Songbirds: A novel perspective on estrogens and the aging brain
Tóm tắt
Songbirds perform some remarkable feats of memory, including forming memories for songs and for complex spatial features of their environments. Research into the neural and hormonal control of these behaviors reveals discrete circuits that can retain considerable plasticity in adulthood. The songbird brain is also a prominent site of estrogen synthesis and a target of estrogen action. Estrogens contribute to the plasticity of the adult songbird brain and contribute to the bird's capacity to form and retrieve some memories. We describe the brain, behavior and endocrinology of songbirds and discuss these findings within the context of the neurology of the aging brain.
Tài liệu tham khảo
Allolio B and Arlt W (2002) DHEA treatment: myth or reality? Trends Endocrinol Metab 13: 288–294
Altman J (1962) Are new neurons formed in the brains of adult mammals? Science 135: 1127–1128
Alvarez-Buylla A and Nottebohm F (1988) Migration of young neurons in adult avian brain. Nature 335: 353–354
Alvarez-Buylla A, Theelen M and Nottebohm F (1990a) Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron 5: 101–109
Alvarez-Buylla A, Kirn JR and Nottebohm F (1990b) Birth of projection neurons in adult avian brain may be related to perceptual or motor learning [published erratum appears in Science 1990 Oct 19; 250(4979):360]. Science 249: 1444–1446
Balthazart J and Ball GF (1998) New insights into the regulation and function of brain estrogen synthase (aromatase). Trends Neurosci 21: 243–249
Balthazart J, Tlemcani O and Ball GF (1996) Do sex differences in the brain explain sex differences in the hormonal induction of reproductive behavior? What 25 years of research on the Japanese Quail tells us. Horm Behav 30: 627–661
Barnea A and Nottebohm F (1996) Recruitment and replacement of hippocampal neurons in young and adult chickadees: An addition to the theory of hippocampal learning. Proc Nat Acad Sci USA 93: 714–718
Bednekoff PA, Balda RP, Kamil AC and Hile AG (1997) Long-term spatial memory in four seed-caching corvid species. Anim Behav 53: 335–341
Berthold P, Gwinner E and Sonnenschein E (eds) (2003) Avian Migration. Berlin, Heidelberg, New York: Springer
Bingman VP and Able KP (2002) Maps in birds: representational mechanisms and neural bases. Curr Opin Neurobio 12: 745–750
Bottjer SW and Johnson F (1997) Circuits, hormones, and learning: vocal behavior in songbirds. J Neurobiol 33: 602–618
Brainard MS and Doupe AJ (2002) What songbirds teach us about learning. Nature 417: 351–358
Brown SD, Johnson F and Bottjer SW (1993) Neurogenesis in adult canary telencephalon is independent of gonadal hormone levels. J. Neuroscience 13: 2024–2032
Callard GV (1984) Aromatization in brain and pituitary: an evolutionary prespective. In: Celotti F, Naftolin F and Martini L (eds). Metabolism of Hormonal Steroids in the Neuroendocrine Structures, pp. 79–102. Raven, NY
Callard GV, Drygas M and Gelinas D (1993) Molecular and cellular physiology of aromatase in the brain and retina. J Steroid Biochem Mol Biol 44: 541–547
Canick JA, Vaccaro DE, Livingston EM, Leeman SE, Ryan KJ and Fox TO (1986) Localization of aromatase and 5 alpha-reductase to neuronal and non-neuronal cells in the fetal rat hypothalamus. Brain Res 372: 277–282
Clayton N (2002) Brain, perception, memory: Advances in cognitive neuroscience. Q J Exp Psychol B-Comp Physiol Psychol 55: 191–192
Dittrich F, Feng Y, Metzdorf R and Gahr M (1999) Estrogen-inducible, sex-specific expression of brain-derived neurotrophicfactor mRNA in a forebrain song control nucleus of the juvenile zebra finch. Proc Natl Acad Sci USA 96: 8241–8246
Erickson KI, Colcombe SJ, Raz N, Korol DL, Scalf P and Webb A et al. (2005) Selective sparing of brain tissue in postmenopausal women receiving hormone replacement therapy. Neurobiol Aging 26: 1205–1213
Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn A, Norborg C and Peterson DA et al. (1998) Neurogenesis in the adult human hippocampus. Nat Med 4: 1313–1317
Forlano PM, Deitcher DL, Myers DA and Bass AH (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
Gahr M (2004) Hormone-dependent neural plasticity in the juvenile and adult song system – What makes a successful male? In: Behavioral Neurobiology of Birdsong, pp 684–703
Garcia-Segura LM, Wozniak A, Azcoitia I, Rodriguez JR, Hutchison RE and Hutchison JB (1999) Aromatase expression by astrocytes after brain injury: implications for local estrogen formation in brain repair. Neurosci 89: 567–578
Garcia-Segura LM, Veiga S, Sierra A, Melcangi RC and Azcoitia I (2003) Aromatase: a neuroprotective enzyme. Prog Neurobiol 71: 31–41
Gibson BM and Kamil AC (2005) The fine-grained spatial abilities of three seed-caching corvids. Learn Behav 33: 59–66
Goldman SA (1990) Neuronal development and migration in explant cultures of the adult canary forebrain. J Neurosci 10: 2931–2939
Goldman SA and Nottebohm F (1983) Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA 80: 2390–2394
Goldman SA and Nedergaard M (1992) Newly generated neurons of the adult songbird brain become functionally active in long-term culture. Dev Brain Res 68: 217–223
Goldman SA, Zaremba A and Niedzwiecki D (1992) In vitro neurogenesis by neuronal precursor cells derived from the adult songbird brain. J Neurosci 12: 2532–2541
Goodson J, Saldanha C, Hahn T and Soma K (2005) Recent advances in behavioral neuroendocrinology: Insights from studies on birds. Horm. Behav. 48: 461–473
Gould E and Gross CG (2002) Neurogenesis in adult mammals: Some progress and problems. J Neurosci 22: 619–623
Gould E, Woolley CS, Frankfurt M and McEwen BS (1990) Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10: 1286–1291
Hajszan T, Maclusky NJ and Leranth C (2004) Dehydroepiandrosterone increases hippocampal spine synapse density in ovariectomized female rats. Endocrinol 145: 1042–1045
Hampton RR and Shettleworth SJ (1996) Hippocampal lesions impair memory for location but not color in passerine birds. Behav Neurosci 110: 831–835
Healy SD and Suhonen J (1996) Memory for locations of stored food in willow tits and marsh tits. Behav 133: 71–80
Hidalgo A, Barami K, Iversen K and Goldman SA (1995a) Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J Neurobiol 27: 470–487
Hidalgo A, Barami K, Iversen K and Goldman SA (1995b) Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J Neurobiol 27: 470– 487
Holloway CC and Clayton DE (2001) Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat Neurosci V4: 170–175
Hoshooley JS and Sherry DF (2004) Neuron production, neuron number, and structure size are seasonally stable in the hippocampus of the food-storing black-capped chickadee (Poecile atricapillus). Behav Neurosci 118: 345–355
Hung AJ, Stanbury MG, Shanabrough M, Horvath TL, Garcia-Segura LM and Naftolin F (2003) Estrogen, synaptic plasticity andhypothalamic reproductive aging. Exp Gerontol 38: 53–59
Iivonen S, Corder E, Lehtovirta M, Helisalmi S, Mannermaa A and Vepsalainen S et al. (2004) Polymorphisms in the CYP19 gene confer increased risk for Alzheimer disease. Neurol 62: 1170–1176
Kirn JR and Nottebohm F (1993) Direct evidence for loss and replacement of projection neurons in adult canary brain. J Neurosci 13: 1654–1663
Kirn J, O'Loughlin B, Kasparian S and Nottebohm F (1994) Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song [see comments]. Proc Natl Acad Sci USA 91: 7844– 7848
Kretz O, Fester L, Wehrenberg U, Zhou LP, Brauckmann S and Zhao ST et al. (2004) Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 24: 5913–5921
Lephart ED (1996) A review of brain aromatase cytochrome P450. Brain Res. Revs. 22: 1–26
London SE, Boulter J and Schlinger BA (2003) Cloning of the zebra finch androgen synthetic enzyme CYP17: A study of its neural expression throughout posthatch development. J Comp Neurol 467(4): 496–508
Lu SF, Mo QX, Hu S, Garippa C and Simon NG (2003) Dehydroepiandrosterone upregulates neural androgen receptor level and transcriptional activity. J Neurobiol 57: 163–171
Marler P (1997) Three models of song learning: Evidence from behavior. J Neurobiol 33: 501–516
Moller AQ, Pavlick B, Hile AG and Balda RP (2001) Clark's nutcrackers Nucifraga columbiana remember the size of their cached seeds. Ethol 107: 451–461
Naftolin F, Ryan KJ and Petro Z (1971) Aromatization of androstenedione by limbic system tissue from human foetuses. J Endocrinol 51: 795–796
Nottebohm F (1981) A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 214: 1368–1370
Nottebohm F (1996) The King Solomon Lectures in Neuroethology. A white canary on Mount Acropolis. J Comp Physiol A 179: 149–156
Nottebohm F (2002) Neuronal replacement in adult brain. Brain Res Bull 57: 737–749
Nottebohm F (2004) The road we travelled – Discovery, choreography, and significance of brain replaceable neurons. In: Behavioral Neurobiology of Birdsong, pp 628–658
Oberlander JG, Schlinger BA, Clayton NS and Saldanha CJ (2004) Neural aromatization accelerates the acquisition of spatial memory via an influence on the songbird hippocampus. Horm Behav 45: 250–258
Pasmanik M and Callard GV (1985) Aromatase and 5-Alpha-Reductase in the Teleost Brain, Spinal Cord, and Pituitary Gland. Gen Comp Endocrinol 60: 244–251
Paton JA and Nottebohm FN (1984) Neurons generated in the adult brain are recruited into functional circuits. Science 225: 1046–1048
Perrini S, Laviola L, Nataliccio A and Giorgino F (2005) Associated hormonal declines in aging: DHEAS. J Endocrinol Invest 28: 2885–2893
Peterson RS, Saldanha CJ and Schlinger BA (2001) Rapid upregulation of aromatase mRNA and protein following neural injury in the zebra finch (Taeniopygia guttata). J Neuroendocrinol 13: 317–323
Peterson RS, Lee DW, Fernando G and Schlinger BA (2004) Radial glia express aromatase in the injured zebra finch brain. J Comp Neurol 480: 261–269
Peterson RS, Yarram L, Schlinger BA and Saldanha CJ (2005) Aromatase is Presynaptic and Sexually Dimorphic in the Adult Zebra Finch Brain. Proc Roy Soc Lond B 272: 2089–2096
Prather J and Mooney R (2004) Neural correlates of learned song in the avaian forebrain: simultaneous representation of self and others. Curr Opin Neurobiol 14: 496–502
Roselli CE and Resko JA (2001) Cytochrome P450 aromatase (CYP19) in the non-human primate brain: distribution, regulation, and functional significance. J Steroid Biochem Mol Biol 79: 247–253
Saldanha CJ, Popper P, Micevych PE and Schlinger BA (1998) The passerine hippocampus is a site of high aromatase: Inter- and intraspecies comparisons. Horm Behav 34: 85–97
Saldanha CJ, Clayton NS and Schlinger BA (1999) Androgen metabolism in the juvenile oscine forebrain: a cross-species analysis at neural sites implicated in memory function. J Neurobiol 40: 397–406
Saldanha CJ, Tuerek MJ, Kim Y-H, Fernandes AO, Arnold AP and Schlinger BA (2000) Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific anitbody. J Comp Neurol 423: 619–630.
Saldanha C, Patel N, Randall J and Kullar R (2004a) Orthogonal patterns of neuroplasticity in the hippocampus and song circuitof a food storing songbird. Soc Neurosci Abstracts 554: 18
Saldanha CJ, Schlinger BA, Micevych PE and Horvath TL (2004b) Presynaptic N-methyl-D-aspartate receptor expression is increased by estrogen in an aromatase-rich area of the songbird hippocampus. J Comp Neurol 469: 522–534
Saldanha CJ, Rohmann KN, Coomaralingam L and Wynne RD (2005) Estrogen provision by reactive glia decreases apoptosis in the zebra finch (Taeniopygia guttata). J Neurobiol 64: 192–201
Schlinger BA (1995) Estrogen synthesis and secretion by the songbird brain. In: Micevych PE and Hammer RP Jr (eds). Neurobiological Effects of Sex Steroid Hormones. Cambridge: Cambridge University Press
Schlinger BA (1997) Sex steroids and their actions on the birdsong system. J Neurobiol 33: 619–631
Schlinger BA and Brenowitz EA (2002) Neural and hormonal control of birdsong. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, (eds) Hormones, Brain and Behavior, pp 799–839. Amsterdam: Academic
Schlinger BA, Amur-Umarjee S, Shen P, Campagnoni AT and Arnold AP (1994) Neuronal and non-neuronal aromatase in primary cultures of developing zebra finch telencephalon. J Neurosci 14: 7541–7552
Shen P, Schlinger BA, Campagnoni AT and Arnold AP (1995) An atlas of aromatase mRNA expression in the zebra finch brain. J Comp Neurol 360: 172–184
Sherry DF and Duff SJ (1996) Behavioural and neural bases of orientation in food-storing birds. J. Exp. Bio. 199: 165–171
Shettleworth SJ, Hampton RR and Westwood RP (1995) Effects ofseason and photoperiod on food storing by black-capped chickadees, Parus atricapillus. Anim Behav 49: 989–998
Smulders TV, Sasson AD and DeVoogd TJ (1995) Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. J Neurobiol 27: 15–25
Smulders TV, Shiflett MW, Sperling AJ and DeVoogd TJ (2000) Seasonal changes in neuron numbers in the hippocampal formation of a food-hoarding bird: The black-capped chickadee. J Neurobiol 44: 414–422
Sohrabji F, Miranda RC and Toran-Allerand CD (1994) Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J Neurosci 14: 459– 471
Soma KK and Wingfield JC (2001) Dehydroepiandrosterone in songbird plasma: Seasonal regulation and relationship to territorial aggression. Gen Comp Endocrinol 123: 144–155
Soma KK, Bindra RK, Gee J, Wingfield JC and Schlinger BA (1999) Androgen-metabolizing enzymes show region-specific changes across the breeding season in the brain of a wild songbird. J Neurobiol 41: 176–188
Soma KK, Wissman AM, Brenowitz EA and Wingfield JC (2002) Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird. Horm Behav 41: 203–212
Soma KK, Schlinger BA, Wingfield JC and Saldanha CJ (2003) Brain aromatase, 5 alpha-reductase, and 5 beta-reductase change seasonally in wild male song sparrows: Relationship to aggressive and sexual behavior. J Neurobiol 56: 209–221
Soma KK, Alday NA and Schlinger BA (2004) DHEA Metabolism by 3b-HSD in Adult Zebra Finch Brain: Sex Difference and Rapid Effect of Stress. Endocrinol 145: 1668–1677
Tramontin AD and Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23: 251–258
Tramontin AD, Wingfield JC and Brenowitz EA (2003) Androgens and estrogens induce seasonal-like growth of song nuclei in the adult songbird brain. J Neurobiol 57: 130–140
Vanson A, Arnold AP and Schlinger BA (1996) 3 beta-hydroxysteroid dehydrogenase/isomerase and aromatase activity in primary cultures of developing zebra finch telencephalon: dehydroepiandrosterone as substrate for synthesis of androstenedione and estrogens. Gen Comp Endocrinol 102: 342–350
Vockel A, Pröve E and Balthazart J (1990) Sex- and age-related differences in the activity of testosterone-metabolizing enzymes in microdissected nuclei of the zebra finch brain. Brain Res 511: 291–302
Wang N, Aviram R and Kirn JR (1999) Deafening alters neuron turnover within the telencephalic motor pathway for song control in adult zebra finches. J Neurosci 19: 10554–10561.
Wang NG, Hurley P, Pytte C and Kirn JR (2002) Vocal control neuron incorporation decreases with age in the adult zebra finch. J. Neurosci. 22: 10864–10870
White SA, Livingston FS and Mooney R (1999) Androgens modulate NMDA receptor-mediated EPSCs in the zebra finch song system. J Neurophysiol 82: 2221–2234
Wise PM (2002) Estrogens and neuroprotection. Trends Endocrinol. Metabol. 13: 229–230
Wise PM and Dubal DB (2000) Estradiol protects against ischemic brain injury in middle-aged rats. Biol Reprod 63: 982–985
Wynne RD and Saldanha CJ (2004) Glial aromatization decreases neural injury in the zebra finch (Taeniopygia guttata): Influence on apoptosis. J Neuroendocrinol 16: 676–683
Wynne RD, Coomaralingam L, Rohmann KN and Saldanha CJ (2004) Locally synthesized estradiol via glial aromatization decreases neural injury in the zebra finch. Horm Behav 46: 124
Zwain IH, Yen SSC and Cheng CY (1997) Astrocytes cultured in vitro produce estradiol-17 beta and express aromatase cytochrome P-450 (P-450 AROM) mRNA. Biochimica Et Biophysica Acta – General Subjects 1334: 338–348