ISSN 1671-3710
CN 11-4766/R
主办:中国科学院心理研究所
出版:科学出版社

心理科学进展, 2019, 27(6): 1058-1071 doi: 10.3724/SP.J.1042.2019.01058

研究前沿

急性有氧运动对认知表现的影响

张斌, 刘莹,

上海体育学院运动科学学院, 上海 200438

The effect of acute aerobic exercise on cognitive performance

ZHANG Bin, LIU Ying,

School of Kinesiology, Shanghai University of Sport, Shanghai 200438, China

通讯作者: 刘莹, E-mail:yummy_liu@126.com

收稿日期: 2017-11-16   网络出版日期: 2019-06-15

基金资助: 上海市教育委员会学校体育科研项目()
上海市教育科学研究一般项目(C16042)
教育部人文社会科学研究一般项目资助(14YJAZH054)

Received: 2017-11-16   Online: 2019-06-15

摘要

急性有氧运动是持续时间在10~60分钟的一次有氧运动。急性有氧运动可暂时性地改变感觉敏感度、记忆、执行功能等认知功能, 但其对不同认知功能的影响效果存在差异, 干预结果受到个体体适能水平、运动强度和运动类型等因素的调节。目前用于解释急性有氧运动影响认知表现的理论有唤醒理论、前额叶功能衰退理论、神经内分泌模型和神经营养因子假说。未来的研究应加强对急性运动发挥作用机制的探究, 更多关注身心运动、团体运动等不同运动形式的干预效果, 以期为长期“运动处方”的开具提供依据。

关键词: 急性运动; 有氧运动; 执行功能; 调节变量

Abstract

Acute aerobic exercise is a bout of aerobic exercise lasting from 10 to 60 minutes. Acute aerobic exercise can temporarily change cognitive performance, such as sensory sensitivity, memory, executive function. The effects of acute aerobic exercise on cognitive performance are varying, which are moderated by participant physical fitness level, exercise intensity and type of exercise. Arousal theory, Reticular- activating hypofrontality model, catecholamines hypothesis, BDNF hypothesis and strength model of self-control have been proposed to account for the effect of acute aerobic exercise on cognitive performance. Future studies are suggested to investigate the mechanism of how acute aerobic exercise effects cognitive performance, explore the interfering effects of different forms of acute aerobic exercise, such as mind-body exercises, group sports, and thus providing more evidence for the long-term ‘exercise prescriptions’.

Keywords: acute exercise; aerobic exercise; executive function; moderator

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本文引用格式

张斌, 刘莹. 急性有氧运动对认知表现的影响 . 心理科学进展, 2019, 27(6): 1058-1071 doi:10.3724/SP.J.1042.2019.01058

ZHANG Bin, LIU Ying. The effect of acute aerobic exercise on cognitive performance. Advances in Psychological Science, 2019, 27(6): 1058-1071 doi:10.3724/SP.J.1042.2019.01058

1 引言

有氧运动对个体认知功能的积极作用, 已经在延缓认知功能衰退, 降低阿尔兹海默症的患病风险, 促进儿童的认知发展, 提升青少年的学业表现等(Colcombe et al., 2006; Hillman, Erickson, & Kramer, 2008; Wilson et al., 2002)多方面得以证实。然而, 近年来, 由于代步工具和移动电子设备的迅速发展, 人们的身体活动量大幅减少(Kohl et al., 2012)。生活方式的改变带来了诸多身心健康隐患(Kerr, Anderson, & Lippman, 2017; Lear et al., 2017)。对此, 如何开具“运动处方”以维持和提升个体认知功能, 成为运动科学领域学者普遍关注的焦点(Haskell et al., 2007), 其中, 急性有氧运动的作用及机制是解析该问题的主要切入点。

急性有氧运动(acute aerobic exercise)又称短时运动、一次性运动(a bout of aerobic exercise), 指持续时间在10~60分钟左右的、以有氧代谢提供能量的一次运动(Chang, Labban, Gapin, & Etnier, 2012; 陈爱国, 殷恒婵, 颜军, 杨钰, 2011)。探索一次有氧运动对认知表现的影响规律, 将有助于理解运动改变认知功能的机制, 为长期运动方案的制定提供依据。本文将从个体的反应时间、感觉灵敏度、记忆、执行功能等认知方面着手, 总结急性有氧运动及相关调节变量的作用, 综述急性有氧运动影响认知表现的生理机制。

1 急性有氧运动与认知表现

1.1 反应时间和感觉灵敏度

早期研究关注急性有氧运动对简单反应时、选择反应时等简单认知任务, 以及闪光融合临界频率的影响。研究发现, 急性有氧运动对简单认知任务表现有促进作用, 具体表现为反应时下降且正确率没有变化(Lambourne & Tomporowski, 2010)。急性有氧运动对反应时的影响作用受运动强度的调节, 随着运动强度由小强度增加到中、高强度, 反应时间的缩短程度随之加强(Davranche & Audiffren, 2004; Davranche, Burle, Audiffren, & Hasbroucq, 2006)。当急性有氧运动与认知任务同时进行时, 这种提升效果最为明显(Audiffren, Tomporowski, & Zagrodnik, 2008)。若结束急性有氧运动, 反应时则很快恢复到基线水平(Audiffren et al., 2008; Lambourne, Audiffren, & Tomporowski, 2009)。急性有氧运动对感觉灵敏度的影响, 主要表现为闪光临界融合频率增加, 感觉灵敏度提升(Davranche & Pichon, 2005)。

对于急性有氧运动提升简单认知任务表现的原因, 主要有两种解释。一种为运动提升了感觉灵敏度。Davranche和Audiffren (2004)要求被试分别进行小强度和中等强度的急性有氧运动, 并在运动过程中完成视觉选择反应时任务, 结果发现, 小强度和中等强度急性有氧运动后, 被试的选择反应时显著缩短, 闪光临界融合频率和警觉度也在运动后得到了提升。该结果提示急性有氧运动后反应时间的缩短可能归功于感觉灵敏度的提升。另一种解释是, 运动改善了动作技能效率, 加快了按键速度。Davranche, Burle, Audiffren和Hasbroucq (2005)在研究中增加了对肌电数据的记录, 以探索急性有氧运动对反应时的影响是在动作反应阶段实现, 还是在更上游的感觉信息加工阶段发生。结果发现, 急性有氧运动对这两个阶段均有促进作用, 表明反应时的缩短可以通过感觉加工和动作反应两个路径相继实现。

1.2 记忆

2003年, Tomporowski (2003)在综述文章中提出急性有氧运动对记忆编码和提取的影响微乎其微, 但是, 该论点受到了后续研究的质疑。Lambourne和Tomporowski (2010)的Meta回归分析研究发现, 急性有氧运动对记忆有促进作用, 并且效应量大于急性有氧运动影响执行功能、信息加工速度的效应量。Roig, Nordbrandt, Geertsen和Nielsen (2013)的元分析证实急性有氧运动可促进短时记忆和长时记忆的表现, 效应量分别达到中等(SMD = 0.15)和中等至较大(SMD = 0.52)水平。不难看出, 这些研究的结论尚存在分歧, 原因在于急性有氧运动对记忆的影响受到运动强度、记忆任务类型等因素的调节。

急性有氧运动对记忆的影响作用存在强度剂量效应。尽管Eich和Metcalfe (2009)发现, 高强度急性运动损害了记忆任务的表现, 但是, 该结论未得到后续研究的支持。Etnier等人(2016)以及Hötting, Schickert, Kaiser, Röder和Schmidt-Kassow (2016)的两项研究均发现高强度急性有氧运动可以提升被试24小时后的回忆成绩, 并且, 这种提升效果明显优于中小强度的效果。还有, Thomas等人(2016)使用程序性动作记忆任务, 检验不同强度急性有氧运动对记忆保持的影响, 发现高强度急性有氧运动组在1天和7天后的信息保持量都优于中等强度组, 再次证明了强度剂量效应的存在。

急性有氧运动对记忆的影响效果受到运动干预时间的调节。Labban和Etnier (2011)让被试在急性有氧运动后立即进行记忆任务的学习, 发现了运动对语义记忆的提升效应; 而急性有氧运动前进行记忆材料的学习, 则没有显著的增益效应。然而, Roig等人研究了急性有氧运动影响程序性记忆的时间点, 却呈现了截然相反的结论, 即, 学习后再进行运动干预, 能够更好地提升程序记忆的保持效果(Roig, Skriver, Lundbyejensen, Kiens, & Nielsen, 2012; Thomas, Beck, et al., 2016)。此外, McNerney和Radvansky (2015)的研究还发现, 无论记忆信息编码发生在急性有氧运动之前还是之后, 语义记忆和程序记忆效果均有所巩固。导致上述研究结论存在冲突的原因有两点。首先, 运功干预方案的差别。Labban等人让被试完成20分钟中等强度功率自行车骑行运动; Roig和Thomas的研究采用持续性高强度有氧运动干预方案; 而McNerney等人的运动干预方案则是2分钟的高强度冲刺跑。运动的持续时间有可能对急性有氧运动影响记忆的效果产生影响。其次, 记忆任务不同。急性有氧运动的发生时间对语义记忆和程序记忆的影响规律相反, 提示急性有氧运动也许通过不同的作用机制对语义记忆和程序记忆产生影响。

1.3 执行功能

执行功能是灵活调节和控制认知过程以实现目标的高级认知活动, 包括抑制控制、工作记忆刷新和转换三个子功能, 与身心健康(Chan, Shum, Toulopoulou, & Chen, 2008)、学业表现(Bull & Scerif, 2001)、社会化发展(Blakemore & Choudhury, 2006)等方面密切相关。Verburgh, Königs, Scherder和Oosterlann (2013)对已有的研究进行元分析, 发现急性有氧运动对儿童、青少年和成年人的执行功能均有促进作用。Ludyga, Gerber, Brand, Holsboer-Trachsler和Pühse (2016)的元分析研究将体适能水平、年龄、执行功能子成分等因素纳入考量, 同样发现中等强度急性有氧运动对执行功能的促进作用, 进一步证实急性有氧运动可暂时性地提升执行功能。

年龄是调节急性有氧运动对执行功能影响效果的重要变量。由于急性有氧运动提升执行功能的表现可能存在天花板效应, 致使执行功能较差的个体在急性有氧运动之后的受益显著大于执行功能较好的被试(Drollette et al., 2014), 处于认知退化阶段的老年人和发展阶段的青春期前儿童, 他们的执行功能在急性有氧运动之后的提升效应显著大于成年人和青春期少年(Ludyga et al., 2016; 蒋长好, 陈婷婷, 2013)。急性有氧运动对执行功能的提升效应对运动强度不敏感, 即使是10分钟、30%最大摄氧量的小强度运动也可以提升执行功能表现(Byun et al., 2014)。

急性有氧运动对抑制控制、工作记忆刷新、转换三个执行功能子成分的影响效果可能存在差异。多项研究发现, 急性有氧运动对抑制控制的影响效果显著高于另外两个子功能(Chen, Yan, Yin, Pan, & Chang, 2014; Drollette et al., 2014; Jäger, Schmidt, Conzelmann, & Roebers, 2014; Kamijo et al., 2009; Pindus et al., 2016), 说明抑制控制或许对急性有氧运动诱发的生理变化更为敏感。但是, Weng, Pierce, Darling和Voss (2015)却发现, 急性有氧运动提升了工作记忆刷新任务表现的同时, 并没有影响抑制控制功能; Gothe, Pontifex, Hillman和McAuley (2013)也证实中等强度的急性有氧运动同样不会促进抑制控制功能的提升; 与此同时, Verburgh, Königs, Scherder和Oosterlaan (2013)通过元分析发现, 中等强度急性有氧运动影响抑制控制、转换和刷新这三个子功能的各效应量之间并不存在显著性差异。这些研究结论彼此冲突, 其原因可能是认知任务测试时间窗口不同所致。这些研究普遍采用继时研究范式, 即先进行运动干预, 随后完成认知任务测试, 只是未统一测试时间的窗口。例如, Kamijo等人(2009)令被试在急性有氧运动后2分钟即开始认知任务测试, 发现了抑制控制表现的提升; 而Weng等人(2015)是在急性有氧运动后6~12分钟开始认知任务, 发现抑制控制的表现没有变化; Hillman, Snook和Jerome (2003)更是延长至运动后48分钟才开始认知任务测试, 最终未能发现急性有氧运动的干预作用。

此外, 当个体同时完成急性有氧运动和认知任务时, 两个过程同时竞争有限的脑血氧、血糖资源, 进而导致执行功能任务的表现不佳。Soga, Shishido和Nagatomi (2015)要求被试进行运动的同时, 完成执行功能的任务测试, 发现中等强度的急性有氧运动选择性地影响执行功能, 青少年即使在急性有氧运动时得以维持抑制控制的表现水平不变, 但工作记忆刷新的表现明显下降。

2 急性有氧运动影响认知表现的调节变量

2.1 运动强度

Yerkes和Dodson曾提出唤醒水平和运动表现呈倒U型曲线的关系, 而唤醒水平和运动强度之间存在同样的曲线关系(Kamijo et al., 2004), 因此, 许多研究者提出并证实急性有氧运动强度之后的认知表现和运动强度之间的关系也呈倒U曲线状, 该观点得到了多个研究的支持(Davranche & Audiffren, 2004; Loprinzi & Kane, 2015; 王莹莹, 周成林, 2014)。例如, Kamijo, Nishihira, Higashiura和Kuroiwa (2007)发现被试完成小、中强度的急性有氧运动之后, 其注意资源分配的效率显著高于高强度急性有氧运动的作用(Kamijo et al., 2007)。随后, Kamijo等人(2009)又进一步发现被试完成中等强度的急性有氧运动之后, 抑制控制的提升幅度显著大于小强度运动的影响效果。中等强度的急性有氧运动亦能显著提高个体的专注力, 而小强度和高强度的急性有氧运动则无法影响注意、认知灵活性等认知过程(Loprinzi & Kane, 2015)。不仅如此, McMorris和Hale (2012)的元分析研究发现, 中等强度的急性有氧运动影响认知任务的效应量显著大于小强度和高强度急性有氧运动的效应量。

对于不同类型的认知任务来说, 急性有氧运动的强度与认知表现改变之间的关系呈现不同趋势。对于较为简单的感知觉任务来说, 急性有氧运动的强度和认知表现呈线性关系, 在达到最大摄氧量之前, 运动强度越大, 认知表现越好(Lambourne et al., 2009; Lambourne & Tomporowski, 2010)。对于较高级的认知任务来说, 当前的研究结果则存在分歧。一些研究认为急性有氧运动的强度和认知表现没有关系, 比如, Sandoff (2015)以多发性硬化患者为研究对象, 发现小、中、高强度的急性有氧运动可以减少被试完成Flanker任务的反应时, 但反应时的减少程度并没有显著差异; Davranche, Brisswalter和Radel (2015)使用Simon任务, 同样发现急性有氧运动对认知控制的影响效果与运动强度无关。另外一些研究则发现急性有氧运动的强度和认知表现之间存在关系, 比如, Córdova等人(2009)证实接近无氧阈(Anaerobic threshold)的高强度急性有氧运动对老年人执行功能的提升效果最好; 陈爱国等人(2011)发现, 不同强度的急性有氧运动对执行功能的抑制控制、刷新和转换三个子功能的影响效果存在差异。因此, 对于执行功能、认知控制等高级认知功能来说, 急性有氧运动强度所产生的效应难以一概而论, 不能忽视被试特征、认知任务特征等因素的作用。

在讨论运动强度时, 有必要对力竭状态进行单独分析。力竭是指肌肉或器官完全不能维持运动的状态。研究表明, 长时间的高强度运动导致个体处于力竭状态时, 其认知表现将受到损害(Ando et al., 2005; Chmura & Nazar, 2010)。Schmit等人(2015)使用功能性近红外光谱技术(fNIRS)检测个体处于力竭过程时的额叶血氧变化情况, 发现与高强度运动同时进行的Flanker任务表现并未受到影响。反倒在运动初期, 个体的认知加工效率有所提升, 当接近力竭状态时, 运动诱发的过度换气导致皮层血流量下降(Ogoh & Ainslie, 2009; Rooks, Thom, McCully, & Dishman, 2010), 脑血氧值急剧下降, 冲动性错误倾向随之增加, 对错误激活的校正效率下降, 不同脑区竞争有限的皮层资源优先使用权, 最终导致了认知效率的下降(Dietrich, 2003; Dietrich & Audiffren, 2011)。

综上所述, 急性有氧运动强度和认知表现提升之间的倒U形曲线关系并不适用于所有的认知任务, 在个体呈现力竭状态之前, 感知觉任务表现与运动强度之间呈线性关系, 随着认知任务难度的增加, 两者之间的关系更为复杂, 受到多种因素的调控。

2.2 运动方式

功率自行车和跑步机作为急性有氧运动研究中最常用的器械, 相应的骑行和跑步两种运动方式对认知表现的影响效果存在差异。元分析研究表明, 在运动-认知任务同时范式中, 跑步会损害认知表现, 而功率自行车则不会; 在运动-认知任务继时范式中, 骑行对认知表现的提升效果更为明显(Lambourne & Tomporowski, 2010)。

骑行和跑步都是使用大肌肉群的有氧运动, 但二者的肌肉使用模式有所不同, 有氧和厌氧运动的能量分配也存在差异。另外, 功率自行车和跑步机的器材特性, 也会影响人体的跑步状态, 跑步机比功率自行车需要个体更多注意平衡控制和上下肢协调; 功率自行车对个体的能量代谢的需求少于跑步机, 几乎不需要人体进行垂直位移(Bijker, de Groot, & Hollander, 2002)。而且, 个体在跑步过程中会产生身体内部噪音干扰, 这种干扰可能是跑步提升认知表现效益差于功率自行车的原因。所以, 鉴于功率自行车既可以提升生理唤醒水平, 又不会产生内部噪音, 近10年的绝大多数研究以其作为急性有氧运动干预方式。

2.3 研究的时间范式

急性有氧运动干预研究的常用范式有两种, 运动-认知任务同时范式与运动后进行认知任务测试的继时范式。元分析研究表明, 以正确率作为因变量, 继时范式的运动干预效应量高于同时范式; 但是, 以反应时作为因变量, 两种范式的效应量并没有显著性差异(McMorris & Hale, 2012)。

在同时范式的情况下, 有研究发现急性有氧运动可以提升认知表现(Chang et al., 2012; Davranche & Audiffren, 2004; Davranche et al., 2015; Lambourne et al., 2009; McMorris, Sproule, Turner, & Hale, 2011), 但是, 也有研究持相反的观点(Davranche & McMorris, 2009)。认知任务性质不同是导致结论不一致的主要原因, 急性有氧运动可以提升同时进行的简单反应时任务的表现, 但对高级认知功能没有影响, 甚至有损害作用。例如, Lambourne等人(2009)的研究急性有氧发现运动可提升感觉灵敏度, 对执行功能没有影响; Soga等人(2015)发现, 与急性有氧运动同时进行的抑制控制并未受到影响, 工作记忆表现则有所损害。对此, Lambourne和Tomporowski (2010)通过元分析发现运动对认知任务的消极干扰效应只出现在前20分钟, 之后, 锻炼诱发的唤醒将提高被试在简单反应时任务和快速决策行为的表现。

在继时范式的情况下, 个体完成急性有氧运动后立即进行认知任务测试, 其运动干预的促进效应最大(Barella, Etnier, & Chang, 2010), 随着时间的推移, 这种促进效应逐渐降低直至消失(Hung, Tsai, Chen, Wang, & Chang, 2013)。但是, 元分析表明急性有氧运动之后, 被试立即测试认知任务(效应量:0.11)和延迟测试(效应量:0.1)之间仅有微弱的差别(Chang et al., 2012)。不仅如此, 急性有氧运动干预后, 若等待心率恢复到静息心率后再进行认知任务测试, 急性有氧运动对认知表现的促进效应则完全消失(Hillman et al., 2003; Themanson & Hillman, 2006)。

2.4 受试者的生理特征

2.4.1 年龄

年龄是影响急性有氧运动干预认知任务效果的重要调节变量。Chang等人(2012)的元分析研究发现急性有氧运动对老年人和青少年认知功能的影响效果显著大于成年人群体。不仅如此, 中等强度的急性有氧运动对青春期前儿童和老年成人执行功能的影响最为明显, 对青春期少年执行功能影响的效应量比较小(Ludyga et al., 2016)。然而, Verburgh等人(2013)并未发现有氧急性运动对青春期前、青春期和成年初期群体执行功能的影响差异。

上述元分析研究结论不一致的原因在于纳入标准不同。Chang的研究分析了急性有氧运动对认知的影响, 未对认知功能进行细分; Verbugh等人仅选取了以执行功能为观测变量的研究纳入分析; Ludyga等人的元分析中进一步限定了运动强度, 仅分析了中等强度有氧运动对执行功能的影响(Chang et al., 2012; Ludyga et al., 2016; Verburgh et al., 2013)。

不难看出, 急性有氧运动对脑部生理结构处于变化时期的群体影响最为显著, 比如, 与脑部结构处于相对稳定期的成年人相比, 处于发育过程中的青春期前儿童和处于退化阶段的老年人在急性有氧运动后的获益更大(Ludyga et al., 2016)。但是, 以成人为对象的研究绝大多数选择18~30岁之间年轻人为被试, 较少涉及30~50岁之间的健康中年人。所以, 通过关注中年群体以丰富研究对象的年龄层, 并且进一步细分认知功能, 将有助于明晰年龄调节急性有氧运动与认知表现之间关系的完整机制(Ludyga, Gronwald, & Hottenrott, 2015)。

2.4.2 体适能水平

体适能水平与认知功能之间的关系密切, 与海马体积、基底核脑容积等均存在不同程度的相关(Chaddock, Erickson, et al., 2010)。高体适能水平的个体在完成认知任务时, 注意资源分布更为优化, 在记忆编码和提取(Chaddock, Hillman, Buck, & Cohen, 2010)、回忆(Raine et al., 2013)等认知过程的表现优于低体适能组。但是, 不同体适能群体从急性有氧运动中的受益程度是否存在差异?研究者们尚未达成共识。

Hogan等人(2013)比较了不同体适能青少年在急性有氧运动后的Flanker任务表现, 发现低体适能青少年的正确率和反应时显著低于高体适能组, 但低体适能组从运动中的受益大于高体适能组(Hogan et al., 2013)。然而, 不同体适能老年人群体从急性有氧运动中的受益情况却呈相反趋势, 反倒是高体适能老年人的执行功能呈现更大的提升效应(Chang, Chu, Wang, Song, & Wei, 2015; Netz, Argov, & Inbar, 2009)。不同的体适能水平也未必产生差异性的调节效果, Chang等人(2014)就发现中等强度急性有氧运动可提升个体在Stroop任务上的表现, 且提升效益不受体适能水平的影响。

体适能水平的调节作用可能与研究所采用的时间范式存在交互关系。在运动-认知任务同时范式的情况下, 体适能水平可以调节急性有氧运动和认知任务表现提升之间的关系(Chang et al., 2012); 在运动-认知任务继时范式的情况下, 适能水平尚未被证实具有调节作用(Ludyga et al., 2016)。产生这种交互现象的原因在于, 对于高体适能水平的个体来说, 进行运动的同时完成认知任务, 使用较少的皮层资源即可维持运动表现(Ludyga et al., 2015), 从而将更多的资源可用于认知任务, 呈现更好的认知表现。当运动停止后, 无论个体的体适能水平是否存在差异, 可供其使用的资源不再有差别, 因此, 体适能水平便不能通过影响资源的使用情况以发挥调节作用。

3 急性有氧运动影响认知表现的理论解释

3.1 唤醒假说

Colin Davey最早从理论角度解释急性有氧运动与认知表现之间的关系时, 便从唤醒视角出发, 认为运动是一种应激源(Davey, 1973), 可以激活自主神经系统, 提升生理与心理的唤醒水平, 个体在运动期间出现脑部新陈代谢加快, 大脑皮层血流量增加等生理变化(Querido & Sheel, 2007; Yerkes & Dodson, 1908), 可以由此优化认知资源的分配, 促进认知加工效率的提升(Audiffren, Tomporowski, & Zagrodnik, 2009)。

唤醒水平和行为表现之间呈倒U型曲线关系(Yerkes & Dodson, 1908), 而运动作为唤醒水平的有效诱发因素, 由此推断, 运动强度和认知功能改变之间的关系也应符合该趋势。研究证明, 运动可通过诱发唤醒使神经系统做出神经递质调节反应(Meeusen & de Meirleir, 1995), 使个体呈现最优化的认知表现(Audiffren et al., 2008)。但是, 随着运动强度和时间的持续增加, 神经信号噪音反而使个体的认知表现下降(Kashihara, Maruyama, Murota, & Nakahara, 2009)。此外, 多巴胺能系统的激活和前额叶的认知表现之间, 同样呈倒U型曲线关系, 当多巴胺激动剂浓度过高时, 与前额叶有关的认知功能表现将受到损害(Arnsten & Li, 2004)。ERP研究发现, 高强度运动导致P300波幅减小, 中等强度急性有氧运动则增大了P300波幅增大, 说明中等强度急性有氧运动提供了最佳的唤醒水平, 有助于增加认知任务所需的注意资源(Kamijo et al., 2004)。借助近红外脑成像技术测量额叶皮层血氧含量, 研究发现急性有氧运动对认知表现的提升、唤醒水平以及相关皮层的激活水平均呈正相关(Byun et al., 2014)。伴随急性有氧运动而产生的高水平生理唤醒, 对简单认知任务和自动化任务表现的提升效应最明显(Tomporowski, 2003)。然而, 急性有氧运动影响认知表现的倒U型关系并非适用于所有的认知任务。如前所述, 高强度急性有氧运动对记忆、感知觉任务的促进作用均优于中、小强度运动。

在急性有氧运动与认知功能的关系中, 个体的唤醒水平起到部分中介作用, 通过加强认知任务相关脑区的激活, 诱发脑电活动、神经递质浓度、血液动力学等方面的变化, 影响认知表现。值得注意的是, 唤醒并非急性有氧运动影响认知表现的唯一中介路径, 例如, 运动诱发的积极情绪也会直接影响执行功能等高级认知功能(Ekkekakis, Parfitt, & Petruzzello, 2011; Reed & Ones, 2006)。

3.2 额叶功能减退假说

额叶功能减退(hypofrontality)指前额叶血流量下降, 新陈代谢减慢, 常见于精神分裂症、多动症、抑郁症等精神疾病患者, 通常伴随着去甲肾上腺素传递的增加和多巴胺能神经传递的减少(Pratt, Winchester, Egerton, Cochran, & Morris, 2008)。Dietrich (2003)用暂时性前额叶功能衰退假说(Transit Hypofrontality Theory, THT)解释运动-认知任务同时范式下运动对认知表现的损害现象(Dietrich, 2003)。

THT理论认为, 个体在运动过程中, 运动和感觉整合系统被持续性激活, 占用了有限的信息处理资源, 导致血氧和血糖资源被分配到运动皮层以应对长时间、高强度运动所导致的肌肉疲劳, 与此同时, 与运动无关的神经网络则受到临时抑制, 前额叶皮层的血流量和血氧含量开始下降。Dietrich和Sparling (2004)发现, 运动选择性损伤了同时进行的涉及前额叶的认知任务, 为该理论提供了支持证据。但是, Rooks等人使用fNIRS观测渐增型急性有氧运动的脑皮层血液动力学变化情况, 发现小、中等强度运动可以逐渐增加皮层氧合血红蛋白含量, 当运动强度增加至高强度时, 血氧和血流水平依然保持稳定, 直至力竭时, 血氧水平方才开始急剧下降(Rooks et al., 2010), 但是, 该结果无法解释同时范式中, 中、高强度急性有氧运动对执行功能的损害现象(Davranche, Hall, & McMorris, 2009; Pontifex, Hillman, Fernhall, Thompson, & Valentini, 2009)。

Dietrich和Audiffren (2011)随后对THT理论进行了修订, 提出了“网状结构激活和额叶功能减退模型” (Reticular-activating hypofrontality, RAH) (Dietrich & Audiffren, 2011), 具体包含网状结构激活和额叶功能减退两个截然相反的机制。基于信息加工的双系统理论(Dienes & Perner, 1999), RAH分别讨论了运动对内隐系统和外显系统的影响。其中, 网状结构激活过程涉及神经递质能系统的激活, 可促进伴随运动过程同时进行的内隐认知信息加工; 额叶功能减退基于资源有限说, 认为个体在追求最佳动作表现时, 与前额叶相关的外显系统难以获得充足资源而损害认知功能。然而, RAH模型并未得到所有研究结果的支持, Tempest等人(2017)使用60分钟急性有氧运动干预方案, 发现个体进行高强度的急性有氧运动时, 前额叶的血氧含量先是小幅提升, 之后维持稳定, 完成Flanker任务的反应时间缩短, 但工作记忆的表现受损。

3.3 神经内分泌模型

Cooper (1973)从神经内分泌学视角提出儿茶酚胺假说(Catecholamines Hypothesis)解释急性有氧运动对认知表现的影响机制, 认为急性有氧运动可以增加脑内多巴胺(DA)和去甲肾上腺素(NE)的浓度, 进而可以激活个体的网状结构, 提高生理唤醒度, 促进认知表现。

儿茶酚胺假说得到了许多动物实验的支持(McMorris, 2016; Meeusen et al., 1997)。以人类为被试的研究, 受限于研究伦理和技术手段, 仅限于测量人体外周血中的DA和NE浓度。McMorris, Collard, Corbett, Dicks和Swain (2008)的研究发现急性有氧运动可提高人体血清中的DA和NE代谢物浓度, 回归分析的结果显示急性运动强度、儿茶酚胺类物质浓度和认知表现之间存在相关关系, 但未发现儿茶酚胺类物质浓度升高可直接影响认知功能的表现。脑内DA和NE水平与前额叶相关的认知功能表现关系密切(Berridge et al., 2006), 虽然已有研究发现外周血儿茶酚胺浓度变化会引发脑内浓度的联动变化, 但是, 外周血和脑内儿茶酚胺浓度的互动关系及机制、运动强度与时间同认知任务的互动过程, 以及脑内儿茶酚胺、5-羟色胺、糖皮质激素和内源性神经营养因子之间的互动关系尚不明晰, 以至于儿茶酚胺在急性有氧运动与认知表现互动关系中所扮演的角色仍有待进一步探索。

急性有氧运动可以通过激活三个单胺能系统以提高个体的认知表现, 分别为5-羟色胺能系统、去甲肾上腺素能系统和多巴胺能系统(Meeusen & de Meirleir, 1995)。5-羟色胺能系统源自中缝核的细胞体, 广泛分布于大脑和脊髓, 通过调节儿茶酚胺活动的激活效应, 进而加强对行为抑制的控制(Meeusen, Watson, Hasegawa, Roelands, & Piacentini, 2006)。去甲肾上腺素能系统源自蓝斑, 主要在前脑进行表达, 可调节警觉过程, 维持高应激条件下的刺激辨别, 该系统活动增加可提高神经活动信噪比(Moxon, Devilbiss, Chapin, & Waterhouse, 2007), 提升记忆效果(Segal, Cotman, & Cahill, 2012)。多巴胺能系统源自位于黑质致密部和中脑腹侧被盖区的细胞体, 作用于纹状体、边缘系统和前额叶皮层, 这些通路共同作用激活行为输出(Robbins & Everitt, 2007)。

除了神经递质和交感神经系统, 下丘脑脑垂体肾上腺轴(HPA)和皮质醇在急性有氧运动与认知表现互动关系中发挥的作用也日益受到关注(McMorris, Turner, Hale, & Sproule, 2016)。运动作为一种应激源, 皮质醇水平在个体的运动过程中不断增加(Fryer et al., 2012)。皮质醇伴随运动强度增加或时间累积而持续增多, 则可能有损认知表现。

3.4 神经营养因子

运动诱发的脑源性神经营养因子(BDNF)浓度变化与脑功能提升存在显著相关(Loprinzi, Herod, Cardinal, & Noakes, 2013)。BDNF是一种直接参与神经元和突触生长的神经营养因子。给大鼠注射BDNF抗体抑制海马BDNF的表达, 可损害大鼠空间学习和记忆功能(Mu, Li, Yao, & Zhou, 1999)。Cirulli, Berry, Chiarotti和Alleva (2004)给大鼠注射外源性神经营养因子后, 大鼠在Morris水迷宫任务上的表现明显提升(Cirulli et al., 2004)。通过检测人类外周血BDNF水平, 发现其与海马体积、空间记忆功能有关(Erickson et al., 2010)。

急性有氧运动与外周血BDNF浓度之间的关系受运动强度的影响较大, 中等和高强度急性有氧运动可促进外周血BDNF浓度的提升, 但是, 受运动形式、运动时间的影响较小, 15分钟高强度自行车骑行和4小时划船运动均能提升外周血BDNF的浓度(Goekint et al., 2008; Knaepen, Goekint, Heyman, & Meeusen, 2010)。有研究建议20~40分钟的中、高强度运动可使血清BDNF浓度增量达到最大值(Schmidt-Kassow et al., 2012)。其实, 运动对BDNF浓度的影响是短暂的, 仅可维持10~60分钟的提升效果, 待个体恢复到静息心率后10分钟, BDNF浓度即降至基线水平(Loprinzi et al., 2013)。Griffin的研究发现, 高强度急性有氧运动提升了被试的认知表现, 改变了外周血清BDNF浓度, 研究还发现, 5周长期有氧训练改变了急性运动引起的血清BDNF浓度变化(Griffin et al., 2011)。

不难看出, 急性有氧运动与外周血BDNF浓度的关系目前尚未达成共识。Chang等人(2017)发现被试进行中等强度急性有氧运动后, 完成Stroop任务的反应时缩短, 但其外周血BDNF浓度没有变化, 根据脑电数据的结果, 这种执行功能表现的提升, 可能因为运动诱发了注意资源增加, 或是神经资源的再分配所致(Chang et al., 2017)。Gapin, Labban, Bohall, Wooten和Chang (2015)令ADHD患者进行中等强度急性有氧运动, 也未发现外周血血清BDNF浓度发生相应改变。或许, 急性有氧运动、外周血BDNF和认知表现三者之间的关系, 只能通过涉及海马参与的认知过程进行探讨, 才得以明晰三者之间的协同变化关系(Piepmeier & Etnier, 2014; Winter et al., 2007)。

除了BDNF之外, 其他神经营养因子也对运动诱发的认知功能改变过程存在一定影响。比如, 血管内皮细胞生长因子(VEGF)和第一型胰岛素样生长因子(IGF-1)可调节突触可塑性(Licht et al., 2011), 与儿童智商存在正相关关系(Gunnell, Miller, Rogers, & Holly, 2005)。但是, 这些神经营养因子在运动过程中的动态变化情况, 以及其与认知表现之间的关系, 仍有待进一步研究。

3.5 自我控制力量的过度补偿理论

自我控制力量模型(Strength Model of Self- control)认为自我控制需要消耗有限的心理资源(或称为力量、能量) (Baumeister, Bratslavsky, Muraven, & Tice, 1998), 可用资源的多少决定了控制行为的成功与失败, 当用于自我控制的资源被使用后, 将在短期内下降, 出现“自我损耗效应” (Ego-depletion Effect), 但是, 经过休息后即可得到恢复(Baumeister, Gailliot, Dewall, & Oaten, 2006)。Audiffren和André (2015)认为自我控制力量模型可以解释运动-认知任务同时范式中, 急性有氧运动损害认知表现的原理, 因为运动和认知任务同时竞争有限的意志力资源, 在保证运动强度的情况下, 认知表现会受损。可是, 自我控制力量模型难以解释继时范式中急性有氧运动对认知表现的促进现象。因为较高强度的急性有氧运动是一项消耗自我控制资源的任务, 当个体进行中高强度急性有氧运动之后, 进入自我控制损耗状态, 理应降低后续的损耗类任务绩效, 但是, 个体在急性有氧运动后却可提升认知表现, 与该模型的预测结果相悖。

4 总结和展望

通过归纳急性有氧运动对认知功能的影响效果、调节变量、影响机制, 证实急性有氧运动可以暂时性地改变个体的认知表现, 且两者之间的关系受到运动强度、运动与认知任务的相对时间、运动方式、个体的生理学特征等多种因素的调节。急性有氧运动可以诱发生理唤醒水平的提升, 进而促进感知觉和内隐信息加工的表现, 并且, 在运动强度和时间累计使个体达到力竭状态之前, 两者之间基本呈线性关系。在记忆方面, 急性有氧运动可以提升随后进行的记忆任务编码, 且高强度运动的提升效果优于中、小强度。同时, 个体完成急性有氧运动后的执行功能表现亦能得到提升, 尤其是处于大脑生理变化期的群体, 其执行功能受运动影响的效益更大。运动是促进儿童青少年认知功能发展, 提升成年人认知表现, 缓解老年人认知能力下降的重要途径(Prakash, Voss, Erickson, & Kramer, 2015), 而个体认知功能对急性有氧运动的短暂反应是长期运动干预的潜在基础。已有研究为急性有氧运动和认知表现之间的关系提供了大量的证据, 但面对诸多尚存争议的问题及矛盾性结论, 未来的研究仍需从以下几个方面不断深入探索。

首先, 进一步明晰运动强度、持续时间、运动方式等因素的调节机制, 从而探索急性有氧运动、长期规律运动、认知表现的临时性改变与认知表现长期提升四者之间的内在联系, 为开具“运动处方”提供科学证据支持。毕竟, 一次性急性有氧运动和长期规律运动对认知表现的影响效果和作用机制存在差异。急性有氧运动对执行功能的积极促进作用已得到大量研究证据的支持, 但长期规律运动是否对执行功能产生持续性改变, 已有结论尚存分歧(Martin et al., 2018; Verburgh et al., 2013; Young, Angevaren, Rusted, & Tabet, 2015)。这种差异主要体现在生理机制方面, 急性有氧运动通过改变脑皮层血流量(Querido & Sheel, 2007)、血氧含量(Secher, Seifert, & van Lieshout, 2007)、血液中的BDNF浓度、儿茶酚胺类物质分泌等对个体的认知功能产生积极影响, 而长期运动则可能通过促进脑血管新生、神经发生等神经生物学变化促进个体的认知表现。所以, 面对急性有氧运动仅带来暂时性的认知改变, 若能将其联合长期规律运动进行整合研究, 在急性有氧运动干预认知表现的研究基础之上, 探索运动对认知表现的长期、持续性提升作用, 更具有现实意义。

第二, 探索不同运动形式对认知表现的影响效果及作用机制。目前, 急性有氧运动干预认知表现的研究普遍采用功率自行车骑行和跑步两种运动方式, 使用心率作为评估强度的主要指标。然而, 其他运动形式对认知表现的影响规律或有不同, 心率亦不应是唯一的运动形式评估与分类指标。比如, 有研究发现瑜伽对执行功能的提升效果优于跑步(Gothe et al., 2013); 太极拳干预帕金森病人的效果优于拉伸等运动方式(Li et al., 2012); 急性阻抗运动可以提升执行功能的刷新子成分(Chang & Etnier, 2009)、情景记忆(Weinberg, Hasni, Shinohara, & Duarte, 2014)等认知功能。所以, 探索跳绳、游泳、太极等不同急性有氧运动形式对认知表现的影响规律, 可提高急性有氧运动干预研究的生态效度。

第三, 使用多学科研究手段探索急性有氧运动影响认知功能的机制。当前, 证实急性有氧运动影响认知功能的证据主要来自行为学领域的研究, 但是, 急性有氧运动影响认知功能的作用机制尚不明晰, 现有的唤醒理论、儿茶酚胺理论、前额叶功能衰退理论等均未得到有力证据的支持。未来的研究可借助脑成像技术、脑电等研究手段, 综合行为科学、生物工程、神经科学等多学科视角, 以回答“为什么急性有氧运动可改变认知表现”这一问题。

第四, 探索急性有氧运动对特殊人群认知功能的影响情况。现有研究普遍选用成年初期个体为被试, 少数研究涉及特殊人群, 如轻度认知障碍患者(Segal et al., 2012), 吸烟人群(Hatzigeorgiadis et al., 2016), 脑瘫儿童(Maltais et al., 2016), 多发性硬化患者(Sandroff et al., 2015), ADHD患者(Piepmeier et al., 2015)和毒品吸食者(Chang, Liu, Yu, & Lee, 2012)。未来的研究若提升研究对象的异质性, 尤其是扩展至身心处于非健康状态的群体, 则可为“运动是良药”理念的推广, 提供更多的科学证据。

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DOI:10.1523/JNEUROSCI.6251-09.2010      URL     [本文引用: 1]

Etnier J. L., Wideman L., Labban J. D., Piepmeier A. T., Pendleton D. M., Dvorak K. K., & Becofsky K . ( 2016).

The effects of acute exercise on memory and brain-derived neurotrophic factor (BDNF)

Journal of Sport and Exercise Psychology, 38( 4), 331-340.

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Capillary cortisol sampling during high-intensity exercise

International Journal of Sports Medicine, 33( 10), 842-845.

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Acute exercise is associated with specific executive functions in college students with ADHD: A preliminary study

Journal of Sport and Health Science, 4( 1), 89-96.

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No influence of noradrenaline manipulation on acute exercise-induced increase of brain-derived neurotrophic factor

Medicine and Science in Sports and Exercise, 40( 11), 1990-1996.

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Gothe N., Pontifex M. B., Hillman C., & McAuley E . ( 2013).

The acute effects of Yoga on executive function

Journal of Physical Activity and Health, 10( 4), 488-495.

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Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males

Physiology & Behavior, 104( 5), 934-941.

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78 An acute bout of aerobic exercise improves performance of the face–name task (an index of hippocampal function), but not the Stroop task, in young male subjects. 78 This cognitive improvement is associated with increased concentration of BDNF in the serum. 78 Chronic training, resulting in improved VO2 max, improves performance of the face–name task and alters the profile of circulating BDNF. 78 The data suggest a role for BDNF in exercise-induced cognitive enhancement in humans.

Gunnell D., Miller L. L., Rogers I., & Holly J. M . ( 2005).

Association of insulin-like growth factor I and insulin-like growth factor-binding protein-3 with intelligence quotient among 8- to 9-Year-old children in the Avon longitudinal study of parents and children

Pediatrics, 116( 5), e681-e686.

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Background. Insulin-like growth factor I (IGF-I) is a hormone that mediates the effects of growth hormone and plays a critical role in somatic growth regulation and organ development. It is hypothesized that it also plays a key role in human brain development. Previous studies have investigated the association of low IGF-I levels attributable to growth hormone receptor deficiency with intelligence but produced mixed results. We are aware of no studies that investigated the association of IGF-I levels with IQ in population samples of normal children.Objectives. To investigate the association of circulating levels of IGF-I and its principle binding protein, IGF-binding protein-3 (IGFBP-3), in childhood with subsequent measures of IQ.Methods. The cohort study was based on data for 547 white singleton boys and girls, members of the Avon Longitudinal Study of Parents and Children, with IGF-I and IGFBP-3 measurements (obtained at a mean age of 8.0 years) and IQ measured with the Wechsler Intelligence Scale for Children (at a mean age of 8.7 years). We also investigated associations with measures of speech and language based on the Wechsler Objective Reading Dimensions test (measured at an age of 7.5 years) and the Wechsler Objective Language Dimensions test (listening comprehension subtest only, measured at an age of 8.7 years). For some children (n = 407), IGF-I (but not IGFBP-3) levels had been measured at 655 years of age in a previous study. Linear regression models were used to investigate associations of the IGF-I system with the measures of cognitive function.Results. Three hundred one boys and 246 girls were included in the sample. IGF-I levels (mean ± SD) were 142.6 ± 53.9 ng/mL for boys and 154.4 ± 51.6 ng/mL for girls. IQ scores (mean ± SD) were 106.05 ± 16.6 and 105.27 ± 15.6 for boys and girls, respectively. IGF-I levels were associated positively with intelligence. For every 100 ng/mL increase in IGF-I, IQ increased by 3.18 points (95% confidence interval [CI]: 0.52 to 5.84 points). These positive associations were seen in relation to the verbal component (coefficient: 4.27; 95% CI: 1.62 to 6.92), rather than the performance component (coefficient: 1.06; 95% CI: 611.67 to 3.78), of IQ. There was no evidence that associations with overall IQ differed between boys and girls. In a data set with complete information on confounders (n = 484), controlling for birth weight (adjusted for gestation), breastfeeding, and BMI slightly strengthened the associations of IGF-I levels with IQ. Additionally controlling for maternal education and IGFBP-3 levels attenuated the associations (change in IQ for every 100 ng/mL increase in IGF-I levels: 2.51 points; 95% CI: 610.42 to 5.44 points). The weakening of associations in models controlling for markers of parental socioeconomic position and education could reflect shared influences of parental IGF levels on parents9 own educational attainment and their offspring9s IGF-I levels. In unadjusted models examining associations of Wechsler Objective Reading Dimensions and Wechsler Objective Language Dimensions test scores with IGF-I levels, there was no strong evidence that performance on either of these tests was associated with circulating IGF-I levels, although positive associations were seen with both measures. Associations between IGF-I levels measured at age 5 and Wechsler Intelligence Scale for Children scores (n = 407) were similar to those for IGF-I levels measured at age 7 to 8. For every 100 ng/mL increase in IGF-I levels at 5 years of age, IQ increased by 2.3 points (95% CI: 610.21 to 4.89 points).Conclusions. This study provides some preliminary evidence that IGF-I is associated with brain development in childhood. Additional longitudinal research is required to clarify the role of IGF-I in neurodevelopment. Because IGF-I levels are modifiable through diet and other environmental exposures, this may be one pathway through which the childhood environment may influence neurodevelopment.

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