雌激素对鸣禽中枢神经系统的调控作用
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摘要
鸣禽是研究人类语言学习与产生的重要模式动物。鸣禽鸣唱需要感知和运动技能学习等神经过程的参与。鸣禽脑内的雌激素主要是雌二醇(estradiol, E2),由脑内睾酮(testosterone, T)通过芳香化酶的作用转化而来。目前已在雌激素对鸣禽中枢神经系统的调控作用方面获得了一系列重要成果,主要集中在雌激素对鸣禽听觉编码、脑损伤修复,以及空间记忆和鸣唱行为的调控作用。该文对雌激素调控鸣禽中枢神经系统进展进行论述。
Songbirds are important model animals for studying human language learning and production. Neural processes such as perception and motor skill learning are participated in singing. Estrogens in the brain of songbirds are mainly estradiol(E2), which is transformed by neural testosterone(T) through aromatase. A series of important results were achieved in the regulation of estrogen on the central nervous system of songbirds, mainly focusing on the regulation of estrogen on auditory coding, brain damage repair, spatial memory and singing behavior of songbirds. The progress of estrogen regulation in the central nervous system of songbirds is discussed in this paper.
Songbirds are important model animals for studying human language learning and production. Neural processes such as perception and motor skill learning are participated in singing. Estrogens in the brain of songbirds are mainly estradiol(E2), which is transformed by neural testosterone(T) through aromatase. A series of important results were achieved in the regulation of estrogen on the central nervous system of songbirds, mainly focusing on the regulation of estrogen on auditory coding, brain damage repair, spatial memory and singing behavior of songbirds. The progress of estrogen regulation in the central nervous system of songbirds is discussed in this paper.
引文
[1]Prather J,Okanoya K,Bolhuis JJ.Brains for birds and babies:neural parallels between birdsong and speech acquisition.Neurosci Biobehav Rev,2017,81:225-37
[2]Lynch KS,Louder MIM,Hauber ME.Species-specific auditory forebrain responses to non-learned vocalizations in juvenile blackbirds.Brain Behav Evol,2018,91:193-200
[3]Xiao L,Chattree G,Oscos FG,et al.A basal ganglia circuit sufficient to guide birdsong learning.Neuron,2018,98:208-221.e5
[4]Pawlisch BA,Remage-Healey L.Neuroestrogen signaling in the songbird auditory cortex propagates into a sensorimotor network via an‘interface’nucleus.Neuroscience,2015,284:522-35
[5]Wang S,Liao C,Li F,et al.Castration modulates singing patterns and electrophysiological properties of RA projection neurons in adult male zebra finches.Peer J,2014,2:e352
[6]Dieni CV,Ferraresi A,Sullivan JA,et al.Acute inhibition of estradiol synthesis impacts vestibulo-ocular reflex adaptation and cerebellar long-term potentiation in male rats.Brain Struct Funct,2018,223:837-50
[7]Pedersen AL,Saldanha CJ.Reciprocal interactions between prostaglandin E2-and estradiol-dependent signaling pathways in the injured zebra finch brain.J Neuroinflammation,2017,14:262
[8]Bailey DJ,Makeyeva YV,Paitel ER,et al.Hippocampal aromatization modulates spatial memory and characteristics of the synaptic membrane in the male zebra finch.Endocrinology,2017,158:852-9
[9]Charlier TD,Po KW,Newman AE,et al.17β-estradiol levels in male zebra finch brain:combining Palkovits punch and an ultrasensitive radioimmunoassay.Gen Comp Endocrinol,2010,167:18-26
[10]Acharya KD,Veney SL.Characterization of the G-protein-coupled membrane-bound estrogen receptor GPR30 in the zebra finch brain reveals a sex difference in gene and protein expression.Dev Neurobiol,2012,72:1433-46
[11]Frankl-Vilches C,Gahr M.Androgen and estrogen sensitivity of bird song:a comparative view on gene regulatory levels.J Comp Physiol A:Neuroethol Sens Neural Behav Physiol,2018,204:113-26
[12]Hadjimarkou MM,Vasudevan N.GPER1/GPR30 in the brain:Crosstalk with classical estrogen receptors and implications for behavior.J Steroid Biochem Mol Biol,2018,176:57-64
[13]Bailey DJ,Saldanha CJ.The importance of neural aromatization in the acquisition,recall,and integration of song and spatial memories in passerines.Horm Behav,2015,74:116-24
[14]Vahaba DM,Remage-Healey L.Neuroestrogens rapidly shape auditory circuits to support communication learning and perception:evidence from songbirds.Horm Behav,2018,104:77-87
[15]Yoder KM,Lu K,Vicario DS.Blocking estradiol synthesis affects memory for songs in auditory forebrain of male zebra finches.Neuroreport,2012,23:922-6
[16]Lattin CR,Stabile FA,Carson RE.Estradiol modulates neural response to conspecific and heterospecific song in female house sparrows:an in vivo positron emission tomography study.PLoS One,2017,12:e0182875
[17]Calisi RM,Knudsen DP,Krause JS,et al.Estradiol differentially affects auditory recognition and learning according to photoperiodic state in the adult male songbird,European starling(Sturnus vulgaris).Peer J,2013,1:e150
[18]Sanford SE,Lange HS,Maney DL.Topography of estradiol-modulated genomic responses in the songbird auditory forebrain.Dev Neurobiol,2010,70:73-86
[19]Chao A,Paon A,Remage-Healey L.Dynamic variation in forebrain estradiol levels during song learning.Dev Neurobiol,2015,75:271-86
[20]Korol DL,Pisani SL.Estrogens and cognition:friends or foes?an evaluation of the opposing effects of estrogens on learning and memory.Horm Behav,2015,74:105-15
[21]Vahaba DM,Remage-Healey L.Brain estrogen production and the encoding of recent experience.Curr Opin Behav Sci,2015,6:148-53
[22]De Groof G,Balthazart J,Cornil CA,et al.Topography and lateralized effect of acute aromatase inhibition on auditory processing in a seasonal songbird.J Neurosci,2017,37:4243-54
[23]Vahaba DM,Macedo-Lima M,Remage-Healey L.Sensory coding and sensitivity to local estrogens shift during critical period milestones in the auditory cortex of male songbirds.eNeuro,2017,4:pii:ENEURO.0317-17.2017
[24]Remage-Healey L,Coleman MJ,Oyama RK,et al.Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird.Proc Natl Acad Sci USA,2010,107:3852-7
[25]Yoder KM,Phan ML,Lu K,et al.He hears,she hears:are there sex differences in auditory processing?Dev Neurobiol,2015,75:302-14
[26]Tremere LA,Jeong JK,Pinaud R.Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression.JNeurosci,2009,29:5949-63
[27]Pinaud R,Terleph TA,Tremere LA,et al.Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain.J Neurophysiol,2008,100:441-55
[28]Caras ML,O’Brien M,Brenowitz EA,et al.Estradiol selectively enhances auditory function in avian forebrain neurons.J Neurosci,2012,32:17597-611
[29]Pedersen AL,Brownrout JL,Saldanha CJ.Neuroinflammation and neurosteroidogenesis:reciprocal modulation during injury to the adult zebra finch brain.Physiol Behav,2018,187:51-6
[30]Pedersen AL,Nelson LH,Saldanha CJ.Centrally synthesized estradiol is a potent anti-inflammatory in the injured zebra finch brain.Endocrinology,2016,157:2041-51
[31]Pedersen AL,Saldanha CJ.Reciprocal interactions between prostaglandin E2-and estradiol-dependent signaling pathways in the injured zebra finch brain.J Neuroinflammation,2017,14:262
[32]Pedersen AL,Gould CJ,Saldanha CJ.Activation of the peripheral immune system regulates neuronal aromatase in the adult zebra finch brain.Sci Rep,2017,7:10191
[33]Mehos CJ,Nelson LH,Saldanha CJ.A quantification of the injury-induced changes in central aromatase,oestrogenic milieu and steroid receptor expression in the zebra finch.J Neuroendocrinol,2016,28:12348
[34]Ikeda MZ,Krentzel AA,Oliver TJ,et al.Clustered organization and region-specific identities of estrogen-producing neurons in the forebrain of zebra finches(Taeniopygia guttata).J Comp Neurol,2017,525:3636-52
[35]Bailey DJ,Ma C,Soma KK,et al.Inhibition of hippocampal aromatization impairs spatial memory performance in a male songbird.Endocrinology,2013,154:4707-14
[36]Roth TC 2nd,Stocker K,Mauck R.Morphological changes in hippocampal cytoarchitecture as a function of spatial treatment in birds.Dev Neurobiol,2017,77:93-101
[37]Luine V,Serrano P,Frankfurt M.Rapid effects on memory consolidation and spine morphology by estradiol in female and male rodents.Horm Behav,2018,104:111-8
[38]Hamaide J,De Groof G,Van Ruijssevelt L,et al.Volumetric development of the zebra finch brain throughout the first200 days of post-hatch life traced by in vivo MRI.Neuroimage,2018,183:227-38
[39]Martin LC,Veney SL.The specific estrogen receptor antagonist ICI 182,780 masculinizes development of the zebra finch syrinx.Gen Comp Endocrinol,2008,156:434-9
[40]Grisham W,Lee J,Park SH,et al.A dose-response study of estradiol’s effects on the developing zebra finch song system.Neurosci Lett,2008,445:158-61
[41]Wade J,Arnold AP.Sexual differentiation of the zebra finch song system.Ann N Y Acad Sci,2004,1016:540-59
[42]Holloway CC,Clayton DF.Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro.Nat Neurosci,2001,4:170-5
[43]Beach LQ,Wade J.Masculinisation of the zebra finch song system:roles of oestradiol and the Z-chromosome gene tubulin-specific chaperone protein A.J Neuroendocrinol,2015,27:324-34
[44]Wade J,Peabody C,Tang YP,et al.Estradiol modulates neurotransmitter concentrations in the developing zebra finch song system.Brain Res,2013,1517:87-92
[45]Alward BA,de Bournonville C,Chan TT,et al.Aromatase inhibition rapidly affects in a reversible manner distinct features of birdsong.Sci Rep,2016,6:32344
[46]Wang S,Meng W,Liu S,et al.Sex differences of excitatory synaptic transmission in RA projection neurons of adult zebra finches.Neurosci Lett,2014,582:75-80
[47]Chen Q,Zhang X,Zhao Y,et al.Sexual differences in cell proliferation in the ventricular zone,cell migration and differentiation in the HVC of juvenile Bengalese finch.PLoS One,2014,9:e97403
[48]Soma KK,Tramontin AD,Featherstone J,et al.Estrogen contributes to seasonal plasticity of the adult avian song control system.J Neurobiol,2004,58:413-22
[49]Sober SJ,Wohlgemuth MJ,Brainard MS.Central contributions to acoustic variation in birdsong.J Neurosci,2008,28:10370-9
[50]Goldberg JH,Fee MS.Vocal babbling in songbirds requires the basal ganglia-recipient motor thalamus but not the basal ganglia.J Neurophysiol,2011,105:2729-39
[51]Tanaka M,Singh Alvarado J,Murugan M,et al.Focal expression of mutant huntingtin in the songbird basal ganglia disrupts cortico-basal ganglia networks and vocal sequences.Proc Natl Acad Sci USA,2016,113:E1720-7
[2]Lynch KS,Louder MIM,Hauber ME.Species-specific auditory forebrain responses to non-learned vocalizations in juvenile blackbirds.Brain Behav Evol,2018,91:193-200
[3]Xiao L,Chattree G,Oscos FG,et al.A basal ganglia circuit sufficient to guide birdsong learning.Neuron,2018,98:208-221.e5
[4]Pawlisch BA,Remage-Healey L.Neuroestrogen signaling in the songbird auditory cortex propagates into a sensorimotor network via an‘interface’nucleus.Neuroscience,2015,284:522-35
[5]Wang S,Liao C,Li F,et al.Castration modulates singing patterns and electrophysiological properties of RA projection neurons in adult male zebra finches.Peer J,2014,2:e352
[6]Dieni CV,Ferraresi A,Sullivan JA,et al.Acute inhibition of estradiol synthesis impacts vestibulo-ocular reflex adaptation and cerebellar long-term potentiation in male rats.Brain Struct Funct,2018,223:837-50
[7]Pedersen AL,Saldanha CJ.Reciprocal interactions between prostaglandin E2-and estradiol-dependent signaling pathways in the injured zebra finch brain.J Neuroinflammation,2017,14:262
[8]Bailey DJ,Makeyeva YV,Paitel ER,et al.Hippocampal aromatization modulates spatial memory and characteristics of the synaptic membrane in the male zebra finch.Endocrinology,2017,158:852-9
[9]Charlier TD,Po KW,Newman AE,et al.17β-estradiol levels in male zebra finch brain:combining Palkovits punch and an ultrasensitive radioimmunoassay.Gen Comp Endocrinol,2010,167:18-26
[10]Acharya KD,Veney SL.Characterization of the G-protein-coupled membrane-bound estrogen receptor GPR30 in the zebra finch brain reveals a sex difference in gene and protein expression.Dev Neurobiol,2012,72:1433-46
[11]Frankl-Vilches C,Gahr M.Androgen and estrogen sensitivity of bird song:a comparative view on gene regulatory levels.J Comp Physiol A:Neuroethol Sens Neural Behav Physiol,2018,204:113-26
[12]Hadjimarkou MM,Vasudevan N.GPER1/GPR30 in the brain:Crosstalk with classical estrogen receptors and implications for behavior.J Steroid Biochem Mol Biol,2018,176:57-64
[13]Bailey DJ,Saldanha CJ.The importance of neural aromatization in the acquisition,recall,and integration of song and spatial memories in passerines.Horm Behav,2015,74:116-24
[14]Vahaba DM,Remage-Healey L.Neuroestrogens rapidly shape auditory circuits to support communication learning and perception:evidence from songbirds.Horm Behav,2018,104:77-87
[15]Yoder KM,Lu K,Vicario DS.Blocking estradiol synthesis affects memory for songs in auditory forebrain of male zebra finches.Neuroreport,2012,23:922-6
[16]Lattin CR,Stabile FA,Carson RE.Estradiol modulates neural response to conspecific and heterospecific song in female house sparrows:an in vivo positron emission tomography study.PLoS One,2017,12:e0182875
[17]Calisi RM,Knudsen DP,Krause JS,et al.Estradiol differentially affects auditory recognition and learning according to photoperiodic state in the adult male songbird,European starling(Sturnus vulgaris).Peer J,2013,1:e150
[18]Sanford SE,Lange HS,Maney DL.Topography of estradiol-modulated genomic responses in the songbird auditory forebrain.Dev Neurobiol,2010,70:73-86
[19]Chao A,Paon A,Remage-Healey L.Dynamic variation in forebrain estradiol levels during song learning.Dev Neurobiol,2015,75:271-86
[20]Korol DL,Pisani SL.Estrogens and cognition:friends or foes?an evaluation of the opposing effects of estrogens on learning and memory.Horm Behav,2015,74:105-15
[21]Vahaba DM,Remage-Healey L.Brain estrogen production and the encoding of recent experience.Curr Opin Behav Sci,2015,6:148-53
[22]De Groof G,Balthazart J,Cornil CA,et al.Topography and lateralized effect of acute aromatase inhibition on auditory processing in a seasonal songbird.J Neurosci,2017,37:4243-54
[23]Vahaba DM,Macedo-Lima M,Remage-Healey L.Sensory coding and sensitivity to local estrogens shift during critical period milestones in the auditory cortex of male songbirds.eNeuro,2017,4:pii:ENEURO.0317-17.2017
[24]Remage-Healey L,Coleman MJ,Oyama RK,et al.Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird.Proc Natl Acad Sci USA,2010,107:3852-7
[25]Yoder KM,Phan ML,Lu K,et al.He hears,she hears:are there sex differences in auditory processing?Dev Neurobiol,2015,75:302-14
[26]Tremere LA,Jeong JK,Pinaud R.Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression.JNeurosci,2009,29:5949-63
[27]Pinaud R,Terleph TA,Tremere LA,et al.Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain.J Neurophysiol,2008,100:441-55
[28]Caras ML,O’Brien M,Brenowitz EA,et al.Estradiol selectively enhances auditory function in avian forebrain neurons.J Neurosci,2012,32:17597-611
[29]Pedersen AL,Brownrout JL,Saldanha CJ.Neuroinflammation and neurosteroidogenesis:reciprocal modulation during injury to the adult zebra finch brain.Physiol Behav,2018,187:51-6
[30]Pedersen AL,Nelson LH,Saldanha CJ.Centrally synthesized estradiol is a potent anti-inflammatory in the injured zebra finch brain.Endocrinology,2016,157:2041-51
[31]Pedersen AL,Saldanha CJ.Reciprocal interactions between prostaglandin E2-and estradiol-dependent signaling pathways in the injured zebra finch brain.J Neuroinflammation,2017,14:262
[32]Pedersen AL,Gould CJ,Saldanha CJ.Activation of the peripheral immune system regulates neuronal aromatase in the adult zebra finch brain.Sci Rep,2017,7:10191
[33]Mehos CJ,Nelson LH,Saldanha CJ.A quantification of the injury-induced changes in central aromatase,oestrogenic milieu and steroid receptor expression in the zebra finch.J Neuroendocrinol,2016,28:12348
[34]Ikeda MZ,Krentzel AA,Oliver TJ,et al.Clustered organization and region-specific identities of estrogen-producing neurons in the forebrain of zebra finches(Taeniopygia guttata).J Comp Neurol,2017,525:3636-52
[35]Bailey DJ,Ma C,Soma KK,et al.Inhibition of hippocampal aromatization impairs spatial memory performance in a male songbird.Endocrinology,2013,154:4707-14
[36]Roth TC 2nd,Stocker K,Mauck R.Morphological changes in hippocampal cytoarchitecture as a function of spatial treatment in birds.Dev Neurobiol,2017,77:93-101
[37]Luine V,Serrano P,Frankfurt M.Rapid effects on memory consolidation and spine morphology by estradiol in female and male rodents.Horm Behav,2018,104:111-8
[38]Hamaide J,De Groof G,Van Ruijssevelt L,et al.Volumetric development of the zebra finch brain throughout the first200 days of post-hatch life traced by in vivo MRI.Neuroimage,2018,183:227-38
[39]Martin LC,Veney SL.The specific estrogen receptor antagonist ICI 182,780 masculinizes development of the zebra finch syrinx.Gen Comp Endocrinol,2008,156:434-9
[40]Grisham W,Lee J,Park SH,et al.A dose-response study of estradiol’s effects on the developing zebra finch song system.Neurosci Lett,2008,445:158-61
[41]Wade J,Arnold AP.Sexual differentiation of the zebra finch song system.Ann N Y Acad Sci,2004,1016:540-59
[42]Holloway CC,Clayton DF.Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro.Nat Neurosci,2001,4:170-5
[43]Beach LQ,Wade J.Masculinisation of the zebra finch song system:roles of oestradiol and the Z-chromosome gene tubulin-specific chaperone protein A.J Neuroendocrinol,2015,27:324-34
[44]Wade J,Peabody C,Tang YP,et al.Estradiol modulates neurotransmitter concentrations in the developing zebra finch song system.Brain Res,2013,1517:87-92
[45]Alward BA,de Bournonville C,Chan TT,et al.Aromatase inhibition rapidly affects in a reversible manner distinct features of birdsong.Sci Rep,2016,6:32344
[46]Wang S,Meng W,Liu S,et al.Sex differences of excitatory synaptic transmission in RA projection neurons of adult zebra finches.Neurosci Lett,2014,582:75-80
[47]Chen Q,Zhang X,Zhao Y,et al.Sexual differences in cell proliferation in the ventricular zone,cell migration and differentiation in the HVC of juvenile Bengalese finch.PLoS One,2014,9:e97403
[48]Soma KK,Tramontin AD,Featherstone J,et al.Estrogen contributes to seasonal plasticity of the adult avian song control system.J Neurobiol,2004,58:413-22
[49]Sober SJ,Wohlgemuth MJ,Brainard MS.Central contributions to acoustic variation in birdsong.J Neurosci,2008,28:10370-9
[50]Goldberg JH,Fee MS.Vocal babbling in songbirds requires the basal ganglia-recipient motor thalamus but not the basal ganglia.J Neurophysiol,2011,105:2729-39
[51]Tanaka M,Singh Alvarado J,Murugan M,et al.Focal expression of mutant huntingtin in the songbird basal ganglia disrupts cortico-basal ganglia networks and vocal sequences.Proc Natl Acad Sci USA,2016,113:E1720-7
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