长期高策略性技能训练对运动员大脑白质结构的影响：一项DTI研究

doi:10.3724/SP.J.1041.2021.00798

摘要/Abstract

摘要：

目前关于运动员经验优势的脑机制还存在争议, 尤其对于涉及较多认知过程参与的高策略性技能项目运动员, 其大脑白质结构可塑性变化还需进一步探究。研究横向对比了乒乓球运动员和非运动员大脑白质纤维束的弥散张量成像数据。结果发现, 相比于非运动员, 乒乓球运动员在连接背侧和腹侧通路脑区的双侧皮质脊髓束、左侧上纵束、左侧下纵束和双侧额枕下束的各向异性值(FA)更大, 进一步分析发现, 部分腹侧通路白质纤维束FA增加的原因是径向扩散系数(RD)下降。研究结果支持了动作双通路模型。提示经过长期高策略性技能训练, 乒乓球运动员在背侧和腹侧通路上的白质纤维束结构完整性增强。

关键词: 脑结构可塑性, 高策略性技能项目, 乒乓球运动员, 弥散张量成像

Abstract:

Previous brain imaging studies have shown that the specialized experience achieved by expert sports players after years of training contributes to plasticity in both brain function and structure. However, changes in brain plasticity related to participating in various types of sports, specifically sports that involve higher-level strategies and cognitive function, remain unclear. Table tennis is a sport requiring high levels of strategy. Thus, the present study investigated the white matter structure of the brain in expert table tennis players who had undergone long-term training. Given the accumulating evidence that action processing in the brain occurs along two distinct pathways—dorsal and ventral—we hypothesized that, in addition to changes in the white matter of the dorsal sensorimotor system, the white matter in the ventral pathway linking brain regions related to higher-level cognitive function would differ between expert table tennis players and nonplayers.
An investigational group of 31 expert table tennis players (20.06 ± 1.69 years of age) and a control group of 28 college students (20.68 ± 1.66 years of age) who had no professional training in table tennis were recruited for the study. The table tennis players were members of university teams, and each player had more than 7 years of table tennis training. Diffusion tensor imaging techniques were used to compare white matter microstructure properties of the brain between expert players and nonplayers. Statistical analyses were performed using independent t-tests. Further analysis was conducted for the expert player group to assess whether any correlation existed between fractional anisotropy (FA) values and training time.
Consistent with our hypothesis, the white matter microstructure properties of both the dorsal and ventral pathways in expert table tennis players significantly differed from those in nonplayers. Specifically, FA values in the bilateral corticospinal tracts, which mainly connect brain regions in the dorsal sensorimotor system, were higher in experts than in nonplayers. Compared with nonplayers, expert players also had higher FA values in the left inferior longitudinal fasciculus and bilateral inferior occipitofrontal fasciculus of the ventral pathway, which are involved in higher-level cognitive processing, such as semantic processing or thinking. By contrast, no white matter region showed a higher FA value in nonplayers than in expert players, and no region was found with axial diffusivity difference between the groups. Additionally, radial diffusivity was lower in the left superior longitudinal fasciculus and bilateral inferior occipitofrontal fasciculus in experts than in nonplayers. Correlation analysis of the expert group showed significant positive correlations between training time and FA values in both the left superior longitudinal fasciculus in the ventral pathway and bilateral corticospinal tracts in the dorsal pathway.
Taken together, these findings suggest that enhanced structural integrity of the white matter in both the dorsal and ventral pathways is associated with long-term, expert table tennis training. The observed structural plasticity is conducive to promoting cognitive processing of concrete sensorimotor and abstract information, which would enable expert players to excel at sports requiring a high level of strategy.

Key words: brain structural plasticity, high-level strategy sports, table tennis player, diffusion tensor imaging

中图分类号:

祁亚鹏, 王怡萱, 朱桦, 周成林, 王莹莹. (2021). 长期高策略性技能训练对运动员大脑白质结构的影响：一项DTI研究. 心理学报, 53(7), 798-806.

QI Yapeng, WANG Yixuan, ZHU Hua, ZHOU Chenglin, WANG Yingying. (2021). Effects associated with long-term training in sports requiring high levels of strategy on brain white matter structure in expert players: A DTI study. Acta Psychologica Sinica, 53(7), 798-806.

图/表 4

表1 被试基本信息

	专家组	对照组
人数(男/女)	31(14/17)	28(13/15)
年龄(M ± SD)	20.06 ± 1.69岁	20.68 ± 1.66岁
BMI	21.21 ±2.59	20.84±2.33
训练年限	11.97 ± 2.68年	/
训练强度	5次/周、2小时/次	/

图1 白质纤维束结构图。左：绿色区域代表白质纤维束骨架, 红色区域代表专家组相比于对照组FA更高的白质纤维束。右：FA存在组间差异的白质纤维束解剖位置。其中, 绿色, 皮质脊髓束; 红色：额枕下束; 黄色：下纵束; 蓝色：上纵束。

图2 专家组和对照组在双侧皮质脊髓束、双侧额枕下束、左侧下纵束和左侧上纵束FA的比较条形图。实心圆代表专家组(ATH), 空心圆代表对照组(CON)。*表示p < 0.05; **表示p < 0.01; ***表示p < 0.001。

图3 专家组左、右侧皮质脊髓束和左侧上纵束的FA与训练时间的相关散点图。*表示p < 0.05。

参考文献 49

[1]	Amoruso, L., Gelormini, C., Aboitiz, F., Gonzalez, M. A., Manes, F., Cardona, J. F., & Ibanez, A. (2013). N400 ERPs for actions: Building meaning in context. Frontiers in Human Neuroscience, 7, 57. doi: 10.3389/fnhum.2013.00057 pmid: 23459873
[2]	Bai, X., Shao, M., Liu, T., Yin, J., & Jin, H. (2020). Altered structural plasticity in early adulthood after badminton training. Acta Psychologica Sinica, 52(2), 173-183. doi: 10.3724/SP.J.1041.2020.00173 URL
	[白学军, 邵梦灵, 刘婷, 尹建忠, 金花. (2020). 羽毛球运动重塑成年早期的大脑灰质和白质结构. 心理学报, 52(2), 173-183.]
[3]	Beilock, S. L., Lyons, I. M., Mattarella-Micke, A., Nusbaum, H. C., & Small, S. L. (2008). Sports experience changes the neural processing of action language. Proceedings of the National Academy of Sciences of the United States of America, 105(36), 13269-13273.
[4]	Bengtsson, S. L., Nagy, Z., Skare, S., Forsman, L., Forssberg, H., & Ullén, F. (2005). Extensive piano practicing has regionally specific effects on white matter development. Nature Neuroscience, 8(9), 1148-1150.
[5]	Bezzola, L., Merillat, S., Gaser, C., & Jancke, L. (2011). Training-induced neural plasticity in golf novices. Journal of Neuroscience, 31(35), 12444-12448. doi: 10.1523/JNEUROSCI.1996-11.2011 URL
[6]	Binder, J. R., Desai, R. H., Graves, W. W., & Conant, L. L. (2009). Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cerebral Cortex, 19(12), 2767-2796. doi: 10.1093/cercor/bhp055 URL
[7]	Blakemore, S. J., & Decety, J. (2001). From the perception of action to the understanding of intention. Nature Reviews Neuroscience, 2(8), 561-567. pmid: 11483999
[8]	Buxbaum, L. J., & Kalenine, S. (2010). Action knowledge, visuomotor activation, and embodiment in the two action systems. Annals of the New York Academy of Sciences, 1191(1), 201-218.
[9]	Calmels, C. (2019). Neural correlates of motor expertise: Extensive motor training and cortical changes. Brain Research, 1739, 146323. doi: 10.1016/j.brainres.2019.146323 URL
[10]	Catani, M., Dell'acqua, F., Bizzi, A., Forkel, S. J., Williams, S. C., Simmons, A., ... de Schotten, M. T. (2012). Beyond cortical localization in clinico-anatomical correlation. Cortex, 48(10), 1262-1287.
[11]	Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7(2), 189-195. doi: 10.1038/nn1176 URL
[12]	Dayan, E., & Cohen, L. G. (2011). Neuroplasticity Subserving Motor Skill Learning. Neuron, 72(3), 443-454. doi: 10.1016/j.neuron.2011.10.008 pmid: 22078504
[13]	Dick, A. S., & Tremblay, P. (2012). Beyond the arcuate fasciculus: Consensus and controversy in the connectional anatomy of language. Brain, 135(12), 3529-3550. doi: 10.1093/brain/aws222 URL
[14]	Duffau, H., Gatignol, P., Mandonnet, E., Peruzzi, P., Tzourio-Mazoyer, N., & Capelle, L. (2005). New insights into the anatomo-functional connectivity of the semantic system: A study using cortico-subcortical electrostimulations. Brain, 128(4), 797-810. doi: 10.1093/brain/awh423 URL
[15]	Giacosa, C., Karpati, F. J., Foster, N. E. V., Penhune, V. B., & Hyde, K. L. (2016). Dance and music training have different effects on white matter diffusivity in sensorimotor pathways. Neuroimage, 135, 273-286. doi: 10.1016/j.neuroimage.2016.04.048 pmid: 27114054
[16]	Guyton, A. C., & Hall, J. E. (2006). Textbook of medical physiology 11th ed. Elsevier Saunders, 788-817.
[17]	Han, Z. Z., Ma, Y. J., Gong, G. L., He, Y., Caramazza, A., & Bi, Y. C. (2013). White matter structural connectivity underlying semantic processing: Evidence from brain damaged patients. Brain, 136(10), 2952-2965. doi: 10.1093/brain/awt205 URL
[18]	Hanggi, J., Langer, N., Lutz, K., Birrer, K., Merillat, S., & Jancke, L. (2015). Structural Brain Correlates Associated with Professional Handball Playing. Plos One, 10(4), e0124222. doi: 10.1371/journal.pone.0124222 URL
[19]	Herbet, G., Zemmoura, I., & Duffau, H. (2018). Functional Anatomy of the Inferior Longitudinal Fasciculus: From Historical Reports to Current Hypotheses. Frontiers in Neuroanatomy, 12, 77. doi: 10.3389/fnana.2018.00077 URL
[20]	Kamali, A., Flanders, A. E., Brody, J., Hunter, J. V., & Hasan, K. M. (2014). Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Structure & Function, 219(1), 269-281.
[21]	Keller, T. A., & Just, M. A. (2009). Altering cortical connectivity: Remediation-induced changes in the white matter of poor readers. Neuron, 64(5), 624-631. doi: 10.1016/j.neuron.2009.10.018 URL
[22]	Kilner, J. M. (2011). More than one pathway to action understanding. Trends in Cognitive Sciences, 15(8), 352-357. doi: 10.1016/j.tics.2011.06.005 URL
[23]	Makris, N., Kennedy, D. N., McInerney, S., Sorensen, A. G., Wang, R., Caviness, V. S., Jr., & Pandya, D. N. (2005). Segmentation of subcomponents within the superior longitudinal fascicle in humans: A quantitative, in vivo, DT-MRI study. Cereb Cortex, 15(6), 854-869. pmid: 15590909
[24]	Makris, N., Meyer, J. W., Bates, J. F., Yeterian, E. H., Kennedy, D. N., & Caviness, V. S. (1999). MRI-Based topographic parcellation of human cerebral white matter and nuclei II. Rationale and applications with systematics of cerebral connectivity. Neuroimage, 9(1), 18-45. pmid: 9918726
[25]	Martino, J., Brogna, C., Robles, S. G., Vergani, F., & Duffau, H. (2010). Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex, 46(5), 691-699. doi: 10.1016/j.cortex.2009.07.015 pmid: 19775684
[26]	Monsell, S. (2003). Task switching. Trends in Cognitive Sciences, 7(3), 134-140. doi: 10.1016/S1364-6613(03)00028-7 URL
[27]	Pulvermuller, F. (2005). Brain mechanisms linking language and action. Nature Reviews Neuroscience, 6(7), 576-582. doi: 10.1038/nrn1706 URL
[28]	Reid, V. M., Hoehl, S., Grigutsch, M., Groendahl, A., Parise, E., & Striano, T. (2009). The neural correlates of infant and adult goal prediction: Evidence for semantic processing systems. Developmental Psychology, 45(3), 620-629. doi: 10.1037/a0015209 URL
[29]	Reid, V. M., & Striano, T. (2008). N400 involvement in the processing of action sequences. Neuroscience Letters, 433(2), 93-97. doi: 10.1016/j.neulet.2007.12.066 URL
[30]	Reng, Z., Hu, L., Zhang, Y., Xu, M., Li, L., Xia, F., & Huang, R. (2019). A review of brain plasticity of motor skill experts: Evidence from magnetic resonance imaging. China Sport Science and Technology, 55(2), 3-18.
	[任占兵, 胡琳琳, 张远超, 徐敏, 李论雄, 夏丰光, 黄瑞旺. (2019). 运动技能专家脑可塑性研究进展:来自磁共振成像的证据. 中国体育科技, 55(2), 3-18.]
[31]	Rizzolatti, G., & Luppino, G. (2001). The cortical motor system. Neuron, 31(6), 889-901. pmid: 11580891
[32]	Romanski, L. M., Tian, B., Fritz, J., Mishkin, M., Goldman-Rakic, P. S., & Rauschecker, J. P. (1999). Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nature Neuroscience, 2(12), 1131-1136.
[33]	Sarubbo, S., de Benedictis, A., Maldonado, I. L., Basso, G., & Duffau, H. (2013). Frontal terminations for the inferior fronto-occipital fascicle: Anatomical dissection, DTI study and functional considerations on a multi-component bundle. Brain Structure & Function, 218(1), 21-37.
[34]	Schlaffke, L., Lissek, S., Lenz, M., Brune, M., Juckel, G., Hinrichs, T., ... Schmidt-Wilcke, T. (2014). Sports and brain morphology - A voxel-based morphometry study with endurance athletes and martial artists. Neuroscience, 259, 35-42. doi: 10.1016/j.neuroscience.2013.11.046 pmid: 24291669
[35]	Shinoura, N., Midorikawa, A., Onodera, T., Tsukada, M., Yamada, R., Tabei, Y., ... Yagi, K. (2013). Damage to the left ventral, arcuate fasciculus and superior longitudinal fasciculus-related pathways induces deficits in object naming, phonological language function and writing, respectively. International Journal of Neuroscience, 123(7), 494-502. doi: 10.3109/00207454.2013.765420 doi: 10.3109/00207454.2013.765420 URL
[36]	Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., ... Behrens, T. E. (2006). Tract-based spatial statistics: Voxelwise analysis of multi- subject diffusion data. Neuroimage, 31(4), 1487-1505.
[37]	Song, S. K., Sun, S. W., Ramsbottom, M. J., Chang, C., Russell, J., & Cross, A. H. (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage, 17(3), 1429-1436.
[38]	Taubert, M., Draganski, B., Anwander, A., Muller, K., Horstmann, A., Villringer, A., & Ragert, P. (2010). Dynamic properties of human brain structure: Learning-related changes in cortical areas and associated fiber connections. Journal of Neuroscience, 30(35), 11670-11677. doi: 10.1523/JNEUROSCI.2567-10.2010 URL
[39]	Urger, S. E., de Bellis, M. D., Hooper, S.R., Woolley, D.P., Chen, S.D., & Provenzale, J. (2015). The superior longitudinal fasciculus in typically developing children and adolescents: Diffusion tensor imaging and neuropsychological correlates. Journal of Child Neurology, 30(1), 9-20. doi: 10.1177/0883073813520503 URL
[40]	Vandermosten, M., Boets, B., Poelmans, H., Sunaert, S., Wouters, J., & Ghesquiere, P. (2012). A tractography study in dyslexia: Neuroanatomic correlates of orthographic, phonological and speech processing. Brain, 135(3), 935-948. doi: 10.1093/brain/awr363 URL
[41]	Vigneau, M., Beaucousin, V., Herve, P. Y., Duffau, H., Crivello, F., Houde, O., ... Tzourio-Mazoyer, N. (2006). Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing. Neuroimage, 30(4), 1414-1432.
[42]	Wang, B., Fan, Y., Lu, M., Li, S., Song, Z., Peng, X., ... Huang, R. (2013). Brain anatomical networks in world class gymnasts: A DTI tractography study. Neuroimage, 65, 476-487. doi: 10.1016/j.neuroimage.2012.10.007 pmid: 23073234
[43]	Wang, Y., Lu, Y., Deng, Y., Gu, N., Parviainen, T., & Zhou, C. (2019). Predicting domain-specific actions in expert table tennis players activates the semantic brain network. Neuroimage, 200, 482-489. doi: 10.1016/j.neuroimage.2019.06.035 URL
[44]	Wilson, S. M., Galantucci, S., Tartaglia, M. C., Rising, K., Patterson, D. K., Henry, M. L., ... Gorno-Tempini, M. L. (2011). Syntactic processing depends on dorsal language tracts. Neuron, 72(2), 397-403. doi: 10.1016/j.neuron.2011.09.014 doi: 10.1016/j.neuron.2011.09.014 URL
[45]	Winkler, A. M., Ridgway, G. R., Webster, M. A., Smith, S. M., & Nichols, T. E. (2014). Permutation inference for the general linear model. Neuroimage, 92, 381-397. doi: 10.1016/j.neuroimage.2014.01.060 URL
[46]	Wright, M. J., Bishop, D. T., Jackson, R. C., & Abernethy, B. (2013). Brain regions concerned with the identification of deceptive soccer moves by higher-skilled and lower-skilled players. Frontiers in Human Neuroscience, 7, 851. doi: 10.3389/fnhum.2013.00851 doi: 10.3389/fnhum.2013.00851
[47]	Wu, Y., Zhang, J., Zeng, Y., & Shen, C. (2015). Structural brain plasticity change in athletes associated with different sports. China Sport Science, 35(4), 52-57.
	[吴殷, 张剑, 曾雨雯, 沈城. (2015). 不同类型运动项目对运动员大脑结构可塑性变化研究. 体育科学, 35(4), 52-57.]
[48]	Yeatman, J. D., Rauschecker, A. M., & Wandell, B. A. (2013). Anatomy of the visual word form area: Adjacent cortical circuits and long-range white matter connections. Brain & Language, 125(2), 146-155.
[49]	Zhang, J., Jones, M., DeBoy, C. A., Reich, D. S., Farrell, J. A., Hoffman, P. N., ... Calabresi, P. A. (2009). Diffusion tensor magnetic resonance imaging of wallerian degeneration in rat spinal cord after dorsal root axotomy. The Journal of Neuroscience, 29(10), 3160-3171. doi: 10.1523/JNEUROSCI.3941-08.2009 URL