Males, but not females, lose tyrosine hydroxylase fibers in the medial prefrontal cortex and are impaired on a delayed alternation task during aging

Behavioural Brain Research

Volumn 243, Issue 1, 2013, Pages 239-246

  Chisholm, Nioka C ^a,b   Kim, Taehyeon ^a   Juraska, Janice M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

Aging; Dopamine; Prefrontal cortex; Sex differences; T Maze; Working memory

Indexed keywords

ESTROGEN; PROGESTERONE; TESTOSTERONE; TYROSINE 3 MONOOXYGENASE;

ADULT ANIMAL; AGE; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BEHAVIORAL SCIENCE; CONTROLLED STUDY; DELAYED ALTERNATION TASK; DOPAMINERGIC SYSTEM; ENZYME ANALYSIS; FEMALE; HORMONE RELEASE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MAZE TEST; MEDIAL PREFRONTAL CORTEX; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; TASK PERFORMANCE;

AGING; ANIMALS; BEHAVIOR, ANIMAL; FEMALE; MALE; MAZE LEARNING; NERVE FIBERS; NEUROPSYCHOLOGICAL TESTS; PREFRONTAL CORTEX; RANDOM ALLOCATION; RATS; RATS, INBRED F344; REACTION TIME; SEX CHARACTERISTICS; TYROSINE 3-MONOOXYGENASE;

EID: 84873498123     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.01.009     Document Type: Article

References (65)

1. Pardo J.V., Lee J.T., Sheikh S.A., Surerus-Johnson C., Shah H., Munch K.R., et al. Where the brain grows old: decline in anterior cingulate and medial prefrontal function with normal aging. Neuroimage 2007, 35:1231-1237. pii: S1053-8119(07)00002-X. 10.1016/j.neuroimage.2006.12.044.
2. Raz N., Lindenberger U., Rodrigue K.M., Kennedy K.M., Head D., Williamson A., et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cerebral Cortex 2005, 15:1676-1689. 10.1093/cercor/bhi044.
3. Resnick S.M., Pham D.L., Kraut M.A., Zonderman A.B., Davatzikos C. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. Journal of Neuroscience 2003, 23:3295-3301.
4. de Brabander J.M., Kramers R.J., Uylings H.B. Layer-specific dendritic regression of pyramidal cells with ageing in the human prefrontal cortex. European Journal of Neuroscience 1998, 10:1261-1269.
5. Huttenlocher P.R. Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Research 1979, 163:195-205.
6. Jacobs B., Driscoll L., Schall M. Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. Journal of Comparative Neurology 1997, 386:661-680.
7. Masliah E., Mallory M., Hansen L., DeTeresa R., Terry R.D. Quantitative synaptic alterations in the human neocortex during normal aging. Neurology 1993, 43:192-197.
8. Grill J.D., Riddle D.R. Age-related and laminar-specific dendritic changes in the medial frontal cortex of the rat. Brain Research 2002, 937:8-21.
9. Markham J.A., Juraska J.M. Aging and sex influence the anatomy of the rat anterior cingulate cortex. Neurobiology of Aging 2002, 23:579-588.
10. Wallace M., Frankfurt M., Arellanos A., Inagaki T., Luine V. Impaired recognition memory and decreased prefrontal cortex spine density in aged female rats. Annals of the New York Academy of Sciences 2007, 1097:54-57. pii: 1097/1/54. 10.1196/annals.1379.026.
11. Stuss D.T., Benson D.F. Neuropsychological studies of the frontal lobes. Psychological Bulletin 1984, 95:3-28.
12. Mizoguchi K., Shoji H., Tanaka Y., Maruyama W., Tabira T. Age-related spatial working memory impairment is caused by prefrontal cortical dopaminergic dysfunction in rats. Neuroscience 2009, 10.1016/j.neuroscience.2009.05.023.
13. Ando S., Ohashi Y. Longitudinal study on age-related changes of working and reference memory in the rat. Neuroscience Letters 1991, 128:17-20. pii: 0304-3940(91)90750-N.
14. Barense M.D., Fox M.T., Baxter M.G. Aged rats are impaired on an attentional set-shifting task sensitive to medial frontal cortex damage in young rats. Learning and Memory 2002, 9:191-201. 10.1101/lm.48602.
15. Backman L., Lindenberger U., Li S.C., Nyberg L. Linking cognitive aging to alterations in dopamine neurotransmitter functioning: recent data and future avenues. Neuroscience and Biobehavioral Reviews 2010, 34:670-677. 10.1016/j.neubiorev.2009.12.008.
16. Juraska J.M., Lowry N.C. Neuroanatomical changes associated with cognitive aging. Current Topics in Behavioral Neurosciences 2012, 10:137-162. 10.1007/7854_2011_137.
17. Suhara T., Fukuda H., Inoue O., Itoh T., Suzuki K., Yamasaki T., et al. Age-related changes in human D1 dopamine receptors measured by positron emission tomography. Psychopharmacology 1991, 103:41-45.
18. de Keyser J., De Backer J.P., Vauquelin G., Ebinger G. The effect of aging on the D1 dopamine receptors in human frontal cortex. Brain Research 1990, 528:308-310.
19. Inoue M., Suhara T., Sudo Y., Okubo Y., Yasuno F., Kishimoto T., et al. Age-related reduction of extrastriatal dopamine D2 receptor measured by PET. Life Sciences 2001, 69:1079-1084.
20. Kaasinen V., Kemppainen N., Nagren K., Helenius H., Kurki T., Rinne J.O. Age-related loss of extrastriatal dopamine D(2)-like receptors in women. Journal of Neurochemistry 2002, 81:1005-1010.
21. Kaasinen V., Vilkman H., Hietala J., Nagren K., Helenius H., Olsson H., et al. Age-related dopamine D2/D3 receptor loss in extrastriatal regions of the human brain. Neurobiology of Aging 2000, 21:683-688.
22. Ota M., Yasuno F., Ito H., Seki C., Nozaki S., Asada T., et al. Age-related decline of dopamine synthesis in the living human brain measured by positron emission tomography with l-[beta-11C]DOPA. Life Sciences 2006, 79:730-736. 10.1016/j.lfs.2006.02.017.
23. Uylings H.B., Groenewegen H.J., Kolb B. Do rats have a prefrontal cortex?. Behavioural Brain Research 2003, 146:3-17.
24. Goldman-Rakic P.S., Brown R.M. Regional changes of monoamines in cerebral cortex and subcortical structures of aging rhesus monkeys. Neuroscience 1981, 6:177-187. pii: 0306-4522(81)90053-1.
25. Lacreuse A., Kim C.B., Rosene D.L., Killiany R.J., Moss M.B., Moore T.L., et al. age, and training modulate spatial memory in the rhesus monkey (Macaca mulatta). Behavioral Neuroscience 2005, 119:118-126. 10.1037/0735-7044.119.1.118.
26. Lacreuse A., Herndon J.G., Killiany R.J., Rosene D.L., Moss M.B. Spatial cognition in rhesus monkeys: male superiority declines with age. Hormones and Behavior 1999, 36:70-76. 10.1006/hbeh.1999.1532.
27. Lukoyanov N.V., Andrade J.P., Dulce Madeira M., Paula-Barbosa M.M. Effects of age and sex on the water maze performance and hippocampal cholinergic fibers in rats. Neuroscience Letters 1999, 269:141-144.
28. Yates M.A., Markham J.A., Anderson S.E., Morris J.R., Juraska J.M. Regional variability in age-related loss of neurons from the primary visual cortex and medial prefrontal cortex of male and female rats. Brain Research 2008, 1218:1-12. 10.1016/j.brainres.2008.04.055.
29. Frick K.M., Burlingame L.A., Delaney S.S., Berger-Sweeney J. Sex differences in neurochemical markers that correlate with behavior in aging mice. Neurobiology of Aging 2002, 23:145-158.
30. Luine V.N., Renner K.J., Heady S., Jones K.J. Age and sex-dependent decreases in ChAT in basal forebrain nuclei. Neurobiology of Aging 1986, 7:193-198.
31. Tanila H., Taira T., Piepponen T.P., Honkanen A. Effect of sex and age on brain monoamines and spatial learning in rats. Neurobiology of Aging 1994, 15:733-741.
32. Veng L.M., Granholm A.C., Rose G.M. Age-related sex differences in spatial learning and basal forebrain cholinergic neurons in F344 rats. Physiology and Behavior 2003, 80:27-36.
33. McDermott J.L., Dluzen D.E. Aging and sex differences in striatal dopaminergic function. Neuroscience 2007, 149:401-408. 10.1016/j.neuroscience.2007.06.058.
34. Luine V., Bowling D., Hearns M. Spatial memory deficits in aged rats: contributions of monoaminergic systems. Brain Research 1990, 537:271-278. pii: 0006-8993(90)90368-L.
35. Kritzer M.F. Long-term gonadectomy affects the density of tyrosine hydroxylase- but not dopamine-beta-hydroxylase-, choline acetyltransferase- or serotonin-immunoreactive axons in the medial prefrontal cortices of adult male rats. Cerebral Cortex 2003, 13:282-296.
36. Kritzer M.F., Kohama S.G. Ovarian hormones differentially influence immunoreactivity for dopamine beta- hydroxylase, choline acetyltransferase, and serotonin in the dorsolateral prefrontal cortex of adult rhesus monkeys. Journal of Comparative Neurology 1999, 409:438-451.
37. Kritzer M.F., Kohama S.G. Ovarian hormones influence the morphology, distribution, and density of tyrosine hydroxylase immunoreactive axons in the dorsolateral prefrontal cortex of adult rhesus monkeys. Journal of Comparative Neurology 1998, 395:1-17. doi: 10.1002/(SICI)1096-9861(19980525)395:1<1::AID-CNE1>3.0.CO;2-4.
38. Wang C., Leung A., Sinha-Hikim A.P. Reproductive aging in the male brown-Norway rat: a model for the human. Endocrinology 1993, 133:2773-2781.
39. Chisholm N.C., Packard A.R., Koss W.A., Juraska J.M. The effects of long-term treatment with estradiol and medroxyprogesterone acetate on tyrosine hydroxylase fibers and neuron number in the medial prefrontal cortex of aged female rats. Endocrinology 2012, 153. 10.1210/en. 2012-1412.
40. Dudley S.D. Responsiveness to estradiol in central nervous system of aging female rats. Neuroscience and Biobehavioral Reviews 1982, 6:39-45.
41. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. Journal of Comparative Neurology 1997, 388:507-525.
42. Maggi A., Zucchi I. Sexual differentiation of mammalian frontal cortex. Life Sciences 1987, 40:1155-1160.
43. Aubele T., Kritzer M.F. Androgen influence on prefrontal dopamine systems in adult male rats: localization of cognate intracellular receptors in medial prefrontal projections to the ventral tegmental area and effects of gonadectomy and hormone replacement on glutamate-stimulated extracellular dopamine level. Cerebral Cortex 2012, 22:1799-1812. 10.1093/cercor/bhr258.
44. Kritzer M.F., McLaughlin P.J., Smirlis T., Robinson J.K. Gonadectomy impairs T-maze acquisition in adult male rats. Hormones and Behavior 2001, 39:167-174. pii: S0018-506X(01)91645-9. 10.1006/hbeh.2001.1645.
45. Gibbs R.B., Johnson D.A. Sex-specific effects of gonadectomy and hormone treatment on acquisition of a 12-arm radial maze task by Sprague Dawley rats. Endocrinology 2008, 149:3176-3183. 10.1210/en.2007-1645.
46. Bimonte-Nelson H.A., Singleton R.S., Nelson M.E., Eckman C.B., Barber J., Scott T.Y., et al. Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Experimental Neurology 2003, 181:301-312. pii: S001448860300061X.
47. Frick KM Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here?. Hormones and Behavior 2009, 55:2-23. 10.1016/j.yhbeh.2008.08.015.
48. Gibbs R.B. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiology of Aging 2000, 21:107-116. pii: S0197-4580(00)00103-2.
49. Miller M.M., Hyder S.M., Assayag R., Panarella S.R., Tousignant P., Franklin K.B. Estrogen modulates spontaneous alternation and the cholinergic phenotype in the basal forebrain. Neuroscience 1999, 91:1143-1153.
50. Chisholm N.C., Juraska J.M. Long-term replacement of estrogen in combination with medroxyprogesterone acetate improves acquisition of an alternation task in middle-aged female rats. Behavioral Neuroscience 2012, 126:128-136. 10.1037/a0026461.
51. Floresco S.B., Magyar O. Mesocortical dopamine modulation of executive functions: beyond working memory. Psychopharmacology 2006, 188:567-585. 10.1007/s00213-006-0404-5.
52. Hao J., Rapp P.R., Leffler A.E., Leffler S.R., Janssen W.G., Lou W., et al. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. Journal of Neuroscience 2006, 26:2571-2578. pii: 26/9/2571. 10.1523/jneurosci.3440-05.2006.
53. Rapp P.R., Morrison J.H., Roberts J.A. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. Journal of Neuroscience 2003, 23:5708-5714. pii: 23/13/5708.
54. Chisholm N.C., Juraska J.M. Effects of long-term treatment with estrogen and medroxyprogesterone acetate on synapse number in the medial prefrontal cortex of aged female rats. Menopause 2012, 19:804-811. 10.1097/gme.0b013e31824d1fc4.
55. Thakur M.K., Asaithambi A., Mukherjee S. Synthesis and phosphorylation of androgen receptor of the mouse brain cortex and their regulation by sex steroids during aging. Molecular and Cellular Biochemistry 2000, 203:95-101.
56. Goudsmit E., Van de Poll N.E., Swaab D.F. Testosterone fails to reverse spatial memory decline in aged rats and impairs retention in young and middle-aged animals. Behavioral and Neural Biology 1990, 53:6-20.
57. Chambers K.C., Thornton J.E., Roselli C.E. Age-related deficits in brain androgen binding and metabolism, testosterone, and sexual behavior of male rats. Neurobiology of Aging 1991, 12:123-130.
58. Cui R., Zhang G., Kang Y., Cheng Q., Tan H., Cui H., et al. Amelioratory effects of testosterone propionate supplement on behavioral, biochemical and morphological parameters in aged rats. Experimental Gerontology 2012, 47:67-76. 10.1016/j.exger.2011.10.009.
59. Mitra S.W., Hoskin E., Yudkovitz J., Pear L., Wilkinson H.A., Hayashi S., et al. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 2003, 144:2055-2067.
60. Carr D.B., Sesack S.R. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. Journal of Neuroscience 2000, 20:3864-3873.
61. Gariano R.F., Groves P.M. Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortices. Brain Research 1988, 462:194-198.
62. Sullivan R.M., Duchesne A., Hussain D., Waldron J., Laplante F. Effects of unilateral amygdala dopamine depletion on behaviour in the elevated plus maze: role of sex, hemisphere and retesting. Behavioural Brain Research 2009, 205:115-122. 10.1016/j.bbr.2009.07.023.
63. Duchesne A., Dufresne M.M., Sullivan R.M. Sex differences in corticolimbic dopamine and serotonin systems in the rat and the effect of postnatal handling. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2009, 33:251-261. 10.1016/j.pnpbp.2008.11.012.
64. Lu X.Y., Churchill L., Kalivas P.W. Expression of D1 receptor mRNA in projections from the forebrain to the ventral tegmental area. Synapse 1997, 25:205-214. doi: 10.1002/(SICI)1098-2396(199702)25:2<205::AID-SYN11>3.0.CO;2-X.
65. Van De Werd H.J., Rajkowska G., Evers P., Uylings H.B. Cytoarchitectonic and chemoarchitectonic characterization of the prefrontal cortical areas in the mouse. Brain Structure & Function 2010, 214:339-353. 10.1007/s00429-010-0247-z.