuki T., Mizuo K., Nakazawa H., Funae Y., Fushiki S., Fukushima S., Shirai T., and Narita M. Prenatal and neonatal exposure to bisphenol-A enhances the central dopamine D1 receptor-mediated action in mice: enhancement of the methamphetamine-induced abuse state. Neuroscience 117 (2003) 639-644
68. Tang K.C., and Lovinger D.M. Role of pertussis toxin-sensitive G proteins in synaptic transmission and plasticity at corticostriatal synapses. J Neurophysiol 83 (2000) 60-69
69. Tang K., Low M.J., Grandy D.K., and Lovinger D.M. Dopamine-dependent synaptic plasticity in striatum during in vivo development. Proc Natl Acad Sci U S A 98 (2001) 1255-1260
70. Tepper J.M., Sharpe N.A., Koós T.Z., and Trent F. Postnatal development of the rat neostriatum: electrophysiological, light- and electron-microscopic studies. Dev Neurosci 20 (1998) 125-145
71. Vallar L., and Meldolesi J. Mechanisms of signal transduction at the dopamine D2 receptors. Trends Pharmacol Sci 10 (1989) 74-77
72. Vallone D., Picetti R., and Borrelli E. Structure and function of dopamine receptors. Neurosci Biobehav Rev 24 (2000) 125-132
73. vom Saal F.S., Cooke P.S., Buchanan D.L., Palanza P., Thayer K.A., Nagel S.C., Parmigiani S., and Welshons W.V. A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol Ind Health 14 (1998) 239-260
74. Walsh J.P. Depression of excitatory synaptic input in rat striatal neurons. Brain Res 608 (1993) 123-128
75. Wickens J.R., Begg A.J., and Arbuthnott G.W. Dopamine reverses the depression of rat corticostriatal synapses which normally follows high-frequency stimulation of cortex in vitro. Neuroscience 70 (1996) 1-5
76. Zsarnovszky A., Le H.H., Wang H.S., and Belcher S.M. Ontogeny of rapid estrogen-mediated extracellular signal-regulated kinase signaling in the rat cerebellar cortex: potent nongenomic agonist and endocrine disrupting activity of the xenoestrogen bisphenol A. Endocrinology 146 (2005) 5388-5396