Integration of neural networks activated by amphetamine in females with different estrogen levels: A functional imaging study in awake rats

Psychoneuroendocrinology

Volumn 56, Issue , 2015, Pages 200-212

  Madularu, Dan ^a   Yee, Jason R ^b   Kenkel, William M ^b   Moore, Kelsey A ^b   Kulkarni, Praveen ^b   Shams, Waqqas M ^a   Ferris, Craig F ^b   Brake, Wayne G ^a  

^a Center for Studies in Behavioural Neurobiology ^*  (Canada)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Amphetamine sensitization; BOLD; Estradiol; FMRI; Ovariectomy; Schizophrenia

Indexed keywords

AMPHETAMINE; ESTRADIOL; ESTROGEN; CENTRAL STIMULANT AGENT; OXYGEN;

ANIMAL EXPERIMENT; ARTICLE; BOLD SIGNAL; BRAIN REGION; CONTROLLED STUDY; ESTROGEN THERAPY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; NERVE CELL NETWORK; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; WAKEFULNESS; ANIMAL; BLOOD; BRAIN MAPPING; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; OVARIECTOMY; SPRAGUE DAWLEY RAT;

AMPHETAMINE; ANIMALS; BRAIN MAPPING; CENTRAL NERVOUS SYSTEM STIMULANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; FEMALE; MAGNETIC RESONANCE IMAGING; NERVE NET; OVARIECTOMY; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84927754252     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2015.02.022     Document Type: Article

References (69)

1. Akhondzadeh S., Nejatisafa A.A., Amini H., Mohammadi M.R., Larijani B., Kashani L., Raisi F., Kamalipour A. Adjunctive estrogen treatment in women with chronic schizophrenia: a double-blind, randomized, and placebo-controlled trial. Prog. Neuropsychopharmacol. Biol. Psychiatry 2003, 27:1007-1012.
2. Almey A., Cannell E., Bertram K., Filardo E., Milner T.A., Brake W.G. Medial prefrontal cortical estradiol rapidly alters memory system bias in female rats: ultrastructural analysis reveals membrane-associated estrogen receptors as potential mediators. Endocrinology 2014, 155:4422-4432.
3. Almey A., Filardo E.J., Milner T.A., Brake W.G. Estrogen receptors are found in glia and at extranuclear neuronal sites in the dorsal striatum of female rats: evidence for cholinergic but not dopaminergic colocalization. Endocrinology 2012, 153:5373-5383.
4. Almey A., Hafez N.M., Hantson A., Brake W.G. Deficits in latent inhibition induced by estradiol replacement are ameliorated by haloperidol treatment. Front. Behav. Neurosci. 2013, 7:136.
5. Becerra L., Chang P.C., Bishop J., Borsook D. CNS activation maps in awake rats exposed to thermal stimuli to the dorsum of the hindpaw. Neuroimage 2011, 54:1355-1366.
6. Becker J.B. Estrogen rapidly potentiates amphetamine-induced striatal dopamine release and rotational behavior during microdialysis. Neurosci. Lett. 1990, 118:169-171.
7. Becker J.B., Cha J.H. Estrous cycle-dependent variation in amphetamine-induced behaviors and striatal dopamine release assessed with microdialysis. Behav. Brain Res. 1989, 35:117-125.
8. Brailoiu E., Dun S.L., Brailoiu G.C., Mizuo K., Sklar L.A., Oprea T.I., Prossnitz E.R., Dun N.J. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 2007, 193:311-321.
9. Breier A., Buchanan R.W., Elkashef A., Munson R.C., Kirkpatrick B., Gellad F. Brain morphology and schizophrenia. A magnetic resonance imaging study of limbic, prefrontal cortex, and caudate structures. Arch. Gen. Psychiatry 1992, 49:921-926.
10. Brevard M.E., Duong T.Q., King J.A., Ferris C.F. Changes in MRI signal intensity during hypercapnic challenge under conscious and anesthetized conditions. Magn. Reson. Imaging 2003, 21:995-1001.
11. Castle D.J., Murray R.M. The epidemiology of late-onset schizophrenia. Schizophr. Bull. 1993, 19:691-700.
12. Dadda M., Domenichini A., Piffer L., Argenton F., Bisazza A. Early differences in epithalamic left-right asymmetry influence lateralization and personality of adult zebrafish. Behav. Brain Res. 2010, 206:208-215.
13. Featherstone R.E., Kapur S., Fletcher P.J. The amphetamine-induced sensitized state as a model of schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 2007, 31:1556-1571.
14. Febo M., Ferris C.F., Segarra A.C. Estrogen influences cocaine-induced blood oxygen level-dependent signal changes in female rats. J. Neurosci. 2005, 25:1132-1136.
15. Ferris C.F., Kulkarni P., Toddes S., Yee J., Kenkel W., Nedelman M. Studies on the Q175 knock-in Model of Huntington's disease using functional imaging in awake mice: evidence of olfactory dysfunction. Front. Neurol. 2014, 5:94.
16. Forgie M.L., Stewart J. Effect of prepubertal ovariectomy on amphetamine-induced locomotor activity in adult female rats. Horm. Behav. 1994, 28:241-260.
17. Geffen L.B., Jessell T.M., Cuello A.C., Iversen L.L. Release of dopamine from dendrites in rat substantia nigra. Nature 1976, 260:258-260.
18. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002, 15:870-878.
19. Gong W., Neill D., Justice J.B. Conditioned place preference and locomotor activation produced by injection of psychostimulants into ventral pallidum. Brain Res. 1996, 707:64-74.
20. Grace A.A. Gating of information flow within the limbic system and the pathophysiology of schizophrenia. Brain Res. Brain Res. Rev. 2000, 31:330-341.
21. Graybiel A.M., Moratalla R., Robertson H.A. Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:6912-6916.
22. Gurevich E.V., Bordelon Y., Shapiro R.M., Arnold S.E., Gur R.E., Joyce J.N. Mesolimbic dopamine D3 receptors and use of antipsychotics in patients with schizophrenia. A postmortem study. Arch. Gen. Psychiatry 1997, 54:225-232.
23. Hafner H. Gender differences in schizophrenia. Psychoneuroendocrinology 2003, 28(Suppl. 2):17-54.
24. Hamamura T., Ichimaru Y. Amphetamine sensitization augments amphetamine-induced Fos expression in the lateral habenula. Brain Res. 1997, 767:140-143.
25. Haun F., Eckenrode T.C., Murray M. Habenula and thalamus cell transplants restore normal sleep behaviors disrupted by denervation of the interpeduncular nucleus. J. Neurosci. 1992, 12:3282-3290.
26. Heerey E.A., Bell-Warren K.R., Gold J.M. Decision-making impairments in the context of intact reward sensitivity in schizophrenia. Biol. Psychiatry 2008, 64:62-69.
27. Hikosaka O. The habenula: from stress evasion to value-based decision-making. Nat. Rev. Neurosci. 2010, 11:503-513.
28. Hu M., Becker J.B. Effects of sex and estrogen on behavioral sensitization to cocaine in rats. J. Neurosci. 2003, 23:693-699.
29. Hussain D., Shams W.M., Brake W.G. Estrogen and memory system bias in females across the lifespan. Transl. Neurosci. 2014, 5:35-50.
30. King J.A., Garelick T.S., Brevard M.E., Chen W., Messenger T.L., Duong T.Q., Ferris C.F. Procedure for minimizing stress for fMRI studies in conscious rats. J. Neurosci. Methods 2005, 148:154-160.
31. Knable M.B., Weinberger D.R. Dopamine, the prefrontal cortex and schizophrenia. J. Psychopharmacol. 1997, 11:123-131.
32. Kohler C.G., Moberg P.J., Gur R.E., O'Connor M.J., Sperling M.R., Doty R.L. Olfactory dysfunction in schizophrenia and temporal lobe epilepsy. NNBN 2001, 14:83-88.
33. Koob G.F., Stinus L., Le Moal M. Hyperactivity and hypoactivity produced by lesions to the mesolimbic dopamine system. Behav. Brain Res. 1981, 3:341-359.
34. Kopala L.C., Clark C., Hurwitz T. Olfactory deficits in neuroleptic naive patients with schizophrenia. Schizophr. Res. 1993, 8:245-250.
35. Kulkarni J., Riedel A., de Castella A.R., Fitzgerald P.B., Rolfe T.J., Taffe J., Burger H. Estrogen - a potential treatment for schizophrenia. Schizophr. Res. 2001, 48:137-144.
36. Lecourtier L., Deschaux O., Arnaud C., Chessel A., Kelly P.H., Garcia R. Habenula lesions alter synaptic plasticity within the fimbria-accumbens pathway in the rat. Neuroscience 2006, 141:1025-1032.
37. Lecourtier L., Kelly P.H. Bilateral lesions of the habenula induce attentional disturbances in rats. Neuropsychopharmacology 2005, 30:484-496.
38. Lin J.S., Hou Y., Jouvet M. Potential brain neuronal targets for amphetamine-, methylphenidate-, and modafinil-induced wakefulness, evidenced by c-fos immunocytochemistry in the cat. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:14128-14133.
39. Lindheim S.R., Legro R.S., Bernstein L., Stanczyk F.Z., Vijod M.A., Presser S.C., Lobo R.A. Behavioral stress responses in premenopausal and postmenopausal women and the effects of estrogen. Am. J. Obstet. Gynecol. 1992, 167:1831-1836.
40. Madularu D., Shams W.M., Brake W.G. Estrogen potentiates the behavioral and nucleus accumbens dopamine response to continuous haloperidol treatment in female rats. Eur. J. Neurosci. 2014, 39:257-265.
41. Matsumoto M., Hikosaka O. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 2007, 447:1111-1115.
42. Matsumoto M., Hikosaka O. Representation of negative motivational value in the primate lateral habenula. Nat. Neurosci. 2009, 12:77-84.
43. McEwen B.S., Alves S.E. Estrogen actions in the central nervous system. Endocr. Rev. 1999, 20:279-307.
44. Moberg P.J., Agrin R., Gur R.E., Gur R.C., Turetsky B.I., Doty R.L. Olfactory dysfunction in schizophrenia: a qualitative and quantitative review. Neuropsychopharmacology 1999, 21:325-340.
45. Moberg P.J., Doty R.L., Turetsky B.I., Arnold S.E., Mahr R.N., Gur R.C., Bilker W., Gur R.E. Olfactory identification deficits in schizophrenia: correlation with duration of illness. Am. J. Psychiatry 1997, 154:1016-1018.
46. Nguyen T.V., Kosofsky B.E., Birnbaum R., Cohen B.M., Hyman S.E. Differential expression of c-fos and zif268 in rat striatum after haloperidol, clozapine, and amphetamine. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:4270-4274.
47. Orzi F., Dow-Edwards D., Jehle J., Kennedy C., Sokoloff L. Comparative effects of acute and chronic administration of amphetamine on local cerebral glucose utilization in the conscious rat. J. Cereb. Blood Flow Metab. 1983, 3:154-160.
48. Overpeck J.G., Colson S.H., Hohmann J.R., Applestine M.S., Reilly J.F. Concentrations of circulating steroids in normal prepubertal and adult male and female humans, chimpanzees, rhesus monkeys, rats, mice, and hamsters: a literature survey. J. Toxicol. Environ. Health 1978, 4:785-803.
49. 3H]dopamine release. Brain Res. 1991, 566:255-264.
50. Quinlan M.G., Hussain D., Brake W.G. Use of cognitive strategies in rats: the role of estradiol and its interaction with dopamine. Horm. Behav. 2008, 53:185-191.
51. Riecher-Rossler A., Hafner H., Stumbaum M., Maurer K., Schmidt R. Can estradiol modulate schizophrenic symptomatology?. Schizophr. Bull. 1994, 20:203-214.
52. Samaha A.N., Seeman P., Stewart J., Rajabi H., Kapur S. Breakthrough dopamine supersensitivity during ongoing antipsychotic treatment leads to treatment failure over time. J. Neurosci. 2007, 27:2979-2986.
53. Sarvari M., Deli L., Kocsis P., Mark L., Maasz G., Hrabovszky E., Kallo I., Gajari D., Vastagh C., Sumegi B., Tihanyi K., Liposits Z. Estradiol and isotype-selective estrogen receptor agonists modulate the mesocortical dopaminergic system in gonadectomized female rats. Brain Res. 2014, 1583:1-11.
54. Schmidt W.J., Beninger R.J. Behavioural sensitization in addiction, schizophrenia, Parkinson's disease and dyskinesia. Neurotox. Res. 2006, 10:161-166.
55. Seeman M.V., Lang M. The role of estrogens in schizophrenia gender differences. Schizophr. Bull. 1990, 16:185-194.
56. Shepard P.D., Holcomb H.H., Gold J.M. Schizophrenia in translation: the presence of absence: habenular regulation of dopamine neurons and the encoding of negative outcomes. Schizophr. Bull. 2006, 32:417-421.
57. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 1997, 388:507-525.
58. Shurman B., Horan W.P., Nuechterlein K.H. Schizophrenia patients demonstrate a distinctive pattern of decision-making impairment on the Iowa Gambling Task. Schizophr. Res. 2005, 72:215-224.
59. Silverman J.L., Koenig J.I. Evidence for the involvement of ERbeta and RGS9-2 in 17-beta estradiol enhancement of amphetamine-induced place preference behavior. Horm. Behav. 2007, 52:146-155.
60. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 1982, 9:321-353.
61. Tamminga C.A., Thaker G.K., Buchanan R., Kirkpatrick B., Alphs L.D., Chase T.N., Carpenter W.T. Limbic system abnormalities identified in schizophrenia using positron emission tomography with fluorodeoxyglucose and neocortical alterations with deficit syndrome. Arch. Gen. Psychiatry 1992, 49:522-530.
62. Torrey E.F., Peterson M.R. Schizophrenia and the limbic system. Lancet 1974, 2:942-946.
63. Turetsky B.I., Moberg P.J., Yousem D.M., Doty R.L., Arnold S.E., Gur R.E. Reduced olfactory bulb volume in patients with schizophrenia. Am. J. Psychiatry 2000, 157:828-830.
64. Uslaner J., Badiani A., Norton C.S., Day H.E., Watson S.J., Akil H., Robinson T.E. Amphetamine and cocaine induce different patterns of c-fos mRNA expression in the striatum and subthalamic nucleus depending on environmental context. Eur. J. Neurosci. 2001, 13:1977-1983.
65. Van Eden C.G., Hoorneman E.M., Buijs R.M., Matthijssen M.A., Geffard M., Uylings H.B. Immunocytochemical localization of dopamine in the prefrontal cortex of the rat at the light and electron microscopical level. Neuroscience 1987, 22:849-862.
66. Ventura J., Nuechterlein K.H., Lukoff D., Hardesty J.P. A prospective study of stressful life events and schizophrenic relapse. J. Abnorm. Psychol. 1989, 98:407-411.
67. Vezina P. D1 dopamine receptor activation is necessary for the induction of sensitization by amphetamine in the ventral tegmental area. J. Neurosci. 1996, 16:2411-2420.
68. Wechsler L.R., Savaki H.E., Sokoloff L. Effects of d- and l-amphetamine on local cerebral glucose utilization in the conscious rat. J. Neurochem. 1979, 32:15-22.
69. Wulff K., Dijk D.J., Middleton B., Foster R.G., Joyce E.M. Sleep and circadian rhythm disruption in schizophrenia. Br. J. Psychiatry 2012, 200:308-316.