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1 50 (2) : , 2004 A cta Zoologica S inica 3 33, , ( Microtus m andarinus) (n = 15) ( M. f ostis), ( ER ) (AR) 2 h, 1 h, 1 h, 1 h, 2 h,,, ER ( ER 2IRs),, AR (AR2IRs), ER 2IRs 2 h, ER 2IRs, AR2IRs ; ER 2IRs AR2IRs, ER 2IRs, AR2IRs : ; ER AR, [ 50 (2) : , 2004 ] ( ER ) (AR) The relationship bet ween social behavior and the expression of estrogen receptor and androgen receptor in olfactory2related bra in regions of the male mandarin vole Microt us mandarinus and reed vole M. f ostis 3 HE Feng2Qin, TAI Fa2Dao 33, ZHAN G Yu2Hui, AN Shu2Cheng College of Life Science, Shaanxi Normal University, Xi an , China Abstract In order to investigate the neurobiological mechanism of the social behavior difference in adult male mandarin voles Microtus m andarinus and reed voles M. f ostis, the behavior focal sampling method and immunohistochemistry method were used to investigate differences in intraspecies male2male interactions and the expressions of estrogen receptor ( ER ) and androgen receptor (AR) between two species, respectively. During the two2hour interaction of male individuals, mandarin voles spent significantly more time on aggressive and defensive behavior to homosexual invaders in the first one hour than in the last hour, whereas the reed voles did not have significantly behavioral difference between the first and last hour. During the whole two2hour interaction of male individuals, mandarin voles spent significantly more time engaged in aggressive and defensive behaviors to homosexual invaders and less time on the nonsocial behaviors than the reed voles. Before the two2hour interaction of male individuals, we found obviously fewer and lighter2stained ER im2 munoreactive neurons ( ER 2IRs) in both main olfactory bulb system project regions and vomeronasal system project re2 gions in the mandarin voles than in the reed voles, but no significant difference in numbers of AR immunoreactive neurons (AR2IRs) between the two species through the examining of immunoreactive neurons. Moreover, there were significantly fewer AR2IRs than ER 2IRs in two species of vole before the two2hour interactions. There were significantly fewer ER2 IRs in both the main olfactory bulb project regions and the vomeronasal system project regions in the mandarin voles after , (No ) [ This research was funded by National Natural Science Foun2 dation of China (No ) and Key Project of Ministry of Education Peoples Republic of China ] 33 (Corresponding author). ν 2004 Acta Zoologica Sinica E2mail : edu. cn

2 interactions than before interactions, but there were significantly more AR2IRs after interactions than before interactions in the mandarin voles. Differences in both numbers of ER 2IRs and AR2IRs between before and after interactions in the reed voles were not significant. There were greatly significantly more ER 2IRs neurons in reed voles than in mandarin voles which had gone through interactions and there were significantly fewer AR2IRs in the reed voles than in the man2 darin voles which had gone through interactions. The results indicate that mandarin voles and reed voles had different so2 cial behaviors in social interactions. The results suggest that the decrease of ER 2IRs and increase of AR2IRs might affect social recognition and aggressive behavior, and this might explain differences in social behaviors between the two vole species [ Acta Zoologica Sinica 50 (2) : , 2004 ]. Key words Mandarin voles, Microtus m andarinus, Reed voles, M. f ostis, Main olfactory bulb system, Vomeronasal system, Estrogen receptor ( ER ), Androgen receptor (AR), ( Summers et al., (, 2001b), 1997),,,, ( Gilles et al., (Wang et al., 1997) 1994 ; Buijs et al., 1978 ; Tribollet et al., 1988) ( M icrot us m andarinus) (, 2001b), : ( M. f ostis) (, 2001a), (Murphy, 1980) (Lepri et al., 1985) (, 2003),, ; ( Wysocki (Lawrence et al., 1991), et al., 1982),, (, 2002 ; Wysocki et al., 1983) ER AR,,, ( Gilles et al., 1994) (Miyachi, 1999) (Ogawa et al., 1999, 2000), 111, 15, g,,, 15,, g,, ( Estrogen receptor, ER ), L 12D, (Androgen receptor, AR) (, 1999),,,, 112, (No2,, mura et al., 2002), ;,, (80 (Mc Ginnis et al., 2002), ER AR, 30 min,, 1 cm 40 cm 40 cm ),,,, THE OBSERV ER ( HOLLAND)

3 2 : h 1 h, ( 1 h, ), 1 h SPSS 5 1 h, h, 2 h, (40 mg/ kg),, 011 mol PBS 150 ml,,, 4 % 300 ml, ( 2) 4 % 3 h (4 ), % OCT, 40 mer ( Sc2 8974) AR (Ba0004) Santa cruz, ( ), SABC ( - ) ER, DAB Sigma (: 2) (: 4) min, ( 4 72 h, 0101 mol PBS 3, 3 min, SABC min, 0101 mol PBS 3, 3 min, DAB min 0101 mol PBS,,, ( P < 0105,, 0101 mol PBS ER AR, (: 1,, 114 ( P > 0105), ER ( : 3) (: 5) ER 2IRs AR2IRs, (, : 7) ( P < 0105),, ( < 8) ( 1) (60 60) m SPSS1010, AR ER, (Mean S E), AR Mann2Whitney U test P < 0105 (: 2) (: 4) ( : 6) 2 211, ( 1) ER, : 6) (: 10) (: 9) ( : 8) ( > 15), ER 8-15) ( 1) 2 h, ER (: 8, P > 0105), ( < 8), ER 1 h, ( P < 0101), ER

4 h 1 h a : 1 h b : 1 h c : 1 h d : 1 h 1 : 2 : 3 : 33 : 1 h 1 h (Mann2Whitney2test, P < 0101), 3 : 1 h 1 h ( Mann2 Whitney test, P < 0105) Fig11 Comparison between behaviors of the f irst one hour and the last hours during the interactions of male2male individuals in Microtus mandarinus and Mirotus f ortis a : Behaviors of the first one hour in the mandarin voles. b : Behaviors of the last one hour in the mandarin voles. c : Be2 haviors of the first one hour in the reed voles. d : Behaviors of the last one hour in the reed voles. 1 : Aggressive behavior. 2 : Other social behaviors. 3 : Nonsocial behaviors. 33 : Both aggressive behavior and nonsocial behaviors of the first one hour and the last hours during the interactions in the mandarin voles have greatly significant dif2 ference by Mann2Whitney2test, P < : Between other social behaviors of the first one hour and the last hours during the interactions in the mandarin voles have significant difference by Mann2Whitney test, P < h a : b : 1 : 2 : 3 : 33 : 2 h (Mann2Whitney test, P < : 2 h (Mann2Whitney U test, P < 0105) Fig12 Behavior during two2hour interactions of male Microtus mandarinus and Mirotus f ortis a : Mandarin voles. b : Reed voles. 1 : Aggressive behavior. 2 : Other social behaviors. 3 : Nonsocial behaviors. 33 : Both aggressive behavior and nonsocial behaviors have greatly significant difference during two hours in two vole species by Mann2Whitney test, P < : Other social behaviors have significant difference between two vole species by Mann2Whitney test, P < 0105.

5 2 : Table 1 Total number of estrogen receptor immunoreactive neurons ( mean S E) in per standard area in brain region before and after interactions of male2male individuals in Microtus mandarinus and Mirotus f ortis Brain region TU LA PO MDI OPCF ME BST VMH MPO LSD Control ER2 M. mandari nus M. f ortis Experimental ER2 P Control ER2 Experimental ER : : TU : LA : PO : MDI : OPCF : ME : BST : VMH : MPO : LSD :, 3 Mann2Whitney ( P < 0105) Control group : Without male exposure. Experimental group : With male exposure. TU : Olfactory tubercle. LA : Lateral amygdaloid nucleus. PO : Piriform cortex. MDI : Mediodorsal thalamic nucleus, intermediate part. OPCF : Orbital prefrontal cortex. ME : Medial amygdaloid nucleus. BST : Bed nucleus of the stria terminalis. VMH : Ventromedial hypothalamic nucleus. MPO : Medial preoptic area. LSD : Lateral septal nucleus, dorsal part. Data is expressed as Mean SD, 3 indicates significant difference between experimental and control groups by Mann2Whitney test, P < Table 2 Total number of androgen receptor immunoreactive neurons ( mean S E) in per standard area in brain region before and after interactions of male2male individuals in Microtus mandarinus and Mirotus f ortis Brain region TU Control AR M. mandari nus M. f ortis Experimental AR P Control AR Experimental LA PO MDI OPCF ME BST VMH MPO LSD : : TU : LA : PO : MDI : OPCF : ME : BST : VMH : MPO : LSD :, 3 Mann2Whitney ( P < 0105) Control group : Without male exposure. Experimental group : With male exposure. TU : Olfactory tubercle. LA : Lateral amygdaloid nucleus. PO : Piriform cortex. MDI : Mediodorsal thalamic nucleus, intermediate part. OPCF : Orbital prefrontal cortex. ME : Medial amygdaloid nucleus. BST : Bed nucleus of the stria terminalis. VMH : Ventromedial hypothalamic nucleus. MPO : Medial preoptic area. LSD : Lateral septal nucleus, dorsal part. Data is expressed as Mean SD, 3 indicates significant difference between experimental and control groups by Mann2Whitney test, P < AR P P

6 ( P < 0105), ( Ferguson et al., 2002),, AR ( 2) 2 h, AR, ER ( P > 0105), AR, ( : ( Hlinak, 1993), 5) (: 1) ER,, (: 3) ER, ( : 7) ER ER, ( P < 0105),, ( 8-15) (Fugger et al., 2000) ER ( 2) ER AR ER,, ER AR, ER AR AR,, ER AR,, AR (AVP) mrna, ER AR 100, AVP (Brot et al., Jane 1993), AVP and J udwh (1995), ( Ferguson et al., 2002), Winslow et, al. ( 1992) ( M icrot us (Jane and J ud2 ochrogaster) : AVP wh, 1995),, AVP,, ( Kevetter and Winas, 1981),,, 313, 2 h, (Wysocki et al., 1983),,, ER ER (Zhang et al., 2000), 1 h,, ER, Insel et al. (1995) 312 ( M icro2 1 h 1 h, t us montanus), 1 h 1 h,,,, 2 h,,, ( Trivers, 1972 ; Pierce and Dewsbury, : 1991) (Wai and Hoar, 1963),

7 2 : 171, AR ER ; ER, AR,, ER ;,,, ER AR, ER, AR ( References) Nomura et al. (2002) ER,,, ER Ogawa et al. (1998) ER,, ER, Temple Ξ et al. ER (2000) : ER, ER,, AR Zhang et al. (2000) ER ER : ER ER, AR,, ER, AR,, ER AR,, by mating. Neuroendocrinology 67 : , ER, AR, ER, AR, (Ben2 Ari, 1981 ; Alheid et al., 1995), ER AR (Baum and Everitt, 1992) Miyachi Y, 1999.,, haviour. Behavioural Processes 47 : (, 1999 ) Greco et al. (1998),, AR Alheid GF, De Olmos J S, Beltramino CA, Amygdala and ex2 tended amygdala. San Diego : Academic Press, Baum MJ, Everitt BJ, Increased expression of c2fos in the medial preoptic area after mating in male rats : role of afferen inputs from the medial amygdala and midbrain central tegmental field. Neuro2 science 50 : Ben2Ari Y, The amygdaloid complex. Amsterdam : Elsevier North Holland Biomedical Press, 516. Brot MD, De Vries GJ, Dorsa DM, Local implants testosterone metabolites regulate vasopressin mrna in sexually dimorphic nuclei of the rat brain. Peptides 14 : Buijs RM, Swaab DF, Dogterom J, Van Leeuwen FW, Intra2 and extrahypothalamic vasopressin and oxytocin pathways in the rat. Cell Tiss. Res. 186 : Ferguson J N, Young LJ, Insel TR, The neuroendocrine basis of social recognition. Frontiers in Neuroendocrinology 23 : Fugger HN, Foster TC, Gustafsson JA, Rissman EF, Novel ef2 fects of estradiol and estrogen receptor and on cognitive func2 tion. Brain Research 883 : Gilles G, Rose2Marie B, Glyn G, Robert D, Social and individu2 al recognition in rodents : methodological aspects and neurobiologi2 cal bases. Behavioural Processes 33 : Greco B, Edwards DA, Michael RP, Clancy AN, Androgen re2 ceptors and estrogen receptors are colocalized in male rat hypothala2 mic and limbic neurons that express Fos immunoreactivity induced Hlinak Z, Social recognition in ovariectomized and estradiol2treat2 ed female rats. Horm. Behav. 27 : Insel TR, Preston S, Winslow J T, Mating in the monogamous male : behavioral consequences. Physiology & Behavior 57 : Jane M K, J udwh MS, Maternal aggression in rats : effects of ol2 factory bulbectomy, ZnSO 4 2induced anosmia, and vomeronasal or2 gan removal. Horm. Behav. 29 : Kevetter GA, Winans SS, Connections of the corticomedial amygdala in the golden hamster.. Efferents of the olfactory amygdala. J. Comp. Neur. 197 : Lawrence ES, Christiana ML, Charlene ES, Donald AD, Thomas RI, Comparative neuroanatomy of the sexually dimorphic hy2 pothalamus in monogamous and polygamous voles. Brain Research 541 : Lepri JJ, Wysocki CJ, Vandenbergh J G, Mouse vomeronasal or2 gen: effects on chemosignals production and maternal behavior. Physiol. Behav. 35 : Extinction of the response to the femaleπs urinary odour as a consequence of low2dose X2irradiation in male hamster, occurs in conjunction with a marked suppression of aggressive be2 Murphy MR, Sexual preferences of male hamster : importance of preweaning and adult experience, vaginal secretion, and olfactory or vomeronasal sensation. Behav. Nural. Biol. 30 : Mc Ginnis M Y, Lumia AR, Breuer ME, Possidente B, Physical provocation potentiates aggression in male rats receiving anabolic Ξ Temple JL, Fugger HN, Li X, Gustafsson JA, Rissman EF, Estrogen receptor hypothalamic pituitary gonadal axis sensitivity to nega2 tive feedback. Social Neuros. Abst. 26 : 540.

8 androgenic steroids. Hormones and Behavior 41 : Nomura M, Durbak L, Chan J, Gustafsson JA, Korach KS, Pfaff DW, Ogawa S, Genotype/ age interactions on aggressive be2 havior in gonadally intact estrogen receptor knockout ( ERKO) male mice. Horm. Behav. 41 : Ogawa S, Chan J, Chester AE, Gustafsson JA, Korach KS, Pfaff DW, Survival of reproductive behaviors in estrogen receptor gene2deficient ( ER KO) male and female mice. Proc. Natl. A2 cad. Sci. USA 96 : Ogawa S, Chester AE, Hewitt SC, Walker VR, Gustafsson JA, Smithies O, Korach KS, Pfaff DW, Abolition of male sexu2 al behaviors in mice lacking estrogen receptors and. Proc. Natl. Acad. Sci. USA 97 : Ogawa S, Washburn TF, Taylor J, Lubahn DB, Korach KS, Pfaff DW, Modifications of testosterone2dependent behaviors by estrogen receptor2alpha gene disruption in male mice. Endocrinolo2 gy 139 : Pierce JD, Dewsbury DA, Female preference or unmated versus mated males in two species of Microlus ochrogaster and Microt us montanus. J. Camp. Psychol. 105 : Summers TR, Hunter AL, Summers CH, Female social repro2 ductive roles affect central monoamines. Brain Research 767 : Tai FD, Sun RY, Wang TZ, Zhou HW, 2001a. Brain and skull mor2 phology in five species of rodents and their ecological relationship. Zoological Research 22 : ( In Chinese). Tai FD, Wang TZ, Sun RY, Functions of vomeronasal system in reproduction behavior of the rodent. Journal of Shaanxi Normal University 30 : ( In Chinese). Tai FD, Wang TZ, Zhao YJ, 2001b. Mate choice and related charac2 teristics of Mandarin voles Microt us Mandarinus. Acta Zool. Sin. 47 : ( In Chinese). Tai FD, Wang TZ, Zhang YH, Hao L, Sun R Y, Histological structure of the vomeronasal organ and accessory olfactory bulb of the mandarian vole Microt us mandarinus and reed vole M. f os2 tis. Acta Zool. Sin. 49 : ( In Chinese). Tribollet E, Barberis C, Jard S, Dubois2Dauphin M, Dreifuss JJ, Localization and pharmacological characterization of high affinity binding sites for vasopressin and oxytocin in the rat brain by light microscopic autoradiography. Brain Research 442 : Trivers RL, Parent offspring conflict. Amer. Zool. 14 : Wai EH, Hoar WS, The secondary sex characters and reproduc2 tive behavior of gonadectmised sticklebacks treated with methyl testosterone. Can. J. Zool. 41 : Wang ZX, Young LJ, Liu Y, Insel TR, Species differences in vasopressin receptor binding are evident early in development : com2 parative anatomic studies in prairie and montane voles. Journal of Comparative Neurology 378 (4) : Winslow J T, Hastings N, Carter CS, Harbaugh CR, Insel TR, A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365 : Wysocki CJ, Nyby J, Whitney G, Beauchamp GK, Katz Y, The vomeronasal organ : primary role in mouse chemosensory gen2 der recognition. Physiol. Behav. 29 : Wysocki CJ, Kate Y, Bernhard R, The male vomeronasal organ mediates female2induced testosterone surges. Biology of Reproduc2 tion 28 : Xu SF, Zhu CQ, Sun FY, Wu GC, Huang XF, Cheng J S, Neurobiology. Shanghai : Shanghai Medical University Publishing House, Zhang WH, Saji ZS, Makinen S, Cheng G, Jensen EV, Warner M, Gustafsson JA, Estrogen receptor ( ER), a modulator of ER in the uterus. Proc. Nat. Acad. Sci. USA 97 : ,,,, 2001a.. 22 : ,,, : ,,, 2001b.. 47 : ,,,,, : ,,,,,, : ER 21 ER 31 2 h ER 41 ER 51 2 h ER 61 ER 71 2 h ER 81 ER 91 ER 101 ER 11 2 h AR 21 AR 31 2 h AR 41 AR 51 2 h AR 61

9 2 : h AR 81 2 h AR PO : MDI : LA : EC : BL P : BST : AC : 3V : VMH : LSD : LV : ME : OT : MPO : CPu : 100 m Explanation of Plates Plate 11 ER immunoreactivity in the lateral amygdaloid nucleus of Microt us mandari nus before interactions of male2male individuals. 21ER immunoreactivity in the lateral amygdaloid of Microt us f ortiss before interactions of male2male individuals. 31ER immunoreactivity in the primary olfactory cortex of Microt us mandari nus after two hours interactions of male2male individuals. 41 ER immunoreactivity in the primary olfactory cortex of Microt us f ortis before interactions of male2male individuals. 51ER immunoreactivity in the medial amygdaloid nucleus nucleus of Microt us mandari nus after two hours interactions of male2male individuals. 61ER immunoreactivity in the medial amygdaloid nucleus nucleus of Microt us f ortis before interactions of male2male individuals. 71ER immunoreactivity in the lateral septal nucleus, dorsal part of Microt us mandari nus after two hours interactions of male2male individuals. 81ER immunoreactivity in the lateral septal nucleus, dorsal part of Microt us f ortiss before interactions of male2male individuals. 91ER immunoreactivity in the medial preoptic area of Microt us f ortiss before interactions of male2male individuals. 101ER immunoreactivity in the bed nucleus of the stria terminalis of Microt us f ortiss before interactions of male2male individuals. Plate 11AR immunoreactivity in the primary olfactory cortex of Microt us mandarinus after two hours interactions of male2male individuals. 21AR immunoreactivity in the primary olfactory cortex of Microt us mandarinus before interactions of male2male individuals. 31 AR immunoreactivity in the mediodorsal thalamic nucleus, intermediate part of Microt us mandarinus after two hours interactions of male2male indi2 viduals. 41AR immunoreactivity in the mediodorsal thalamic nucleus, intermediate part of Microt us mandarinus before interactions of male2male individuals. 51AR immunoreactivity in the lateral amygdaloid nucleus of Microt us mandarinus after two hours interactions of male2male individuals. 61AR immunoreactivity in the bed nucleus of the stria terminalis of Microt us mandarinus before interactions of male2male individuals. 71AR immunoreactivity in the ventromedial hypothalamic nucleus of Microt us mandarinus after two hours interactions of male2male individuals. 81AR immunoreactivity in the lateral septal nucleus, dorsal part of Microt us mandarinus after two hours interactions of male2male individuals. PO : Piriform cortex. MDI : Mediodorsal thalamic nucleus, intermediate part. LA : Lateral amygdaloid nucleus. EC : External capsule. BL P : Posterior division of the basolateral nucleus of the amygdala. BST : Bed nucleus of the stria terminalis. AC : Anterior commissure. 3V : Third ventricle. VMH : Ventromedial hypothalamic nucleus. LSD : Lateral septal nucleus, dorsal part. LV : Lateral ventricle. ME : Medial amygdaloid nucleus. OT : Optic tract. MPO : Medial preoptic area. CPu : Caudate putamen. Scale bar = 100 m.

10 : HE Feng2Qin et al. : The relationship between social behavior and t he expression of est rogen receptor and androgen receptor in olfactory2related brain regions of the male mandarin vole M icrot us m andarinus and reed vole M. f ostis Plate ( Explanation at the end of the text)

11 : HE Feng2Qin et al. : The relationship between social behavior and t he expression of est rogen receptor and androgen receptor in olfactory2related brain regions of the male mandarin vole M icrot us m andarinus and reed vole M. f ostis Plate ( Explanation at the end of the text)

240 生异性相吸的异性效应 [6] 虽然, 心理学基础研 [7-8] 究已经证实存在异性相吸异性相吸是否存在于名字认知识别尚无报道本实验选取不同性别的名字作为刺激材料, 通

240 生异性相吸的异性效应 [6] 虽然, 心理学基础研 [7-8] 究已经证实存在异性相吸异性相吸是否存在于名字认知识别尚无报道本实验选取不同性别的名字作为刺激材料, 通 2011 年 Journal of Capital Medical University 4月第2 期 Apr 2011 Vol 32 No 2 基础研究 doi: 10 3969 / j issn 1006-7795 2011 02 015 人脑识别不同性别名字反应时的差异研究高迎霄陈昭燃 * 张明霞 ( 首都医科大学神经生物系高级脑功能中心) 摘要目的探讨男女对不同性别名字认知加工速度是否存在差异