Measurement of steroid concentrations in brain tissue: Methodological considerations

Frontiers in Endocrinology

Volumn 2, Issue SEP, 2011, Pages

  Taves, Matthew D ^a   Ma, Chunqi ^a   Heimovics, Sarah A ^a   Saldanha, Colin J ^b   Soma, Kiran K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b LEHIGH UNIVERSITY   (United States)

Author keywords

Corticosterone; Estradiol; Mouse; Songbird; Testosterone

Indexed keywords

EID: 84857433943     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2011.00039     Document Type: Review

References (149)

1. Alomary, A. A., Fitzgerald, R. I., and Purdy, R. H. (2001). Neurosteroid analysis. Int. Rev. Neurobiol. 46, 97-115.
2. Amateau, S. K., Alt, J. J., Stamps, C. L., and McCarthy, M. M. (2004). Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology 145, 2906-2917.
3. American Veterinary Medical Association. (2007). AVMA Guidelines on Euthanasia. Available at: http://www.avma.org/issues/animal_welfare/euthanasia.pdf
4. Appelblad, P., and Irgum, K. (2002). Separation and detection of neu-roactive steroids from biological matrices. J. Chromatogr. A 955, 151-182.
5. Azcoitia, I., Sierra, A., Veiga, S., Honda, S.-I., Harada, N., and Garcia-Segura, L. M. (2001). Brain aromatase is neuroprotective. J. Neurobiol. 47, 318-329.
6. Balthazart, J., Baillien, M., and Foidart, A. (1993). Brain aromatase and the control of male sexual behavior. J. Steroid Biochem. Mol. Biol. 44, 521-540.
7. Balthazart, J., and Ball, G. F. (2006). Is brain estradiol a hormone or a neu-rotransmitter Trends Neurosci. 29, 241-249.
8. Barbaccia, M. L., Roscetti, G., Trabuc-chi, M., Mostallino, M. C., Con-cas, A., Purdy, R. H., and Biggio, G. (1996). Time-dependent changes in rat brain neuroactive steroid concentrations and GABAA receptor function after acute stress. Neuroen-docrinology 63, 166-172.
9. Baulieu, E. E. (1998). Neurosteroids: a novel function of the brain. Psy-choneuroendocrinology 23, 963-987.
10. Bélanger, A., Couture, J., Caron, S., and Roy, R. (1990). Determination of nonconjugated and conjugated steroid levels in plasma and prostate after separation on C-18 columns. Ann. N. Y. Acad. Sci. 595, 251-259.
11. Breuner, C. W., and Orchinik, M. (2002). Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175, 99-112.
12. Brummelte, S., Schmidt, K. L., Taves, M. D., Soma, K. K., and Galea, L. A. M. (2010). Elevated corticosterone levels in stomach milk, serum, and brain of male and female offspring after maternal corticosterone treatment in the rat. Dev. Neurobiol. 70, 714-725.
13. Bruzzone, F., Do Rego, J.-L., Luu-The, V., Pelletier, G., Vallarino, M., and Vaudry, H. (2010). Immunohisto-chemical localization and biological activity of 3β-hydroxysteroid dehy-drogenase and 5α-reductase in the brain of the frog, Rana esculenta, during development. J. Chem. Neu-roanat. 39, 35-50.
14. Butte, J. C., Kakihana, R., and Noble, E. P. (1972). Rat and mouse brain corticosterone. Endocrinology 90, 1091-1100.
15. Callard, G. V., Petro, Z., and Ryan, K. J. (1978). Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology 103, 2283-2291.
16. Caruso, D., Scurati, S., Maschi, O., De Angelis, L., Roglio, I., Giatti, S., Garcia-Segura, L. M., and Mel-cangi, R. C. (2008). Evaluation of neuroactive steroid levels by liquid chromatography-tandem mass spectrometry in central and peripheral nervous system: effect of diabetes. Neurochem. Int. 52, 560-568.
17. Chao, A., Schlinger, B. A., and Remage-Healey, L. (2011). Combined liquid and solid-phase extraction improves quantification of brain estrogen content. Front. Neuroanat. 5:57. doi: 10.3389/fnana.2011.00057
18. Chard, T. (1995). An Introduction to Radioimmunoassay and Related Techniques, 5th Edn. Amsterdam: Elsevier.
19. Charlier, T. D., Newman, A. E. M., Heimovics, S. A., Po, K. W. L., Saldanha, C. J., and Soma, K. K. (2011). Rapid effects of aggressive interactions on aromatase activity and oestradiol in discrete brain regions of wild male white-crowned sparrows. J. Neuroendocrinol. 23, 742-753.
20. Charlier, T. D., Po, K. W. L., Newman, A. E. M., Shah, A. H., Saldanha, C. J., and Soma, K. K. (2010). 17β-Estradiol levels in male zebra finch brain: combining Palkovits punch and an ultrasensitive radioimmunoassay. Gen. Comp. Endocrinol. 167, 18-26.
21. Charlier, T. D., Underhill, C., Hammond, G. L., and Soma, K. K. (2009). Effects of aggressive encounters on plasma corticosteroid-binding globulin and its ligands in white-crowned sparrows. Horm. Behav. 56, 339-347.
22. Chin, E. H., Shah, A. H., Schmidt, K. L., Sheldon, L. D., Love, O. P., and Soma, K. K. (2008). Sex differences in DHEA and estradiol during development in a wild songbird: jugular versus brachial plasma. Horm. Behav. 54, 194-202.
23. Close, D. A., Yun, S.-S., McCormick, S. D., Wildbill, A. J., and Li, W. (2010). 11-Deoxycortisol is a corti-costeroid hormone in the lamprey. Proc. Natl. Acad. Sci. U.S.A. 107, 13942-13947.
24. Compagnone, N. A., and Mellon, S. H. (2000). Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinol. 21:1-56. doi: 10.1006/frne.1999.0188
25. Concas, A., Porcu, P., Sogliano, C., Serra, M., Purdy, R. H., and Biggio, G. (2000). Caffeine-induced increases in the brain and plasma concentrations of neuroactive steroids in the rat. Pharmacol. Biochem. Behav. 66, 39-45.
26. Cornil, C. A. (2009). Rapid regulation of brain oestrogen synthesis: the behavioural roles of oestrogens and their fates. J. Neuroendocrinol. 21, 217-226.
27. Corpéchot, C., Robel, P., Axelson, M., Sjövall, J., and Baulieu, E.-E. (1981). Characterization and measurement of dehydroepiandrosterone sulfate in rat brain. Proc. Natl. Acad. Sci. U.S.A. 78, 4704-4707.
28. Croft, A. P., O'Callaghan, M. J., Shaw, S. G.,Connolly, G., Jacquot, C., and Little, H. J. (2008). Effects of minor laboratory procedures, adrenalectomy, social defeat or acute alcohol on regional brain concentrations of cor-ticosterone. Brain Res. 1238, 12-22.
29. De Kloet, E. R. (2006). From punch to profile. Neurochem. Res. 31, 131-135.
30. Diotel, N., Do Rego, J.-L., Anglade, I., Vaillant, C., Pellegrini, E., Gueguen, M.-M., Mironov, S., Vaudry, H., and Kah, O. (2011). Activity and expression of steroidogenic enzymes in the brain of adult zebrafish. Eur. J. Neurosci. 34, 45-56.
31. Diotel, N., Le Page, Y., Mouriec, K., Tong, S.-K., Pellegrini, E., Vail-lant, C., Anglade, I., Brion, F., Pakdel, F., Chung, B.-C., and Kah, O. (2010). Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front. Neuroendocrinol. 31:172-192. doi: 10.1016/j.yfrne.2010.01.003
32. Do Rego, J. L., Seong, J. Y., Burel, D., Leprince, J., Luu-The, V., Tsutsui, K., Tonon, M.-C., Pelletier, G., and Vaudry, H. (2009). Neuros-teroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides. Front. Neu-roendocrinol. 30:259-301. doi: 10.1016/j.yfrne.2009.05.006
33. Dornhorst, A., and Gann, D. S. (1978). Immunoperoxidase stains cortisol in adrenal and pituitary. J. Histochem. Cytochem. 26, 909-913.
34. Droste, S. K., de Groote, L., Atkinson, H. C., Lightman,S. L., Reul,J. M. H. M., and Linthorst, A. C. E. (2008). Cor-ticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim test. Endocrinology 149, 3244-3253.
35. Ebner, M. J., Corol, D. I., Havlíková, H., Honour, J. W., and Fry, J. P. (2006). Identification of neu-roactive steroids and their precursors and metabolites in adult male rat brain. Endocrinology 147, 179-190.
36. Edinger, K. L., and Frye, C. A. (2004). Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5α-reduced metabolites in the hippocampus. Behav. Neurosci. 118, 1352-1364.
37. Forlano, P. M., Deitcher, D. L., Myers, D. A., and Bass,A. H. (2001). Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J. Neurosci. 21, 8943-8955.
38. Frye, C. A., Petralia, S. M., and Rhodes, M. E. (2000). Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3α,5α-THP. Pharmacol. Biochem. Behav. 67, 587-596.
39. Garcia-Segura, L. M., Azcoitia, I., and DonCarlos, L. L. (2001). Neuropro-tection by estradiol. Prog. Neurobiol. 63, 29-60.
40. Garcia-Segura, L. M., Wozniak, A., Azcoitia, I., Rodriguez, J. R., Hutchison, R. E., and Hutchison, J. B. (1999). Aromatase expression by astrocytes after brain injury: implications for local estrogen formation in brain repair. Neuroscience 89, 567-578.
41. Gomez-Sanchez, C. E., Zhou, M. Y., Cozza, E. N., Morita, H., Foeck-ing, M. F., and Gomez-Sanchez, E. P. (1997). Aldosterone biosynthesis in the rat brain. Endocrinology 138, 3369-3373.
42. Gomez-Sanchez, E. P., Ahmad, N., Romero, D. G.,and Gomez-Sanchez, C. E. (2005). Is aldosterone syn thesized within the rat brain Am. J. Physiol. Endocrinol. Metab. 288, E342-E346.
43. González-Gil, A., Silván, G., García-Partida, P., and Illera, J. C. (2006). Serum glucocorticoid concentrations after halothane and isoflurane anaesthesia in New Zealand white rabbits. Vet. Rec. 159, 51-52.
44. Goodson, J. L., Saldanha, C. J., Hahn, T. P., and Soma, K. K. (2005). Recent advances in behavioral neuroen-docrinology: insights from studies on birds. Horm. Behav. 48, 461-473.
45. Griffiths,W. J., Jonsson,A. P., Liu, S., Rai, D. K., and Wang, Y. (2001). Electro-spray and tandem mass spectrome-try in biochemistry. Biochem. J. 355, 545-561.
46. Guazzo, E. P., Kirkpatrick, P. J., Goodyer, I. M., Shiers, H. M., and Herbert, J. (1996). Cortisol, dehydroepiandros-terone (DHEA), and DHEA sul-fate in the cerebrospinal fluid of man: relation to blood levels and the effects of age. J. Clin. Endocrinol. Metab. 81, 3951-3960.
47. Guo, T., Taylor, R. L., Singh, R. J., and Soldin, S. J. (2006). Simultaneous determination of 12 steroids by isotope dilution liquid chromatography-photospray ion-ization tandem mass spectrometry. Clin. Chim. Acta 372, 76-82.
48. Hackbarth, H., Küppers, N., and Bohnet, W. (2000). Euthanasia of rats with carbon dioxide - animal welfare aspects. Lab. Anim. 34, 91-96.
49. Hammond, G. L. (1990). Molecular properties of corticosteroid binding globulin and the sex-steroid binding proteins. Endocr. Rev. 11, 65-79.
50. Higashi, T. (2006). Trace determination of steroids causing age-related diseases using LC/MS combined with detection-oriented derivatiza-tion. Chem. Pharm. Bull. (Tokyo) 54, 1479-1485.
51. Higashi, T., and Shimada, K. (2004). Derivatization of neutral steroids to enhance their detection characteristics in liquid chromatography-mass spectrometry. Anal. Bioanal. Chem. 378, 875-882.
52. Higashi, T., Takido, N., and Shi-mada, K. (2005). Studies on neu-rosteroids XVII. Analysis of stress-induced changes in neurosteroid levels in rat brains using liquid chromatography-electron capture atmospheric pressure chemical ionization-mass spectrometry. Steroids 70, 1-11.
53. Higo, S., Hojo, Y., Ishii, Y., Komat-suzaki, Y., Ooishi, Y., Murakami, G., Mukai, H., Yamazaki, T., Naka-hara, D., Barron, A., Kimoto, T., and Kawato, S. (2011). Endogenous synthesis of corticosteroids in the hippocampus. PLoS ONE 6, e21631. doi: 10.1371/journal.pone.0021631
54. Hojo, Y., Hattori, T., Enami, T., Furukawa, A., Suzuki, K., Ishii, H., Mukai, H., Morrison, J. H., Janssen, W. G. M., Kominami, S., Harada, N., Kimoto, T., and Kawato, S. (2004). Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017α andP450aro-matase localized in neurons. Proc. Natl. Acad. Sci. U.S.A. 101, 865-870.
55. Hojo, Y., Higo, S., Ishii, H., Ooishi, Y., Mukai, H., Murakami, G., Kominami, T., Kimoto, T., Honma, S., Poirier, D., and Kawato, S. (2009). Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus. Endocrinology 150, 5106-5112.
56. Holloway, C. C., and Clayton, D. F. (2001). Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat. Neurosci. 4, 170-175.
57. Holson, R. R. (1992). Euthanasia by decapitation: evidence that this technique produces prompt, painless unconsciousness in laboratory rodents. Neurotoxicol. Teratol. 14, 253-257.
58. Jäntti, S. E., Tammimäki, A., Raattamaa, H., Piepponen, P., Kostiainen, R., and Ketola, R. A. (2010). Determination of steroids and their intact glu-curonide conjugates in mouse brain by capillary liquid chromatography-tandem mass spectrometry. Anal. Chem. 82, 3168-3175.
59. Karmarkar, S. W., Bottum, K. M., and Tischkau, S. A. (2010). Considerations for the use of anesthetics in neurotoxicity studies. Comp. Med. 60, 256-262.
60. Karssen, A. M., Meijer, O. C., van der Sandt, I. C. J., Lucassen, P. J., de Lange, E. C. M., de Boer,A. G., and de Kloet, E. R. (2001). Multidrug resistance P-glycoprotein hampers the access of cortisol but not corticos-terone to mouse and human brain. Endocrinology 142, 2686-2694.
61. Kim, S.-B., Hill, M., Kwak, Y.-T., Hampl, R., Jo, D.-H., and Morfin, R. (2003). Neurosteroids: cere-brospinal fluid levels for Alzheimer's disease and vascular dementia diagnostics. J. Clin. Endocrinol. Metab. 88, 5199-5206.
62. Konkle, A. T. M., and McCarthy, M. M. (2011). Developmental time course of estradiol, testosterone, and dihy-drotestosterone levels in discrete regions of male and female rat brain. Endocrinology 152, 223-235.
63. Korneyev, A. Y., Costa, E., and Guidotti, A. (1993a). During anesthetic-induced activation of the hypothal-amic pituitary adrenal axis, blood-borne steroids fail to contribute to the anesthetic effect. Neuroen-docrinology 57, 559-565.
64. Korneyev,A., Pan, B. S., Polo,A., Romeo, E., Guidotti, A., and Costa, E. (1993b). Stimulation of brain preg-nenolone synthesis by mitochon-drial diazepam binding inhibitor receptor ligands in vivo. J. Neu-rochem. 61, 1515-1524.
65. Kretz, O., Fester, L., Wehrenberg, U., Zhou, L., Brauckmann, S., Zhao, S., Prange-Kiel, J., Naumann, T., Jarry, H., Frotscher, M., and Rune, G. M. (2004). Hippocampal synapses depend on hippocampal estrogen synthesis. J. Neurosci. 24, 5913-5921.
66. Krone, N., Hughes, B. A., Lavery, G. G., Steward, P. M., Arlt, W., and Shackleton, C. H. L. (2010). Gas chromatography/mass spectrometry (GC/MS) remains a pre-eminent discovery tool in clinical steroid investigations even in the era of fast liquid chromatography tandem mass spectrometry (LC/MS/MS). J. Steroid Biochem. Mol. Biol. 121, 496-504.
67. Lanthier, A., and Patwardhan, V. V. (1987). Effect of heterosexual olfactory and visual stimulation on 5-en-3β-hydroxysteroids and progesterone in the male rat brain. J. Steroid Biochem. 28, 697-701.
68. Le Goascogne, C., Robel, P., Goué-zou, M., Sananès, N., Baulieu, E.-E., and Waterman, M. (1987). Neurosteroids: cytochrome P-450scc in rat brain. Science 237, 1212-1215.
69. Liere, P., Akwa, Y., Weill-Engerer, S., Eychenne, B., Pianos, A., Robel, P., Sjövall, J., Schumacher, M., and Baulieu, E.-E. (2000). Validation of an analytical procedure to measure trace amounts of neurosteroids in brain tissue by gas chromatography-mass spectrometry. J. Chromatogr. B 739, 301-312.
70. Liere, P., Pianos, A., Eychenne, B., Cam-bourg, A., Bodin, K., Griffiths, W., Schumacher, M., Baulieu, E.-E., and Sjövall, J. (2009). Analysis of preg-nenolone and dehydroepiandros-terone in rodent brain: cholesterol autoxidation is the key. J. Lipid. Res. 50, 2430-2444.
71. Liere, P., Pianos, A., Eychenne, B., Cam-bourg, A., Liu, S., Griffiths, W., Schumacher, M., Sjövall, J., and Baulieu, E.-E. (2004). Novel lipoidal derivatives of pregnenolone and dehy-droepiandrosterone and absence of their sulfated counterparts in rodent brain. J. Lipid Res. 45, 2287-2302.
72. Little, H. J., Croft, A. P., O'Callaghan, M. J. O., Brooks, S. P., Wang, G., and Shaw, S. G. (2008). Selective increases in regional brain glucocor-ticoid: a novel effect of chronic alcohol. Neuroscience 156, 1017-1027.
73. Liu, S., Sjövall, J., and Griffiths, W. J. (2003). Neurosteroids in rat brain: extraction, isolation, and analysis by nanoscale liquid chromatography-electrospray mass spectrometry. Anal. Chem. 75, 5835-5846.
74. London, S. E., Monks, D. A., Wade, J., and Schlinger, B. A. (2006). Widespread capacity for steroid synthesis in the avian brain and song system. Endocrinology 147, 5975-5987.
75. MacLusky, N. J. (2009). Euthanasia in endocrinology: The choices get more complex. Endocrinology 150, 2505-2506.
76. Magariños, A. M., Ferrini, M., and De Nicola, A. F. (1989). Corticosteroid receptors and glucocorticoid content in microdis-sected brain regions: correlative aspects. Neuroendocrinology 50, 673-678.
77. Makin, H. L. J., and Gower, D. B. (2010). Steroid Analysis, 2nd Edn. Dordrecht: Springer.
78. Matsunaga, M., Ukena, K., Baulieu, E.-E., and Tsutsui, K. (2004). 7α-Hydroxypregnenolone acts as a neu-ronal activator to stimulate locomo-tor activity of breeding newts by means of the dopaminergic system. Proc. Natl. Acad. Sci. U.S.A. 101, 17282-17287.
79. Meffre, D., Pianos, A., Liere, P., Eychenne, B., Cambourg, A., Schumacher, M., Stein, D. G., and Guen-noun, R. (2007). Steroid profiling in brain and plasma of male and pseudopregnant female rats after traumatic brain injury: analysis by gas chromatography/mass spectrometry. Endocrinology 148, 2505-2517.
80. Mellon, S. H., and Griffin, L. D. (2002). Neurosteroids: biochemistry and clinical significance. Trends Endocrinol. Metab. 13, 35-43.
81. Mensah-Nyagan, A. G., Feuilloley, M., Do-Rego, J. L., Marcual, A., Lange, C., Tonon, M. C., Pelletier, G., and Vaudry, H. (1996). Localization of 17β-hydroxysteroid dehy-drogenase and characterization of testosterone in the brain of the male frog. Proc. Natl. Acad. Sci. U.S.A. 93, 1423-1428.
82. Mensah-Nyagan, A. G., Saredi, S., Scha-effer, V., Kibaly, C., Meyer, L., Mel-cangi, R. C., and Patte-Mensah, C. (2008). Assessment of neuroactive steroid formation in diabetic rat spinal cord using high-performance liquid chromatography and continuous flow scintillation detection. Neurochem. Int. 52, 554-559.
83. Munetsuna, E., Hojo, Y., Hattori, M., Ishii, H., Kawato, S., Ishida, A., Kom-inami, S. A. J., and Yamazaki, T. (2009). Retinoic acid stimulates 17β-estradiol and testosterone synthesis in rat hippocampal slice cultures. Endocrinology 150, 4260-4269.
84. Murphy, E. J. (2010). Brain fixation for analysis of brain lipid-mediators of signal transduction and brain eicosanoids requires head-focused microwave irradiation: an historical perspective. Prostaglandins Other Lipid Mediat. 91, 63-67.
85. Naftolin, F., Horvath, T. L., Jakab, R. L., Leranth,C., Harada, N., and Balthaz-art, J. (1996). Aromatase immunore-activity in axon terminals of the vertebrate brain. Neuroendocrinol-ogy 63, 149-155.
86. Newman, A. E. M., Chin, E. H., Schmidt, K. L., Bond, L., Wynne-Edwards, K. E., and Soma, K. K. (2008a). Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoas-say. Gen. Comp. Endocrinol. 155, 503-510.
87. Newman, A. E. M., Pradhan, D. S., and Soma, K. K. (2008b). Dehy-droepiandrosterone and corticos-terone are regulated by season and acute stress in a wild songbird: jugular versus brachial plasma. Endocrinology 149, 2537-2545.
88. Newman, A. E. M., and Soma, K. K. (2009). Corticosterone and dehydroepiandrosterone in songbird plasma and brain: effects of season and acute stress. Eur. J. Neurosci. 29, 1905-1914.
89. Newman, A. E. M., and Soma, K. K. (2011). Aggressive interactions differentially modulate local and systemic levels of corticosterone and DHEA in a wild songbird. Horm. Behav. 60, 389-396.
90. O'Callaghan,J.P., andSriram,K. (2004). Focused microwave irradiation of the brain preserves in vivo protein phosphorylation: comparison with other methods of sacrifice and analysis of multiple phosphoproteins. J. Neurosci. Methods 135, 159-168.
91. Ocvirk, R., Bisson, J. M., and Murphy, B. E. P. (2009). Alcohols which have been in contact with any plastics may interfere in radioimmunoassays of progesterone. J. Steroid Biochem. Mol. Biol. 113, 150-154.
92. Palkovits, M. (1973). Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res. 59, 449-450.
93. Pardridge, W. M., and Mietus, L. J. (1979). Transport of steroid hormones through the rat blood-brain barrier. J. Clin. Invest. 64, 145-154.
94. Pesaresi, M., Maschi, O., Giatti, S., Garcia-Segura, L. M., Caruso, D., and Melcangi, R. C. (2010). Sex differences in neuroactive steroid levels in the nervous system of diabetic and non-diabetic rats. Horm. Behav. 57, 46-55.
95. Peterson, R. S., Saldanha, C. J., and Schlinger, B. A. (2001). Rapid upregulation of aromatase mRNA and protein following neural injury in the zebra finch (Taeniopygia guttata). J. Neuroendocrinol. 13, 317-323.
96. Pradhan, D. S., Lau, L. Y., Schmidt, K. L., and Soma, K. K. (2010a). 3β-HSD in songbird brain: subcellu-lar localization and rapid regulation by estradiol. J. Neurochem. 115, 667-675.
97. Pradhan, D. S., Newman, A. E. M., Wacker, D. W., Wingfield, J. C., Schlinger, B. A., and Soma, K. K. (2010b). Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season. Horm. Behav. 57, 381-389.
98. Pradhan, D. S., Yu, Y., and Soma, K. K. (2008). Rapid estrogen regulation of DHEA metabolism in the male and female songbird brain. J. Neurochem. 104, 244-253.
99. Purdy, R. H., Morrow, A. L., Moore, P. H., and Paul, S. M. (1991). Stress-induced elevations of y-aminobutyric acid type A receptor-active steroids in the rat brain. Proc. Natl Acad. Sci. U.S.A. 88, 4553-4557.
100. Rash, J. M., Jerkunica, I., and Sgoutas, D. S. (1980). Lipid interference in steroid radioimmunoassay. Clin. Chem. 26, 84-88.
101. Reburn, C. J., andWynne-Edwards, K. E. (2000). Cortisol and prolactin concentrations during repeated blood sample collection from freely moving, mouse-sized mammals (Phodo-pus spp.). Comp. Med. 50, 184-198.
102. Remage-Healey, L., Maidment, N. T., and Schlinger, B. A. (2008). Fore-brain steroid levels fluctuate rapidly during social interactions. Nat. Neu-rosci. 11, 1327-1334.
103. Rijn, C. M. v., Krijnen, H., Menting-Hermeling, S., and Coenen, A. M. L. (2011). Decapitation in rats: latency to unconsciousness and the "wave of death." PLoS ONE 6, e16514. doi: 10.1371/journal.pone.0016514
104. Robb, D. B., Covey, T. R., and Bruins, A. P. (2000). Atmospheric pressure photoionization: an ionization method for liquid chromatography-mass spectrometry. Anal Chem. 72, 3653-3659.
105. Robel, P., Corpéchot, C, and Baulieu, E.-E. (1973). Testosterone and androstanolone in rat plasma and tissues. FEBS Lett. 33, 218-220.
106. Rosario, E. R., Chang, L., Stanczyk, F. Z., and Pike, C. J. (2004). Age-related testosterone depletion and the development of Alzheimer disease. JAMA 292, 1431-1432.
107. Saalmann, Y. B., Kirkcaldie, M. T. K., Waldron, S., and Calford, M. B. (2007). Cellular distribution of the GABAA receptor-modulating 3a-hydroxy, 5a-reduced pregnane steroids in the adult rat brain. J. Neuroendocrinol. 19,272-284.
108. Sakamoto, H., Ukena, K., and Tsut-sui, K. (2001a). Activity and localization of 3|3-hydroxysteroid dehydrogenase/A5-A4-isomerase in the zebrafish central nervous system. J. Comp. Neurol 439, 291-305.
109. Sakamoto, H., Ukena, K., and Tsutsui, K. (2001b). Effects of progesterone synthesized de novo in the developing Purkinje cell on its dendritic growth and synaptogenesis. J. Neurosci. 21, 6221-6232.
110. Saldanha, C. J., Duncan, K. A., and Walters, B. J. (2009). Neuroprotective actions of brain aromatase. Front. Neuroendocrinol. 30:106-118. doi: 10.1016/j.yfrne.2009.04.016
111. Saldanha, C. J., Remage-Healey, L., and Schlinger, B. A. (2011). Synap-tocrine signaling: steroid synthesis and action at the synapse. Endocr. Rev. 32, 532-549.
112. Saldanha, C. J., and Schlinger, B. A. (1997). Estrogen synthesis and secretion in the brown-headed cowbird (Molothrus ater). Gen. Comp. Endocrinol. 105, 390-401.
113. Saldanha, C. J., Tuerk, M. J., Kim, Y.-H., Fernandes, A. O., Arnold, A. P., and Schlinger, B. A. (2000). Distribution and regulation of telen-cephalic aromatase expression in the zebra finch revealed with a specific antibody. J. Comp. Neurol. 423, 619-630.
114. Saldanha, C. J., Walters, B. J., and Fraley, G. S. (2010). Neurons that co-localize aromatase- and kisspeptin-like immunoreactivity may regulate the HPG axis of the Mallard drake (Anas platyrhyn-chos). Gen. Comp. Endocrinol. 166, 606-613.
115. Saleh, T. M., Connell, B. J.,Legge, C., and Cribb, A. E. (2004). Stroke-induced changes in estrogen release and neu-ronal activity in the parabrachial nucleus of the male rat. J. Stroke Cerebrovasc. Dis. 13, 24-34.
116. Santa, T. (2011). Derivatization reagents in liquid chromatog-raphy/electrospray ionization tandem mass spectrometry. Biomed. Chromatogr. 25, 1-10.
117. Schlinger, B. A., Amur-Umarjee, S., Shen, P., Campagnoni, A. T., and Arnold, A. P. (1994). Neuronal and non-neuronal aromatase in primary cultures of developing zebra finch telencephalon. J. Neurosci. 14, 7541-7552.
118. Schlinger, B. A., and Arnold, A. P. (1992). Circulating estrogens in a male songbird originate in the brain. Proc. Natl. Acad. Sci. U.S.A. 89, 7650-7653.
119. Schlinger, B. A., and Arnold, A. P. (1993). Estrogen synthesis in vivo in the adult zebra finch: additional evidence that circulating estrogens can originate in brain. Endocrinology 133, 2610-2616.
120. Schmidt, K. L., Pradhan, D. S., Shah, A. H., Charlier, T. D., Chin, E. H., and Soma, K. K. (2008). Neurosteroids, immunosteroids, and the Balkaniza-tion of endocrinology. Gen. Comp. Endocrinol. 157, 266-274.
121. Schmidt, K. L., and Soma, K. K. (2008). Cortisol and corticosterone in the songbird immune and nervous systems: local vs. systemic levels during development. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R103- R110.
122. Schumacher, M., Liere, P., Akwa, Y., Rajkowski, K., Griffiths, W., Bodin, K., Sjövall, J., and Baulieu, E.-E. (2008). Pregnenolone sul-fate in the brain: a controversial neurosteroid. Neurochem. Int. 52, 522-540.
123. Scott, A. P., and Ellis, T. (2007). Measurement of fish steroids in water-a review. Gen. Comp. Endocrinol. 153, 392-400.
124. Soldin, S. J., and Soldin, O. P. (2009). Steroid hormone analysis by tandem mass spectrometry. Clin. Chem. 55, 1061-1066.
125. Soma, K. K. (2006). Testosterone and aggression: Berthold, birds and beyond. J. Neuroendocrinol. 18, 543-551.
126. Soma, K. K., Alday, N. A., Hau, M., and Schlinger, B. A. (2004). Dehydroepiandrosterone metabolism by 3ß-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase in adult zebra finch brain: sex differences and rapid effect of stress. Endocrinology 145, 1668-1677.
127. Soma, K. K., Scotti, M.-A., Newman, A. E. M., Charlier, T. D., and Demas, G. E. (2008). Novel mechanisms for neuroendocrine regulation of aggression. Front. Neuroendocrinol. 29:476-489. doi: 10.1016/j.yfrne.2007.12.003
128. Soma, K. K., Sinchak, K., Lakhter, A., Schlinger, B. A., and Micevych, P. E. (2005). Neurosteroids and female reproduction: estrogen increases 3β-HSD mRNA and activity in rat hypothalamus. Endocrinology 146, 4386-4390.
129. Soma, K. K., and Wingfield, J. C. (2001). Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression. Gen. Comp. Endocrinol. 123, 144-155.
130. Sorrells, S. F., and Sapolsky, R. M. (2009). The stressed CNS: when glu-cocorticoids aggravate inflammation. Neuron 64, 33-39.
131. Stanczyk, F. Z., and Clarke, N. J. (2010). Advantages and challenges of mass spectrometry assays for steroid hormones. J. Steroid Biochem. Mol. Biol. 121, 491-495.
132. Stoffel-Wagner, B. (2001). Neurosteroid metabolisminthe human brain.Eur. J. Endocrinol. 145, 669-679.
133. Takase, M., Ukena, K., Yamazaki, T., Kominami, S., and Tsutsui, K. (1999). Pregnenolone, preg-nenolone sulfate, and cytochrome P450 side-chain cleavage enzyme in the amphibian brain and their seasonal changes. Endocrinology 1936-1944.
134. Taves, M. D., Gomez-Sanchez, C. E., and Soma, K. K. (2011). Extra-adrenal glucocorticoids and miner-alocorticoids: evidence for local synthesis, regulation, and function. Am. J. Physiol. Endocrinol. Metab. 301, E11-E24.
135. Taves, M. D., Schmidt, K. L., Ruhr, I. M., Kapusta, K., Prior, N. H., and Soma, K. K. (2010). Steroid concentrations in plasma, whole blood and brain: effects of saline perfusion to remove blood contamination from brain. PLoS ONE 5, e15727. doi: 10.1371/journal.pone.0015727
136. Telepchak, M. J., August, T. F., and Chaney, G. (2004). Forensic and Clinical Applications of Solid Phase Extraction. Totowa: Humana.
137. Tokuda, K., Izumi, Y., and Zorumski, C. F. (2011). Ethanol enhances neurosteroidogenesis in hip-pocampal pyramidal neurons by paradoxical NMDA receptor activation. J. Neurosci. 31, 9905-9909.
138. Toran-Allerand, C. D., Tinnikov, A. A., Singh, R. J., and Nethrapalli, I. S. (2005). 17α-Estradiol: a brain-active estrogen Endocrinology 146, 3843-3850.
139. Tsutsui, K., Ukena, K., Usui, M., Sakamoto, H., and Takase, M. (2000). Novel brain function: biosynthesis and actions of neuros-teroids in neurons. Neurosci. Res. 36, 261-273.
140. Vallée, M., Rivera, J. D., Koob, G. F., Purdy, R. H., and Fitzgerald, R. L. (2000). Quantification of neurosteroids in rat plasma and brain following swim stress and allopregnanolone administration using negative chemical ion-ization gas chromatography/mass spectrometry. Anal. Biochem. 287, 153-166.
141. von Schoultz, E., Bixo, M., Bäckström, T., Silfvenius, H., Wilking, N., and Henriksson, R. (1990). Sex steroids in human brain tumors and breast cancer. Cancer 65, 949-952.
142. Wang, M.-D., Wahlström, G., and Bäckström, T. (1997). The regional brain distribution of the neuros-teroids pregnenolone and preg-nenolone sulfate following intravenous infusion. J. Steroid Biochem. Mol. Biol. 62, 299-306.
143. Wang, Y., Karu, K., and Griffiths, W. J. (2007). Analysis of neurosterols and neurosteroidsbymass spectrometry. Biochimie 89, 182-191.
144. Washburn, B. E., Morris, D. L., Millspaugh, J. J., Faaborg, J., and Schulz, J. H. (2002). Using a commercially available radioimmunoas-say to quantify corticosterone in avian plasma. Condor 104, 558.
145. Wingfield, J. C., and Farner, D. S. (1975). The determination of five steroids in avian plasma by radioim-munoassay and competitive protein-binding. Steroids 26, 311-321.
146. Wong, S., Dykstra, M., Campbell, J. M., and Earley, R. L. (2008). Measuring water-borne cortisol in convict cich-lids (Amatitlania nigrofasciata): is the procedure a stressor Behaviour 145, 1283-1305.
147. Wynne, R. D., Walters, B. J., Bailey, D. J., and Saldanha, C. J. (2008). Inhibition of injury-induced glial aro-matase reveals a wave of secondary degeneration in the songbird brain. Glia 56, 97-105.
148. Yu, L., Romero, D. G., Gomez-Sanchez, C. E., and Gomez-Sanchez, E. P. (2002). Steroidogenic enzyme gene expression in the human brain. Mol. Cell. Endocrinol. 190, 9-17.
149. Zwain, I. H., and Yen, S. S. C. (1999). Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140, 3843-3852.