达乌尔黄鼠犁鼻器和副嗅球的组织结构及嗅球c-Fos表达的季节变化

doi:10.16829/j.slxb.150483

摘要/Abstract

摘要： 啮齿动物的犁鼻器和副嗅球与社会通讯和生殖行为有关，主嗅球影响其觅食行为。达乌尔黄鼠（Spermophilus dauricus）是一种具有较低社会行为的储脂类冬眠动物。本研究用组织学和免疫组织化学方法探究了其犁鼻器和副嗅球的结构特点及嗅球神经元活动对季节变化的适应。结果发现，达乌尔黄鼠犁鼻器具有较大的血管，犁鼻器管腔外侧为非感觉性的呼吸上皮（Respiratory epithelium，RE），内侧为感觉上皮（Sensory epithelium，SE），RE较SE薄，靠近管腔处为假复层柱状上皮。选取犁鼻器中间部位比较，发现SE的厚度、长度及感觉细胞密度均无性别差异。副嗅球位于主嗅球后方背内侧，由6层细胞构成。侧嗅束穿过副嗅球，位于颗粒细胞层之上。雄性达乌尔黄鼠较雌性有更长的僧帽细胞层和颗粒细胞层。春季（3月）和冬季（1月）达乌尔黄鼠主嗅球的嗅小球层、僧帽细胞层和颗粒细胞层的c-Fos-ir神经元密度显著低于夏季（7月）和秋季（10月），且冬季外网织层的c-Fos-ir神经元密度显著低于夏季和秋季，说明达乌尔黄鼠在冬季和春季的嗅觉神经活动较弱，呈现出对冬眠的生理性适应。这些结果丰富了动物犁鼻器和副嗅球的形态学资料，并有助于理解冬眠动物嗅觉系统对季节变化和冬眠的适应。

关键词: 达乌尔黄鼠, 冬眠, 犁鼻系统, 嗅球, c-Fos, 季节

Abstract: The vomeronasal organ (VNO) and the accessory olfactory bulb (AOB) in rodents are related to social communication and reproductive behavior, while the main olfactory bulb (MOB) influences foraging behavior. The Daurian ground squirrel (Spermophilus dauricus) is a typical fat-storing hibernator that exhibits low levels of social behaviors. Using histological and immunohistochemical methods, this study has investigated the detailed histological features of the VNO and AOB in the Daurian ground squirrels and how the neuronal activation of the MOB responds to the seasonal variations. There is a large vomeronasal blood vessel in the VNO of the Daurian ground squirrel. The lumen of the VNO is lined laterally by a non-sensory respiratory epithelium (RE) and medially by the sensory epithelium (SE). The RE is thinner than that of the SE, and it consists of pseudostratified columnar epithelium near the lumen. At the middle region of the VNO, no sex differences are observed in either the height or length of the SE, nor in the density of the receptor cells. The AOB is located caudal and dorso-medially relative to the position of the MOB. The AOB strata consist of six layers of cells. The lateral olfactory tract (LOT) passes through the AOB and is positioned above the granule cell layer (GCL). The mitral cell layer (MCL) and GCL in males are longer than that in females. The densities of c-Fos-ir neurons of the glomerular layer (GL), MCL, and GCL in spring (March) and winter (January) are less than that in summer (July) and autumn (October). Furthermore, the external plexiform layer (EPL) displays fewer c-Fos-ir neurons in winter than that in summer and autumn. These results indicate that the olfactory bulb of the Daurian ground squirrel exhibits much weaker neuronal activation in winter and spring, showing a physiological adaptation to hibernation. The present study adds to the body of morphological knowledge on the VNO and AOB and furthers our understanding of the specific acclimatization of the olfactory system to seasonal variation and hibernation in hibernating rodents.

Key words: Daurian ground squirrels, Hibernation, Vomeronasal system, Olfactory bulb, c-Fos, Season

中图分类号:

Q494

王恒, 王建礼, 杨晨希, 何娅婷. 达乌尔黄鼠犁鼻器和副嗅球的组织结构及嗅球c-Fos表达的季节变化[J]. 兽类学报, 2021, 41(6): 685-694.

WANG Heng, WANG Jianli, YANG Chenxi, HE Yating. Histological structure of the vomeronasal organ and accessory olfactory bulb and the seasonal changes of olfactory bulb c-Fos expression in Spermophilus dauricus[J]. ACTA THERIOLOGICA SINICA, 2021, 41(6): 685-694.

参考文献

Aland R C, Gosden E, Bradley A J. 2016. Seasonal morphometry of the vomeronasal organ in the marsupial mouse, Antechinus subtropicus. Journal of Morphology, 277 (11):1517-1530.
Apelbaum A F, Chaput M A. 2003. Rats habituated to chronic feeding restriction show a smaller increase in olfactory bulb reactivity compared to newly fasted rats. Chemical Senses, 28 (5):389-395.
Bargmann C I. 1997. Olfactory receptors, vomeronasal receptors, and the organization of olfactory information. Cell, 90 (4):585-587.
Bitting L, Sutin E L, Watson F L, Leard L E, O' Hara B F, Heller H C, Kilduff T S. 1994. C-fos mRNA increases in the ground squirrel suprachiasmatic nucleus during arousal from hibernation. Neuroscience Letters, 165 (1-2):117.
Bratincsák A, Mcmullen D, Miyake S, Toth Z E, Hallenbeck J M, Palkovits M. 2010. Spatial and temporal activation of brain regions in hibernation:c-fos expression during the hibernation bout in thirteen-lined ground squirrel. Journal of Comparative Neurology, 505 (4):443-458.
Caminero A A, Segovia S, Guillamon A. 1991. Sexual dimorphism in accessory olfactory bulb mitral cells:a quantitative Golgi study. Neuroscience, 45 (3):663-670.
Dennis J C, Stilwell N K, Smith T D, Park T J, Bhatnagar K P, Morrison E E. 2020. Is the mole rat vomeronasal organ functional? The Anatomical Record, 303 (2):318-329.
DeVries A C, Carter C S. 1999. Sex differences in temporal parameters of partner preference in prairie voles (Microtus ochrogaster). Canadian Journal of Zoology, 77:885-889.
Frahm H D, Bhatnagar K P. 1980. Comparative morphology of the accessory olfactory bulb in bats. Journal of Anatomy (Lond), 130:349-365
Halpern M. 1987. The organization and function of the vomeronasal system. Annual Review of Neuroscience, 10 (1):325-362.
He F Q, Tai F D, Zhang Y H, Ding X L. 2005. Observation on microstructure of vomeronasal system of Cricetulus barabensis, Microtus mandarinus, Apodemus peninsulae. Journal of Shaanxi Normal University (Natural Science Edition), 33 (2):87-90. (in Chinese)
He L. 2005. Study on the vomeronasal system of Gansu zokor (Myospalax cansus) and root vole (Microtus oeconomus). Master thesis. Xi' an:Shaanxi Normal University. (in Chinese).
Keverne E B. 1999. The vomeronasal organ. Science, 286 (5440):716-720.
Kondoh D, Tanaka Y, Kawai Y K, Mineshige T, Watanabe K, Kobayashi Y. 2021. Morphological and histological features of the vomeronasal organ in African pygmy hedgehog (Atelerix albiventris). Animals, 11 (5):1462.
Liberles S D. 2014. Mammalian pheromones. Annual Review of Physiology, 76 (1):151-175.
Long D, Guo B R, Gao L, Jiang L, Gao Y, Lu S S. 2011. The differences of c-Fos expression in Hedgehog (Erinaceus europaeus) olfactory bulb during hibernation and non-hibernation. Acta Theriologica Sinica, 31 (3):272-277. (in Chinese)
Mahdy E, Behery E, Mohamed S. 2019. Comparative morpho-histological analysis on the vomeronasal organ and the accessory olfactory bulb in Balady dogs (Canis familiaris) and New Zealand rabbits (Oryctolagus cuniculus). Journal of Advanced Veterinary And Animal Research, 6 (4):506-515.
Maico L M, Roslinski D L, Burrows A M, Mooney M P, Smith T D. 2001. Size of the Vomeronasal Organ in Wild Microtus. New York:Springer US.
Meisami E, Bhatnagar K P. 1998. Structure and diversity in mammalian accessory olfactory bulb. Microscopy Research & Technique, 43 (6):476-499.
Mendoza A S. 1993. Morphological studies on the rodent main and accessory olfactory systems:The regioolfactoria and vomeronasal organ. Annals of Anatomy-Anatomischer Anzeiger, 175 (5):425-446.
Mogi K, Sakurai K, Ichimaru T, Ohkura S, Mori Y, Okamura H. 2007. Structure and chemical organization of the accessory olfactory bulb in the goat. Anatomical Record-advances In Integrative Anatomy And Evolutionary Biology (Hoboken), 290 (3):301-310.
Ortiz-Leal I, Torres M V, Villamayor P R, López-Beceiro A, SanchezQuinteiro P. 2020. The vomeronasal organ of wild canids:the fox (Vulpes vulpes) as a model. Journal of Anatomy, 237 (5):890-906.
Park C, Ahn M, Lee J Y, Lee S, Yun Y, Lim Y K, Taniguchi K, Shin T. 2014. A morphological study of the vomeronasal organ and the accessory olfactory bulb in the Korean roe deer, Capreolus pygargus. Acta Histochemica, 116 (1):258-264.
Pospisilova E, Malinsky J. 1985. The accessory olfactory bulb of the hedgehog. Folia Morphol (Prah), 33:34-37.
Prud'Homme M J, Lacroix M C, Badonnel K, Gougis S, Baly C, Salesse R, Caillol M. 2009. Nutritional status modulates behavioural and olfactory bulb Fos responses to isoamyl acetate or food odour in rats:roles of orexins and leptin. Neuroscience, 162(4):1287-1298.
Salazar I, Lombardero M, Alemañ N, Quinteiro P S. 2003. Development of the vomeronasal receptor epithelium and the accessory olfactory bulb in sheep. Microscopy Research & Technique, 61(5):438-447.
Segovia S, Guillamon A. 1982. Effects of sex steroids on the development of the vomeronasal organ in the rat. Brain Research, 281(2):209-212.
Smith T D, Roslinski D L, Burrows A M, Bhatnagar K P, Siegel M I. 2001. Size of the vomeronasal neuroepithelium in two species of Microtus with differing levels of paternal behavior. Journal of Mammalogy, 82 (1):209-217.
Sun X Y, Gao Y F, Wang Q, Jiang S F, Guo S P, Liu K. 2012. The artificial feeding, breeding and research on hibernation bouts the artificial feeding, breeding and research on hibernation bouts. Acta Theriologica Sinica, 32 (4):356-361. (in Chinese)
Tai F D, Wang T Z, Zhang Y H, Hao L, Sun R Y. 2003. Histological structure of the vomeronasal organ and accessory olfactory histological structure of the vomeronasal organ and accessory olfactory. Current Zoology, 49 (2):248-255. (in Chinese)
Tai F D, Wang T Z, Zhang Y H, Sun R Y. 2004. Sexual dimorphism of the vomeronasal organ and the accessory olfactory bulb of the mandarin vole Microtus mandarinus and the reed vole M. fortis. Acta Theriologica, 49 (1):33-42.
Valencia A, Segovia S, Guillamón A. 1986. Effects of sex steroids on the development of the accessory olfactory bulb mitral cells in the rat. Brain Research, 24 (1-2):287-290.
Wang H, He C, Yang C X, Ma X M, Wang J L. 2020. Comparison on sociability and social behaviors between wild and laboratory F1 generation Daurian ground squirrels (Spermophilus dauricus). Chinese Journal of Wildlife, 41 (3):580-588. (in Chinese)
Wang J, Ji W H, Su J H, Gao K, Xu Y H, Liu R T. 2015. The research status on Spermophilus dauricus. Chinese Agricultural Science Bulletin, 31 (8):33-39. (in Chinese)
Yan J L, Adilijiang·Yiming, He J J, Yang R Y, Yang X Q, Gao L P, Jing Y H. 2015. The behavior of olfactory explore enhanced by starvation is associated with the activity of neurons of piriform cortex. Chinese Journal of Neuroanatomy, 31 (4):460-464. (in Chinese)
Yang M, Xing X, Guan S J, Zhao Y, Wang Z Y, Wang D H. 2011. Hibernation patterns and changes of body temperature in Daurian ground squirrels (Spermophilus dauricus) during hibernation. Acta Theriologica Sinica, 31 (4):387-395. (in Chinese)
王恒, 赫晨, 杨晨希, 马小梅, 王建礼. 2020.野生达乌尔黄鼠与室内F1代的社会性及社会行为比较.野生动物学报, 41 (3):580-588.
王静, 纪维红, 苏军虎, 高科, 徐彦花, 刘荣堂. 2015.达乌尔黄鼠(Spermophilus dauricus)生态学研究进展.中国农学通报, 31 (8):33-39.
龙娣, 郭炳冉, 高玲, 江乐, 高燕, 卢少俊. 2011.刺猬嗅球冬眠期与非冬眠期 c-Fos表达的差异.兽类学报, 31 (3):272-277.
孙小勇, 高云芳, 王琦, 姜山峰, 郭树攀, 刘坤. 2012.达乌尔黄鼠实验室饲养, 繁殖及其冬眠阵.兽类学报, 32 (4):356-361.
邰发道, 王廷正, 张育辉, 郝琳, 孙儒泳. 2003.棕色田鼠与沼泽田鼠犁鼻器和副嗅球的组织结构.动物学报, 49 (2):248-255.
何凤琴, 邰发道, 张育辉, 丁小丽. 2005.黑线仓鼠、棕色田鼠和大林姬鼠犁鼻系统的显微结构观察.陕西师范大学学报(自然科学版), 33 (2):87-90.
杨明, 邢昕, 管淑君, 赵岩, 王子英, 王德华. 2011.达乌尔黄鼠冬眠期间体温的变化和冬眠模式.兽类学报, 31 (4):387-395.
郝琳. 2005.甘肃鼢鼠 (Myospalax cansus)、根田鼠 (Microtus oeconomus)犁鼻系统研究.西安:陕西师范大学硕士学位论文.
阎继龙, 阿迪力江·伊明, 何俊杰, 杨汝阳, 杨晓庆, 高丽萍, 景玉宏. 2015.饥饿促进嗅觉探索与梨状皮层神经细胞反应.神经解剖学杂志, 31 (4):460-464.

[1]	范超, 张良志, 付海波, 刘传发, 李文靖, 张贺, 唐显江, 程琪, 沈文娟, 张堰铭. 高原鼠兔肠道微生物中丰富及稀有类群的季节性特征[J]. 兽类学报, 2021, 41(6): 617-630.
[2]	王德华, 赵志军, 张学英, 张志强, 徐德立, 邢昕, 杨生妹, 王政昆, 高云芳, 杨明. 中国哺乳动物生理生态学研究进展与展望[J]. 兽类学报, 2021, 41(5): 537-555.
[3]	吴明阳, 陈仕望, 孙丙华, 王希, 夏东坡, 李进华. 季节和等级顺位对雄性黄山短尾猴粪样皮质醇水平的影响[J]. 兽类学报, 2021, 41(4): 398-405.
[4]	李兴康, 钟旭凯, 韦绍干, 崔亮伟, 范朋飞, 管振华, 马长勇. 群体大小和觅食环境变化对东黑冠长臂猿日移动距离的影响[J]. 兽类学报, 2021, 41(4): 388-397.
[5]	张永俊, 和育超, 赵娟钧, 陈尧, 李延鹏, 黄志旁, 崔亮伟, 肖文. 云岭自然保护区拉沙山区域亚洲黑熊的活动模式[J]. 兽类学报, 2021, 41(2): 136-143.
[6]	安晓宇王玉军李永昌贾功雪杨其恩. 高原鼢鼠精子发生的形态学特征和关键调控因子探究[J]. 兽类学报, 2020, 40(5): 435-445.
[7]	邓林华陈艳魏荣平王承东黄山魏明徐娅琳王群李德生张志忠. 圈养大熊猫生理和血液指标的季节变化[J]. 兽类学报, 2020, 40(4): 398-406.
[8]	王玉军贾功雪王婷王秀蓉刘忠浩都玉蓉马建滨. 光周期-褪黑素信号调控高原鼠兔精原细胞分化和季节性精子发生[J]. 兽类学报, 2020, 40(1): 54-63.
[9]	纪羽袁帅付和平岳闯满都呼杨素文武晓东. 草原鼢鼠土丘与不同根系类型植物的关系[J]. 兽类学报, 2019, 39(2): 162-171.
[10]	张宇飞曹满园王丽英赵伟刚许保增. 水貂睾丸退化期间TGFB家族生长因子及其受体基因表达量的变化[J]. 兽类学报, 2019, 39(2): 191-201.
[11]	朱博伟王彬冉江洪李波黄蜂李晓清古晓东. 黄喉貂日活动节律及食性的季节变化[J]. 兽类学报, 2019, 39(1): 52-61.
[12]	顾晨殷宝法丁晓倩陆意史一然李世平魏万红. 猫尿液气味持续暴露对褐家鼠FOS表达的影响[J]. 兽类学报, 2018, 38(1): 66-73.
[13]	白鸽杨明宋士一彭霞张慧莹刘新宇. 实验室条件下达乌尔黄鼠的越冬繁殖[J]. 兽类学报, 2017, 37(2): 172-178.
[14]	夏凡朱平芬李明任宝平. 白马雪山自然保护区响古箐滇金丝猴（Rhinopithecus bieti）的交配行为[J]. 兽类学报, 2016, 36(1): 1-14.
[15]	李亚军蔡琼刘雪华 Melissa Songer 武鹏峰贾晓东何祥博. 海拔对大熊猫主食竹结构、营养及大熊猫季节性分布的影响[J]. 兽类学报, 2016, 36(1): 24-35.