Sex differences and effects of cocaine on excitatory synapses in the nucleus accumbens

Neuropharmacology

Volumn 61, Issue 1-2, 2011, Pages 217-227

  Wissman, Anne Marie ^a   McCollum, Andrew F ^a   Huang, Guang Zhe ^a   Nikrodhanond, Amisra A ^a   Woolley, Catherine S ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Addiction; Dendritic spine; Medium spiny neuron; Psychostimulants; Sensitization; Sex difference

Indexed keywords

COCAINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL DENSITY; COCAINE DEPENDENCE; CONTROLLED STUDY; DENDRITIC SPINE; EVOKED RESPONSE; EXCITATORY SYNAPSE; FEMALE; FREQUENCY MODULATION; LOCOMOTION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; SMOKING CESSATION; SPINAL CORD NERVE CELL; SYNAPSE;

ANIMALS; COCAINE; DENDRITIC SPINES; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; MALE; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; SYNAPSES;

EID: 79957813381     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.04.002     Document Type: Article

References (69)

1. Alvarez, V.A., Sabatini, B.L., 2007. Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 30, 79-97.
2. Bachtell, R.K., Self, D.W., 2008. Renewed cocaine exposure produces transient alterations in nucleus accumbens AMPA receptor-mediated behavior. J. Neurosci. 28, 12808-12814.
3. Becker, J.B., Hu, M., 2008. Sex differences in drug abuse. Front Neuroendocrinol. 29, 36-47.
4. Bell, K., Duffy, P., Kalivas, P.W., 2000. Context-specific enhancement of glutamate transmission by cocaine. Neuropsychopharmacology 23, 335-344. (Pubitemid 30609667)
5. Belleau, M.L., Warren, R.A., 2000. Postnatal development of electrophysiological properties of nucleus accumbens neurons. J. Neurophysiol. 84, 2204-2216.
6. Boudreau, A.C., Wolf, M.E., 2005. Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J. Neurosci. 25, 9144-9151. (Pubitemid 41500822)
7. Boudreau, A.C., Reimers, J.M., Milovanovic, M., Wolf, M.E., 2007. Cell surface AMPA receptors in the rat nucleus accumbens increase during cocaine withdrawal but internalize after cocaine challenge in association with altered activation of mitogen-activated protein kinases. J. Neurosci. 27, 10621-10635. (Pubitemid 47502017)
8. Boudreau, A.C., Ferrario, C.R., Glucksman, M.J., Wolf, M.E., 2009. Signaling pathway adaptations and novel protein kinase A substrates related to behavioral sensitization to cocaine. J. Neurochem. 110, 363-377.
9. Bourdeau, V., Deschenes, J., Metivier, R., Nagai, Y., Nguyen, D., Bretschneider, N., Gannon, F., White, J.H., Mader, S., 2004. Genome-wide identification of high-affinity estrogen response elements in human and mouse. Mol. Endocrinol. 18, 1411-1427.
10. Brog, J.S., Salyapongse, A., Deutch, A.Y., Zahm, D.S., 1993. The patterns of afferent innervation of the core and shell in the "accumbens" part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluorogold. J. Comp. Neurol. 338, 255-278.
11. Chen, J., An, B.S., Cheng, L., Hammond, G.L., Leung, P.C., 2009. Gonadotropin-releasing hormone-mediated phosphorylation of estrogen receptor-alpha contributes to fosB expression in mouse gonadotrophs. Endocrinology 150, 4583-4593.
12. Dietz, D.M., Dietz, K.C., Nestler, E.J., Russo, S.J., 2009. Molecular mechanisms of psychostimulant-induced structural plasticity. Pharmacopsychiatry 42 (Suppl.1), S69-S78.
13. Dong, Y., Green, T., Saal, D., Marie, H., Neve, R., Nestler, E.J., Malenka, R.C., 2006. CREB modulates excitability of nucleus accumbens neurons. Nat. Neurosci. 9, 475-477.
14. Downs, A.W., Eddy, N.B., 1932. The effect of repeated doses of cocaine on the rat. J. Pharmacol. Exp. Ther. 46, 199-200.
15. Evans, S.M., Foltin, R.W., 2010. Does the response to cocaine differ as a function of sex or hormonal status in human and non-human primates? Horm. Behav. 58, 13-21.
16. Fan, L., Hanbury, R., Pandey, S.C., Cohen, R.S., 2008. Dose and time effects of estrogen on expression of neuron-specific protein and cyclic AMP response element-binding protein and brain region volume in the medial amygdala of ovariectomized rats. Neuroendocrinology 88, 111-126.
17. Ferrario, C.R., Robinson, T.E., 2007. Amphetamine pretreatment accelerates the subsequent escalation of cocaine self-administration behavior. Eur. Neuropsychopharmacol. 17, 352-357.
18. Festa, E.D., Quinones-Jenab, V., 2004. Gonadal hormones provide the biological basis for sex differences in behavioral responses to cocaine. Horm. Behav. 46, 509-519.
19. Forlano, P.M., Woolley, C.S., 2010. Quantitative analysis of pre- and postsynaptic sex differences in the nucleus accumbens. J. Comp. Neurol. 518, 1330-1348.
20. French, S.J., Totterdell, S., 2004. Quantification of morphological differences in boutons from different afferent populations to the nucleus accumbens. Brain Res. 1007, 167-177. (Pubitemid 38520185)
21. Ghasemzadeh, M.B., Permenter, L.K., Lake, R., Worley, P.F., Kalivas, P.W., 2003. Homer1 p.oteins and AMPA receptors modulate cocaine-induced behavioural plasticity. Eur. J. Neurosci. 18, 1645-1651.
22. Groenewegen, H.J., Wright, C.I., Beijer, A.V., 1996. The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog. Brain Res. 107, 485-511. (Pubitemid 26401684)
23. Groenewegen, H.J., Wright, C.I., Beijer, A.V., Voorn, P., 1999. Convergence and segregation of ventral striatal inputs and outputs. Ann. N.Y. Acad. Sci. 877, 49-63.
24. Heimer, L., Alheid, G.F., de Olmos, J.S., Groenewegen, H.J., Haber, S.N., Harlan, R.E., Zahm, D.S., 1997. The accumbens: beyond the core-shell dichotomy. J. Neuropsychiatry Clin. Neurosci. 9, 354-381.
25. Hu, M., Becker, J.B., 2003. Effects of sex and estrogen on behavioral sensitization to cocaine in rats. J. Neurosci. 23, 693-699. (Pubitemid 36139568)
26. Ito, R., Robbins, T.W., Everitt, B.J., 2004. Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat. Neurosci. 7, 389-397.
27. Kalivas, P.W., 2009. The glutamate homeostasis hypothesis of addiction. Nat. Rev. Neurosci. 10, 561-572.
28. Kalivas, P.W., Volkow, N.D., 2005. The neural basis of addiction: a pathology of motivation and choice. Am. J. Psychiatry 162, 1403-1413. (Pubitemid 41105554)
29. King, T.S., Canez, M.S., Gaskill, S., Javors, M.A., Schenken, R.S., 1993. Chronic cocaine disruption of estrous cyclicity in the rat: dose-dependent effects. J. Pharmacol. Exp. Ther. 264, 29-34.
30. Kourrich, S., Thomas, M.J., 2009. Similar neurons, opposite adaptations: psychostimulant experience differentially alters firing properties in accumbens core versus shell. J. Neurosci. 29, 12275-12283.
31. Kourrich, S., Rothwell, P.E., Klug, J.R., Thomas, M.J., 2007. Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J. Neurosci. 27, 7921-7928. (Pubitemid 47173313)
32. Kudoh, S.N., Taguchi, T., 2002. A simple exploratory algorithm for the accurate and fast detection of spontaneous synaptic events. Biosens. Bioelectron.17, 773-782.
33. Lai, K.O., Ip, N.Y., 2009. Recent advances in understanding the roles of Cdk5 in synaptic plasticity. Biochim. Biophys. Acta 1792, 741-745.
34. LeDoux, J.E., 2000. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184.
35. Li, Y., Kolb, B., Robinson, T.E., 2003. The location of persistent amphetamine-induced changes in the density of dendritic spines on medium spiny neurons in the nucleus accumbens and caudate-putamen. Neuropsychopharmacology 28, 1082-1085.
36. Li, Y., Acerbo, M.J., Robinson, T.E., 2004. The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur. J. Neurosci. 20, 1647-1654.
37. Lorrain, D.S., Arnold, G.M., Vezina, P., 2000. Previous exposure to amphetamine increases incentive to obtain the drug: long-lasting effects revealed by the progressive ratio schedule. Behav. Brain Res. 107, 9-19.
38. Loweth, J.A., Singer, B.F., Baker, L.K., Wilke, G., Inamine, H., Bubula, N., Alexander, J.K., Carlezon Jr., W.A., Neve, R.L., Vezina, P., 2010. Transient overexpression of alpha-Ca2+/calmodulin-dependent protein kinase II in the nucleus accumbens shell enhances behavioral responding to amphetamine. J. Neurosci. 30, 939-949.
39. Lynch, W.J., Carroll, M.E., 1999. Sex differences in the acquisition of intravenously self-administered cocaine and heroin in rats. Psychopharmacology (Berl.) 144, 77-82. (Pubitemid 29242673)
40. Matsuzaki, M., Honkura, N., Ellis-Davies, G.C., Kasai, H., 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766. (Pubitemid 38833127)
41. Maze, I., Covington 3rd, H.E., Dietz, D.M., LaPlant, Q., Renthal, W., Russo, S.J., Mechanic, M., Mouzon, E., Neve, R.L., Haggarty, S.J., Ren, Y., Sampath, S.C., Hurd, Y.L., Greengard, P., Tarakhovsky, A., Schaefer, A., Nestler, E.J., 2010. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327, 213-216.
42. McGinty, J.F., Whitfield Jr., T.W., Berglind, W.J., 2010. Brain-derived neurotrophic factor and cocaine addiction. Brain Res. 1314, 183-193.
43. Meredith, G.E., Agolia, R., Arts, M.P., Groenewegen, H.J., Zahm, D.S., 1992. Morphological differences between projection neurons of the core and shell in the nucleus accumbens of the rat. Neuroscience 50, 149-162.
44. Nestler, E.J., 2008. Review. Transcriptional mechanisms of addiction: role of DeltaFosB. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 3245-3255.
45. O'Donnell, P., Grace, A.A., 1993. Physiological and morphological properties of accumbens core and shell neurons recorded in vitro. Synapse 13, 135-160. (Pubitemid 23051482)
46. Paulson, P.E., Camp, D.M., Robinson, T.E., 1991. Time course of transient behavioral depression and persistent behavioral sensitization in relation to regional brain monoamine concentrations during amphetamine withdrawal in rats. Psychopharmacology (Berl.) 103, 480-492.
47. Paxinos, G., Watson, C., 1998. The Rat Brain in Stereotaxic Coordinates, 4th ed. Academic Press, San Diego.
48. Piazza, P.V., Deminiere, J.M., Le Moal, M., Simon, H., 1989. Factors that predict individual vulnerability to amphetamine self-administration. Science 245,1511-1513. (Pubitemid 19243245)
49. Pierce, R.C., Kalivas, P.W., 1997. A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res. Brain Res. Rev. 25, 192-216.
50. Pierce, R.C., Bell, K., Duffy, P., Kalivas, P.W., 1996. Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J. Neurosci. 16, 1550-1560. (Pubitemid 26145933)
51. Prut, L., Belzung, C., 2003. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463, 3-33.
52. Pulvirenti, L., Berrier, R., Kreifeldt, M., Koob, G.F., 1994. Modulation of locomotor activity by NMDA receptors in the nucleus accumbens core and shell regions of the rat. Brain Res. 664, 231-236. (Pubitemid 24347619)
53. Quinones-Jenab, V., 2006. Why are women from Venus and men from Mars when they abuse cocaine? Brain Res. 1126, 200-203.
54. Robinson, T.E., Kolb, B., 1997. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J. Neurosci. 17, 8491-8497. (Pubitemid 27461070)
55. Robinson, T.E., Kolb, B., 1999. Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur. J. Neurosci. 11, 1598-1604.
56. Robinson, T.E., Kolb, B., 2004. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47 (Suppl. 1), 33-46. (Pubitemid 39298251)
57. Roy, S.N., Bhattacharyya, A.K., Pradhan, S., Pradhan, S.N., 1978. Behavioural and neurochemical effects of repeated administration of cocaine in rats. Neuropharmacology 17, 559-564. (Pubitemid 9003536)
58. Russo, S.J., Mazei-Robison, M.S., Ables, J.L., Nestler, E.J., 2009. Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 56 (Suppl. 1), 73-82.
59. Russo, S.J., Jenab, S., Fabian, S.J., Festa, E.D., Kemen, L.M., Quinones-Jenab, V., 2003. Sex differences in the conditioned rewarding effects of cocaine. Brain Res. 970, 214-220. (Pubitemid 36423197)
60. Scharfman, H.E., MacLusky, N.J., 2006. Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front. Neuroendocrinol 27, 415-435. (Pubitemid 44738017)
61. Sell, S.L., Thomas, M.L., Cunningham, K.A., 2002. Influence of estrous cycle and estradiol on behavioral sensitization to cocaine in female rats. Drug Alcohol Depend. 67, 281-290. (Pubitemid 34786263)
62. Sircar, R., Kim, D., 1999. Female gonadal hormones differentially modulate cocaine-induced behavioral sensitization in Fischer, Lewis, and Sprague-Dawley rats. J. Pharmacol. Exp. Ther. 289, 54-65.
63. Sturm, V., Lenartz, D., Koulousakis, A., Treuer, H., Herholz, K., Klein, J.C., Klosterkotter, J., 2003. The nucleus accumbens: a target for deep brain stimulation in obsessive-compulsive- and anxiety-disorders. J. Chem. Neuroanat. 26, 293-299.
64. van Haaren, F., Meyer, M.E., 1991. Sex differences in locomotor activity after acute and chronic cocaine administration. Pharmacol. Biochem. Behav. 39, 923-927.
65. Voorn, P., Gerfen, C.R., Groenewegen, H.J., 1989. Compartmental organization of the ventral striatum of the rat: immunohistochemical distribution of enkephalin, substance P, dopamine, and calcium-binding protein. J. Comp. Neurol. 289, 189-201.
66. Wheeler, R.A., Carelli, R.M., 2009. Dissecting motivational circuitry to understand substance abuse. Neuropharmacology 56 (Suppl. 1), 149-159.
67. Yang, C.R., Seamans, J.K., Gorelova, N., 1996. Electrophysiological and morphological properties of layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro. J. Neurosci. 16, 1904-1921. (Pubitemid 26145967)
68. Zachariou, V., Sgambato-Faure, V., Sasaki, T., Svenningsson, P., Berton, O., Fienberg, A.A., Nairn, A.C., Greengard, P., Nestler, E.J., 2006. Phosphorylation of DARPP-32 at Threonine-34 is required for cocaine action. Neuropsychopharmacology 31, 555-562. (Pubitemid 43276971)
69. Zhang, X.F., Hu, X.T., White, F.J., 1998. Whole-cell plasticity in cocaine withdrawal: reduced sodium currents in nucleus accumbens neurons. J. Neurosci. 18, 488-498. (Pubitemid 28046806)