Olfactory experience modulates neuron expression in piriform cortex of adult guinea pigs after olfactory deprivation

doi:10.3969/j.issn.2095-4344.2015.18.014

Abstract

Abstract:

BACKGROUND: Animal experiments and clinical studies have shown that, functional deprivation at the early development stage may possibly cause nerve and cognition dysfunction at adulthood. However, no research focuses on the effect of olfactory function on the neurogenesis in piriform cortex of adult guinea pigs.
OBJECTIVE: To establish olfactory deprivation models and explore the effect of olfactory experience on the distribution of doublecortin, parvalbumin, glutamic acid decarboxylase 67 and the co-localization of doublecortin with neuron-specific nuclear-binding protein in piriform cortex of adult guinea pigs.
METHODS: Twenty guinea pigs were randomly divided into two groups. Olfactory deprivation models were established through unilateral naris-occlusion and the occluded animals were allowed to survive 3 and 6 weeks, then the specimens were harvested. The distribution of doublecortin, parvalbumin, glutamic acid decarboxylase 67 was detected with immunohistochemistry. The co-localization of doublecortin with neuron-specific nuclear-binding protein in piriform cortex of adult guinea pigs was determined with immunofluorescence method.
RESULTS AND CONCLUSION: The number of doublecortin, parvalbumin, glutamic acid decarboxylase 67 positive cells in piriform cortex at the undeprived side was significantly higher than that at the deprived side at 3 and 6 weeks (P < 0.05). There was no significant difference in the co-localization of doublecortin with neuron-specific nuclear-binding protein in piriform cortex at 3 weeks group and 6 weeks group (P > 0.05). The findings suggest that olfactory experience promotes the maturation and differentiation of neurons in piriform cortex of adult guinea pigs.

中国组织工程研究杂志出版内容重点：肾移植；肝移植；移植；心脏移植；组织移植；皮肤移植；皮瓣移植；血管移植；器官移植；组织工程

全文链接：

Key words: Olfactory Sensation, Microtubule-Associated Protein, Neuron-Specific Nuclear-Binding Protein

CLC Number:

R318

Liu Yuan-yue, Hou Ju-hua, Liu Fu-xiang, Wang Wei, He Xu. Olfactory experience modulates neuron expression in piriform cortex of adult guinea pigs after olfactory deprivation [J]. Chinese Journal of Tissue Engineering Research, 2015, 19(18): 2867-2873.

Figures/Tables 3

2.1 模型构建成功评价单侧嗅觉剥夺模型制作过程中鼻黏膜收到损伤，没有给豚鼠增加额外的疼痛刺激；豚鼠自然苏醒，在预定存活时间点内(3周，6周)模型侧鼻孔无感染发生；豚鼠在预定存活时间点内(3周，6周)左侧鼻孔保持完全封闭，不能接受外界信息的刺激，同时无再度穿孔。 2.2 两侧梨状皮质微管相关蛋白的表达变化及与神经元特异性核蛋白的共表达免疫组织化学结果显示，微管相关蛋白+主要分布在梨状皮质的第Ⅱ层，细胞胞体明显，形状和大小明显不同，有多极神经元、双极神经元以及单极神经元(图1A1和图B1)；来自树突的分支以及胞体发出的形似树突的微丝在梨状皮质第Ⅰ层形成密集的“从”(图1A，B)。豚鼠左侧嗅觉剥夺3周后，未剥夺侧梨状皮质表达的微管相关蛋白阳性细胞高于剥夺侧，差异有显著性意义(P < 0.05)，6周组微管相关蛋白阳性细胞在两侧梨状皮质的表达情况与3周组的表达相一致(P < 0.05)。见图2。 3周组和6周组两侧梨状皮质第Ⅱ层都有共表达细胞(图3)，共表达阳性细胞数目差异无显著性意义(P > 0.05)。见图4。 2.3 两侧梨状皮质小白蛋白和谷氨酸脱羧酶67的表达变化及阳性细胞统计结果小白蛋白阳性细胞和谷氨酸脱羧酶67阳性细胞在梨状皮质的第Ⅰ层零星分布，绝大部分细胞分布在梨状皮质的Ⅱ，Ⅲ层(图5和图7)。小白蛋白阳性细胞胞核染色明显，胞体称球状或吊灯状，属于多极神经元，而谷氨酸脱羧酶67阳性细胞胞体呈颗粒状(图5)。豚鼠左侧嗅觉剥夺3周后，未剥夺侧状皮质表达的小白蛋白阳性细胞、谷氨酸脱羧酶67阳性细胞分别多于剥夺侧，差异有显著性意义(P < 0.05)；嗅觉剥夺6周后，小白蛋白阳性细胞、谷氨酸脱羧酶67阳性细胞在两侧梨状皮质的表达情况与嗅觉剥夺3周的表达情况相一致(P < 0.05)。见图6和图8。"

References

[1] Apicella A, Yuan Q, Scanziani M, et al. Pyramidal cells in piriform cortex receive convergent input from distinct olfactory bulb glomeruli. J Neurosci. 2010;30(42): 14255-14260.
[2] Franks KM, Russo MJ, Sosulski DL, et al. Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron. 2011;72(1): 49-56.
[3] Saaltink DJ, Havik B, Verissimo CS, et al. Doublecortin and doublecortin-like are expressed in overlapping and non-overlapping neuronal cell population: implications for neurogenesis. J Comp Neurol. 2012;520(13): 2805-2823.
[4] Couillard-Despres S, Winner B, Schaubeck S, et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci. 2005;21(1): 1-14.
[5] Francis F, Koulakoff A, Boucher D, et al. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron. 1999;23(2): 247-256.
[6] Gavrilovici C, D'Alfonso S, Poulter M O. Diverse interneuron populations have highly specific interconnectivity in the rat piriform cortex. J Comp Neurol. 2010; 518(9): 1570-1588.
[7] Wu KN, Tan BK, Howard JD, et al. Olfactory input is critical for sustaining odor quality codes in human orbitofrontal cortex. Nat Neurosci.2012;15(9): 1313-1319.
[8] 刘勇,唐亚梅,蒲唯丹,等. MK-801诱导的精神分裂症发育模型大鼠脑组织DA,DOPAC,Glu和GABA浓度的变化(英文)[J]. 中南大学学报：医学版,2011,36(8): 712-719.
[9] Hubel DH, Wiesel TN. Ferrier lecture. Functional architecture of macaque monkey visual cortex. Proc R Soc Lond B Biol Sci. 1977;198(1130): 1-59.
[10] Keck T, Scheuss V, Jacobsen R I, et al. Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron. 2011;71(5): 869-882.
[11] Benson TE, Ryugo DK, Hinds JW. Effects of sensory deprivation on the developing mouse olfactory system: a light and electron microscopic, morphometric analysis. J Neurosci. 1984;4(3): 638-653.
[12] Desgent S, Ptito M. Cortical GABAergic interneurons in cross-modal plasticity following early blindness. Neural Plast. 2012;2012: 590725.
[13] Marco EM, Macri S, Laviola G. Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models. Neurotox Res. 2011;19(2): 286-307.
[14] Weisberg J, Koo DS, Crain KL, et al. Cortical plasticity for visuospatial processing and object recognition in deaf and hearing signers. Neuroimage. 2012; 60(1): 661-672.
[15] Miyazaki T, Takase K, Nakajima W, et al. Disrupted cortical function underlies behavior dysfunction due to social isolation. J Clin Invest. 2012;122(7): 2690-2701.
[16] Coppola D M. Studies of olfactory system neural plasticity: the contribution of the unilateral naris occlusion technique. Neural Plast. 2012;2012: 351752.
[17] Brunjes P C, Smith-Crafts L K, Mccarty R. Unilateral odor deprivation: effects on the development of olfactory bulb catecholamines and behavior. Brain Res. 1985; 354(1): 1-6.
[18] 曾建军,贺旭,严小新,等. 电烙铁损伤左侧外周鼻孔区构建单侧嗅觉剥夺模型:嗅球神经的发生和转化[J]. 中国组织工程研究, 2014(02): 231-238.
[19] Zhang X M, Xiong K, Cai Y, et al. Functional deprivation promotes amyloid plaque pathogenesis in Tg2576 mouse olfactory bulb and piriform cortex. Eur J Neurosci. 2010;31(4): 710-721.
[20] Shapiro LA, Ng KL, Zhou QY, et al. Olfactory enrichment enhances the survival of newly born cortical neurons in adult mice. Neuroreport. 2007;18(10): 981-985.
[21] Leung CH, Wilson DA. Trans-neuronal regulation of cortical apoptosis in the adult rat olfactory system. Brain Res. 2003; 984(1-2): 182-188.
[22] Gomez-Climent MA, Hernandez-Gonzalez S,Shionoya K,et al.Olfactory bulbectomy, but not odor conditioned aversion, induces the differentiation of immature neurons in the adult rat piriform cortex. Neuroscience. 2011;181: 18-27.
[23] Arisi GM, Foresti ML, Mukherjee S, et al. The role of olfactory stimulus in adult mammalian neurogenesis. Behav Brain Res. 2012;227(2): 356-362.
[24] He X, Zhang XM, Wu J, et al. Olfactory experience modulates immature neuron development in postnatal and adult guinea pig piriform cortex. Neuroscience. 2014; 259: 101-112.
[25] Cai Y, Xiong K, Chu Y, et al. Doublecortin expression in adult cat and primate cerebral cortex relates to immature neurons that develop into GABAergic subgroups. Exp Neurol. 2009; 216(2): 342-356.
[26] Zhang X M, Cai Y, Chu Y, et al. Doublecortin-expressing cells persist in the associative cerebral cortex and amygdala in aged nonhuman primates. Front Neuroanat. 2009;3: 17.
[27] Klempin F,Kronenberg G,Cheung G,et al.Properties of doublecortin-(DCX)-expressing cells in the piriform cortex compared to the neurogenic dentate gyrus of adult mice. PLoS One. 2011;6(10): e25760.
[28] Mullen RJ, Buck CR, Smith AM. NeuN, a neuronal specific nuclear protein in vertebrates. Development. 1992;116(1): 201-211.
[29] Wang C, Liu F, Liu YY, et al. Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res. 2011;21(11): 1534-1550.
[30] Yang HK, Sundholm-Peters NL, Goings GE, et al. Distribution of doublecortin expressing cells near the lateral ventricles in the adult mouse brain. J Neurosci Res. 2004;76(3): 282-295.
[31] 高俊彦,李明,薛志琴,等. 触觉剥夺后豚鼠桶状皮质DCX阳性细胞的实验研究[J]. 现代生物医学进展,2012(18): 3407-3411.
[32] Chattopadhyaya B, Di Cristo G, Wu C Z, et al. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron. 2007;54(6): 889-903.
[33] Suzuki N, Bekkers JM. Inhibitory interneurons in the piriform cortex. Clin Exp Pharmacol Physiol. 2007;34(10): 1064-1069.
[34] Kutsuna N, Suma T, Takada Y, et al. Decrease in doublecortin expression without neuronal cell death in rat retrosplenial cortex after stress exposure. Neuroreport. 2012;23(4): 211-215.