摘 要 记忆巩固通常被认为是一个缓慢的过程, 需要数年甚至更长时间。然而, 新的研究显示, 当新信息与已有图式一致或采用特定编码方式时, 记忆能够迅速巩固。此外, 睡眠和提取对记忆的促进也被认为与记忆的快速巩固有关。这些现象揭示了记忆快速巩固两种可能的途径:基于图式的学习和记忆重复再激活。在未来的研究中, 可以进一步探索海马在皮层学习中的作用, 干扰抑制对记忆巩固的意义, 以及在理解记忆快速巩固两面性的基础上, 从适应环境的视角来考察记忆巩固的快与慢。
关键词 记忆巩固, 海马, 图式, 再激活
分类号 B842
1 引言
早期的研究发现, 当海马受到损伤时, 病人不仅难以形成新的情景记忆, 还会出现回溯性记忆损伤, 即失去海马损伤前一段时间内所发生事件的记忆, 而更久远的记忆则不受影响(Squire etal., 1975)。为了解释这一现象, 研究者提出了记忆巩固这一概念, 认为依赖海马的记忆会逐渐巩固到皮层, 因此记忆痕迹在形成初期依赖海马, 而一旦巩固完成, 其存储和检索就不再依赖海马(Squire & Alvarez, 1995)。准确来说, 巩固是指将新获得的记忆转变为更稳定、持久的记忆状态的过程(Dudai, 2012; Squire et al., 2015), 它包含“突触/细胞巩固”和“系统巩固”两个层面的含义。“突触/细胞巩固”是指编码后短时间内发生的细胞激活和突触变化(Gisquet-Verrier & Riccio, 2019; Hardt et al., 2010)。“系统巩固”则是指在更长的时间尺度上, 记忆表征在大脑网络中的重组(Dudai et al., 2015; Winocur & Moscovitch, 2011)。通常这也意味着情景记忆的语义化与图式化(Renoult etal., 2019; Sekeres et al., 2018)。本文探讨记忆的快速巩固, 但这里主要是指快速的“系统巩固”。
早期对记忆巩固的观察主要来自海马损伤的失忆症病人, 根据内侧颞叶不同的损伤程度, 受损的记忆能追溯到几年(Manns et al., 2003; Squire et al., 1975)甚至几十年前(Bayley et al., 2006; Bright et al., 2006)。因此, 传统上, 记忆巩固被认为是一个十分缓慢的过程(Frankland & Bontempi, 2005; Squire et al., 2004)。然而新的研究表明, 在某些情况下记忆能够迅速巩固。例如, 一项开创性的研究发现, 先前类似的学习经验能让新的记忆在48小时之内就不再依赖海马(Tse et al., 2007); 而某些特殊编码方式也被发现能促进快速的皮层学习(D’Angelo et al., 2015; Sharon et al., 2011); 此外, 睡眠(Klinzing et al., 2019)和提取(Antony etal., 2017)对记忆的促进也被认为与记忆快速巩固有关。这些发现涵盖了不同的研究领域, 相互之间存在怎样的关联?而记忆又是如何实现快速巩固的呢?本文先回顾了记忆巩固的主要理论, 然后梳理了记忆快速巩固的相关证据, 并分析总结了两种快速巩固的途径, 最后对未来研究方向进行了展望。
2 记忆巩固主要理论
2.1 标准巩固理论
标准巩固理论(Standard Consolidation Theory, SCT)提出了记忆巩固的概念, 半个多世纪以来对记忆各领域的研究影响深远。SCT的提出最初是为了解释H.M. (Scoville & Milner, 1957)和其他内侧颞叶损伤病人出现的回溯性记忆受损(综述见Squire et al., 2015)。SCT认为记忆痕迹起源于大脑皮层对事件的反应性激活, 海马记录并存储了这种激活模式, 因此提取这些记忆高度依赖于海马(Teyler & DiScenna, 1986)。而随着时间的推移, 皮层上直接的相互联结增强, 于是记忆的存储和检索就不再需要海马的参与(McClelland et al., 1995; Squire & Zola-Morgan, 1991)。这就导致越久远的记忆受海马损伤的影响越小, 出现回溯记忆受损的时间梯度效应(Squire et al., 2015)。这一效应在失忆症病人(Penfield & Milner, 1958; Scoville & Milner, 1957)和动物研究(Anagnostaras et al., 1999; Zola-Morgan & Squire, 1990)中得到大量证实, 进而支持了SCT的基本观点。
SCT认为, 海马的功能是对记忆的索引(Indexing; Teyler & DiScenna, 1986)。根据这一观点, 记忆是皮层在经历事件时的激活模式, 包含了各脑区的激活信息。这些激活模式被一一记录在海马当中, 即海马存储的并不是记忆本身, 而是记忆的索引或指针。通过这些索引在皮层上复现先前的皮层激活模式就能重新体验先前的经历。因此, SCT默认海马只是临时存储记忆的地方, 当皮层上的激活模式逐渐增强后, 记忆就不再依赖海马。
2.2 多痕迹理论
SCT确定了记忆巩固的基本框架, 但随着研究的不断深入, 越来越多证据表明, 海马受损导致的回溯性记忆损伤并不是总与时间有关(Clark et al., 2005; Miller et al., 2020)。Winocur等人(2010)回顾以往内侧颞叶损伤病人的研究发现, 回溯性记忆受损出现与没出现时间梯度的案例在数量上相差无几。在严格控制损伤位置和面积的动物实验中, 也有研究发现记忆损伤程度并不受获得这些记忆的时间影响(Clark et al., 2005; Sutherland et al., 2001)。
为了解释回溯性记忆损伤的不同模式, Nadel和Moscovitch (1997)提出了多痕迹理论(Multiple Trace Theory, MTT)。MTT在记忆巩固中区分了情景记忆与语义记忆, 提出情景记忆每一次再激活都会在海马中生成新的痕迹。久远的记忆有更多的再激活机会, 形成更多痕迹, 因此更可能在海马损伤时保留记忆信息。而且, 足够多的记忆痕迹能够在皮层上形成脱离情境的语义知识。这些表征一旦形成, 记忆就可以完全不依赖海马。与SCT不同的是, MTT认为那些保留了细节的情景记忆始终依赖海马而与获得该记忆的时间无关, 这一预测随后得到了大量研究的证实(Audrain etal., 2022; Bonnici & Maguire, 2018)。
尽管MTT所预测的海马中多个相似记忆痕迹并未得到实验支持(Karlsson & Frank, 2008; Mankin et al., 2012), 但其对记忆巩固中情景记忆和语义记忆的区分以及记忆转变的观点对该领域产生了深远影响。当前主流的转变观点认为记忆巩固是一个连续的动态过程, 这个过程中记忆的心理和神经基础逐渐发生转变(Dudai et al., 2015; Winocur et al., 2007)。且各种理论越来越强调心理−神经表征一致性(Neural-Psychological Representation Correspondence), 即巩固过程中神经基础的变化会伴随记忆性质的转变(Gilboa & Moscovitch, 2021; Sekeres et al., 2018)。由MTT演变而来的痕迹转变理论(Trace Transformation Theory, TTT; Winocur & Moscovitch, 2011)更是将这一过程细化, 提出记忆痕迹的形成和转变会经历知觉表征、细节、概要以及图式等4个连续过程, 其神经基础分别对应皮层后部、海马后部、海马前部、腹内侧前额叶(Robin & Moscovitch, 2017; Sekeres et al., 2018)。
2.3 互补学习系统理论
互补学习系统理论(Complementary Learning Systems, CLS)基于SCT和MTT的基本观念, 根据机器学习的原理描述了一套关于人脑记忆巩固的计算理论(Kumaran et al., 2016; McClelland etal., 1995)。CLS认为大脑中有两套学习系统, 一个是基于海马的学习系统, 对情景记忆快速编码。另一个是基于皮层的渐进式语义学习系统。人经历事件时, 海马接受各个脑区的输入信息并将它们绑定(如时空信息与事件本身), 形成基于样例的记忆表征。这种表征保留了丰富的情境细节, 但存储效率不高, 会受到记忆容量限制(Treves & Rolls, 1994)。作为补充, 相似的信息形成结构化的知识, 以基于参数的表征存储在皮层。在此过程中, 皮层接受海马的输入, 并将先前获得的样例当作一个个数据点, 这样就能用一个特定函数来表征所有相似的样例, 而该函数的各个参数则由其中所有数据点决定(Kumaran et al., 2016)。于是无限的样例就能用有限的参数来进行表征, 极大地提高了存储效率。
在CLS中, 皮层系统的学习过程就是记忆从海马向皮层转移的过程, 即记忆巩固。CLS认为记忆巩固必须十分缓慢。其原因一是准确稳定的统计表征需要足够多的数据样本, 这类似于MTT提出的多个记忆痕迹(Nadel & Moscovitch, 1997; Sutherland et al., 2020), 需要在更长的时间中逐渐获得。二是统计表征的参数不是突然形成的, 而是根据每一个新的输入来进行调整并需要考虑之前的所有输入, 因此指示如何调整参数的信号较为微弱并充满噪音, 使统计表征的形成十分缓慢(Kumaran et al., 2016)。
3 记忆快速巩固
上文介绍的几种记忆巩固理论都对回溯性记忆损伤的各种现象进行了解释, 尽管存在差异, 但都认可巩固过程包含记忆神经基础从海马到皮层的转移, 且这是一个缓慢的过程。然而, 新的研究表明, 在某些情况下记忆巩固所需时间远小于研究者之前的预期。
3.1 先前学习经验
人们早已知道先前经验会影响新信息的学习, 比如专长效应(Expertise Effect)的研究发现, 象棋大师对棋盘上棋子位置的记忆要明显优于新手(杜建政, 杨治良, 2002; Bilalić et al., 2009)。进一步的研究发现, 先前经验不仅会影响记忆的编码方式(Liu et al., 2017; Meßmer et al., 2021), 也会影响记忆的巩固。动物(Tse et al., 2007, 2011)和脑成像(Sommer, 2017; Sommer et al., 2022)研究都表明, 先前学习经验能够加快记忆从海马向皮层的转移。
Tse等人(2007)在一个边长1.6米的方形实验场景中训练大鼠学习气味与位置的联结配对。前6个气味−位置的配对学习需要在数周时间内多次重复训练才能得以保留, 但这之后, 2个新的配对却仅需一次训练就可以让大鼠在24小时之后的测试中表现出明显的偏好。为了更直接地考察记忆巩固, 在学习新配对48小时之后, 研究者切除了大鼠的海马, 结果在随后的记忆测试中大鼠不仅保留了之前反复训练的6对气味−位置联结记忆, 同样也保留了2对新学习的联结记忆。这表明新的联结记忆已经从海马转移到皮层, 且这一过程发生在短短48小时之内, 远小于之前所认为的巩固所需时间尺度, 说明先前的学习经验加速了新记忆的巩固。
研究者普遍认为先前学习经验对记忆巩固的影响源于图式的作用。在这类研究中, 图式被操作定义为多次训练中形成的一种记忆结构, 反映了多次情景记忆中的共同模式(Ghosh & Gilboa, 2014)。有研究者对Tse等人(2007)研究大鼠的范式进行修改, 使其适用于人类被试(Sommer, 2017)。在该项长达302天的研究中, 研究者在一个页面上随机选择20个位置用于放置不同形状的图案, 然后让被试记忆其中12个位置−图案配对, 并通过反复学习来形成图式。而在控制条件下, 图形与位置的配对关系在不同的训练试次中随机变化, 因而难以形成稳定图式。结果发现, 经过3个月反复的编码与提取, 实验组被试对固定形状−位置配对的记忆逐渐去情景化(Decontextualization), 被试更多反应为“知道”某一形状对应某一位置, 而不是“记得”特定的编码细节。这一变化与强调记忆转变的巩固理论(Dudai et al., 2015; Sekeres etal., 2018)相一致。同时, fMRI研究结果也表明, 提取过程中激活的脑区随着时间推移逐渐从海马转移到皮层。这些结果说明实验有效模拟了图式的形成。之后, 研究者让被试学习4对新的形状−位置配对以考察图式对新学习的影响。结果发现, 相对于控制条件, 图式条件下不仅学习效率更高, 且间隔一段时间之后再提取时, 海马激活出现了更明显的减弱, 而皮层激活明显增强(Sommer, 2017)。整个研究表明, 情景记忆在多次重复激活中逐渐巩固到皮层形成图式, 而图式则能加速新记忆的巩固。使用相似的范式, 其他研究训练被试在实验中习得不同的人工图式, 也得到了类似的结果(Liu et al., 2017; Sommer et al., 2022)。
计算机模拟的学习模型也表明与先前训练的图式相一致能够加快新信息的吸收(Kumaran etal., 2016; McClelland, 2013)。研究者首先用不同的例子训练模型形成关于动物的图式, 如喜鹊是一种鸟, 会飞翔; 鲤鱼是一种鱼, 会游泳。随后考察模型对新信息的学习能力, 一种条件下新信息与已有图式一致(如, X是一种鸟, 会飞翔), 另一种条件下则不一致(如, X是一种鸟, 会游泳)。结果发现, 模型能够快速学习一致的信息, 且不会对已有知识产生干扰(McClelland, 2013)。这一结果也促使作者对其先前提出的CLS理论(McClelland et al., 1995)做出修正。指出当新的信息与先前图式相一致时, 皮层能够快速整合新的信息(Kumaran et al., 2016; McClelland, 2013)。
3.2 特殊编码方式
编码方式对学习效果的影响通常被认为与加工深度有关(Craik, 2002), 主要作用于编码阶段(Bernstein et al., 2002)。然而, 有研究发现一些特殊的编码方式能够促进记忆的快速巩固。其中有代表性的两种方式是快速映射(Fast Mapping)和一体化(Unitization)编码。
3.2.1 快速映射
与直接的外显编码不同, 快速映射需要被试通过推测来进行学习。如给被试呈现一张图片, 图中有两只昆虫, 一只是被试熟悉的蛐蛐, 另一只则是被试不认识的昆虫, 两只昆虫的一个共同特点是都有触须。相应地, 图片下方则是需要回答的问题:XX的触须是向上的吗?其中XX是作者设计的假词, 由于蛐蛐是熟悉的, 因而被试能够通过排除法习得另一种昆虫的名字XX。有研究者认为这种编码模拟了婴儿快速学习大量词汇的方式(Bloom & Markson, 1998; Halberda, 2006)。由于婴儿时期个体的情景记忆及海马系统发育尚未完善, 因此这种学习方式可能并不依赖海马, 而是一种快速的皮层学习(Sharon et al., 2011), 或者是一种不依赖海马的快速记忆巩固(Coutanche & Thompson-Schill, 2014; Merhav et al., 2015)。
Sharon等人(2011)让4名失忆症病人使用快速映射或外显编码的方式学习罕见物体的图片名称, 之后进行迫选再认。虽然失忆症病人外显编码的记忆成绩显著低于对照组, 但是快速映射编码条件下, 两组被试记忆成绩却无显著差异。由于这些病人海马严重受损, 作者认为快速映射是一种不依赖海马的快速皮层学习。实验中, 有2名颞叶前部受损的病人无法通过快速映射获得记忆改善, 作者进一步推测这种皮层学习需要颞叶前部的参与, 而该区域通常与语义记忆的提取有关(Alam et al., 2021; Lambon Ralph et al., 2012)。脑成像研究也表明, 提取外显编码获得的记忆主要依赖海马网络, 而提取快速映射获得的记忆时则会激活颞叶前部(Merhav et al., 2015)。这说明, 与一般的外显情景编码不同, 通过快速映射获得的记忆在神经基础上更加类似已经巩固的语义知识。行为研究也表明, 通过快速映射获得的记忆具有语义网络的特点。相对于外显学习, 通过快速映射习得的联结记忆会受到更严重的语义干扰(Merhav et al., 2014), 而习得的新词也对其他语义相似词汇具有启动效应(Coutanche & Thompson- Schill, 2014)。另外, Coutanche和Thompson-Schill (2014)发现在快速映射学习中取消原来呈现的熟悉同类, 只给被试呈现不熟悉的动物, 这并不影响被试对编码问题的回答和对词图关联的推测, 但快速映射的学习优势消失了, 说明快速映射可能依赖熟悉的同类来激活类属概念等结构化的知识。
值得注意的是, 目前学界对快速映射能否促进皮层学习仍存有争议(Cooper et al., 2019; O’Connor & Riggs, 2019)。一些后续研究在失忆症病人(Elward et al., 2019; Smith et al., 2014; Warren et al., 2014)和海马功能衰退的老人被试中(Greve et al., 2014)并未发现快速映射的编码优势。
3.2.2 一体化
另一种特殊的编码方式是一体化。一体化是指将多个项目整合为单一整体(Graf & Schacter, 1989)。根据整合方式的不同可以分为自下而上和自上而下两种一体化(Tibon et al., 2014)。自下而上的一体化指利用材料本身的关联形成整体表征(Delhaye et al., 2018; Greve et al., 2007)。典型的操作方式是利用复合词(如, 交通−堵塞)和语义关联词对(如, 动物−老鼠)。在这种情况下, 一体化利用的是已有知识结构, 更多反映了记忆巩固的结果。相反, 自上而下的一体化则是利用特殊的编码指导语, 指导被试将多个项目编码为单一整体(Lu et al., 2020; Quamme et al., 2007)。一种典型的方式是概念定义法, 即通过给出定义(如, “一个观看天空的园子”)来指导被试将两个无关词汇(如, “云彩−草地”)组成新的复合词。一体化最主要的影响是改变了情景记忆的再认过程(Tibon et al., 2018)。而新的研究表明, 以这种方式进行编码可能促进了记忆的快速巩固。
情景记忆再认的双过程模型(Dual-Process Model; Yonelinas, 2002)提出再认依赖两个独立的过程, 即熟悉(Familiarity)和回想(Recollection)。其中, 熟悉是一种知道的感觉, 反映整体记忆痕迹的强度而不包含具体内容和细节, 回想则是对记忆内容和细节的有意提取(Rugg & Curran, 2007; Yonelinas, 2002)。熟悉与嗅周皮层的激活有关(Diana et al., 2007), 而回想主要依赖海马(Weis etal., 2004)。一体化增加了再认过程中熟悉的贡献(Greve et al., 2007; Parks, 2013), 减小了再认对海马的依赖(Quamme et al., 2007)。因此, 与快速映射类似, 一体化编码也能有效改善失忆症病人(D’Angelo et al., 2015; Ryan et al., 2013)和老人(Ahmad et al., 2015; Zheng et al., 2016) 的记忆成绩。有研究者认为回想和熟悉在功能和结构上分别对应了情景记忆和语义记忆(Souza et al., 2022; Wang et al., 2018), 那么一体化对再认过程的影响就是促进了情景记忆到语义记忆的转变。另外, 脑成像研究表明, 一体化编码增强了图式相关的内侧前额叶的激活(Bader et al., 2014)。因此, 有研究者提出一体化可能将原来的情景联结转变成了语义联结(Tibon et al., 2018), 与巩固过程中记忆性质所发生的变化一致(Renoult et al., 2019; Sekeres etal., 2018)。
一体化与已有知识密切相关。自下而上的一体化直接利用了已有知识提供的关联, 而自上而下的一体化也需要与已有知识一致才能形成合理的组合概念, 否则并不能形成一体化表征, 进而影响再认过程(Meßmer et al., 2021, 2023)。
3.3 睡眠过程
人们早就意识到睡眠对记忆具有积极作用(Jenkins & Dallenbach, 1924)。在学习和测试之间有睡眠的情况下记忆成绩明显更好(Barrett & Ekstrand, 1972; Wagner et al., 2001)。先前有研究者认为这是由于睡眠被动地减少了后续信息的干扰(Wixted, 2004; Yonelinas et al., 2019)。然而, 一系列研究表明, 在新的学习之后, 仅仅一段睡眠就能使记忆产生与巩固相关的变化(Dumay & Gaskell, 2007; Ellenbogen et al., 2007), 包括神经基础(Cowan et al., 2020; Gais et al., 2007)和记忆性质(Lewis & Durrant, 2011; Tamminen et al., 2015)的改变。这也让研究者认为, 睡眠过程中大脑会主动进行记忆巩固(Klinzing et al., 2019; Pöhlchen & Schönauer, 2020)。
睡眠相关的脑成像研究发现, 睡眠能促进神经表征从海马向皮层转移。多个研究表明, 在学习并经过睡眠后, 提取睡前学习的信息时海马激活程度降低, 而内侧前额叶的激活增强(Gais etal., 2007; van den Berg et al., 2022)。在最近的一项fMRI研究中, 研究者让被试反复学习和提取一个词表, 之后让被试睡眠或保持清醒并在12小时之后进行测试。结果两种条件下皮层表征均得到了加强, 但只有睡眠组在提取时海马的激活显著降低(Himmer et al., 2019)。另外, 编码后睡眠会增加海马与皮层特别是内侧前额叶之间的功能连接(Cowan et al., 2020), 这被认为是巩固过程中信息传递的重要过程(Helfrich et al., 2019; Klinzing etal., 2019)。
使用人类被试的行为研究也发现睡眠会促进记忆性质的变化。在婴儿时期, 睡眠会促进类属概念的生成(Friedrich et al., 2015)。在该研究中, 研究者训练1岁左右的婴儿学习人造类属词汇, 每个词汇匹配一组相似的图形。之后的测试中, 给婴儿呈现这些词汇与新图形的配对, 并考察他们对正确和错误配对的反应。结果只有学习之后经过睡眠的婴儿对错误配对表现出了反映语义冲突的N400效应(Kutas & Federmeier, 2011), 表明他们学会了这一类属概念对应的图形特征。与此类似, 在成年人中, 睡眠也会促进对类属概念(Schapiro et al., 2017)和隐藏规则的学习(Lerner & Gluck, 2019, 2022)。此外, 睡眠也会促进人脑将具体的关系记忆整合为更高级的关系结构。如Ellenbogen等人(2007)先训练被试记忆一组配对关系(A>B, B>C, C>D, D>E, E>F), 12小时之后, 相对无睡眠组, 睡眠组被试能更多利用关系结构(A>B>C>D>E>F)在任意配对中做出正确选择。最后, 睡眠也会促进情绪记忆的泛化(Pace-Schott etal., 2015)。反过来, 也有研究表明睡眠剥夺能阻止恐惧记忆泛化(Kuriyama et al., 2010)。总之, 这些研究一致表明, 睡眠能够促进结构化和抽象化表征的形成。这些表征让人能够根据经验做出预测并促进问题解决(Paller et al., 2021; Sanders etal., 2019), 而这被认为是记忆巩固的意义和目的(Sun et al., 2023)。另外, 睡眠之后抽象表征的形成也伴随着事件时间差异(Lerner & Gluck, 2022)和细节(Witkowski et al., 2021)的损失。这些变化与记忆巩固中记忆性质的转变相一致(Dudai et al., 2015; Sekeres et al., 2018)。
3.4 提取
有充分的证据表明, 相对于简单的重复学习, 对学习过的内容进行测试具有更好的学习效果, 这一现象也被称为测试效应(Carrier & Pashler, 1992; Roediger & Abel, 2022)。对测试效应的一种直观解释是从迁移恰当加工(Transfer-Appropriate Processing; Morris et al., 1977)的角度出发, 将提取和重复学习都看作是编码, 因为最后的测试与提取具有更相似的加工过程, 所以这种学习方式在测试中具有优势。也有研究者认为测试效应源于提取过程难度更高, 需要投入更多的认知资源(Bjork, 1994; Pyc & Rawson, 2009)。然而, 这些观点都各有不足, 难以全面准确地解释测试对学习效果的影响(综述见McDermott, 2021)。受记忆快速巩固相关研究的启发, 一种新的解释提出, 测试效应的出现是由于提取促进了记忆快速巩固(Antony et al., 2017; Lifanov et al., 2021)。
首先, 提取会促进记忆表征神经基础的转移。动物研究表明, 提取会减少记忆对海马的依赖(Lehmann et al., 2009)。在人类被试中也发现, 随着提取次数增加, 海马激活逐渐减少, 同时腹内侧前额叶和顶叶区域的激活逐渐增强(Ferreira et al., 2019; Himmer et al., 2019)。其次, 伴随着神经基础的变化, 经过反复提取, 记忆性质也发生了改变。Ferreira等(2019)使用基于fMRI的表征相似性分析发现, 属于同一类属概念(如, 动物)的不同项目在经过重复提取后, 相互之间的表征相似性增加了, 说明这些项目记忆表征中类属特征增加而特异性特征减少了, 即这一记忆变得更加抽象了。使用行为范式, 其他研究也得到了提取促进记忆表征语义化的结论(Lifanov et al., 2021; Siler & Benjamin, 2020)。这一结论也更好地解释了先前研究中测试效应的泛化和迁移(Butler, 2010; Karpicke & Blunt, 2011; Pan & Rickard, 2018), 如Butler (2010)在一系列实验中对每一个学习内容设置了两种不同的提问方式, 其中一个用于重学或提取练习, 而另一个用于之后的测试。结果表明, 相对于重学, 提取更能促进对第二种提问的回答。这说明测试效应并不依赖学习与测试过程的严格匹配, 相反, 更可能是提取过程促进了知识的整合。最后, 相较于重学, 提取对记忆的促进更多出现在延迟测试条件下, 如当提取与最后测试之间间隔数天甚至数周时(Antony & Paller, 2018; Toppino & Cohen, 2009)。而在即刻测试中, 有时重学对记忆的促进作用反而更大(Kornell et al., 2011; Roediger & Karpicke, 2006)。一项元分析研究也表明, 测试效应随着测试间隔时间增长而增加(Rowland, 2014)。这就说明, 提取所带来的记忆优势并不在编码阶段, 而是在记忆巩固阶段, 并不能简单用难度和认知资源的投入(Bjork, 1994; Pyc & Rawson, 2009)来解释。
4 记忆快速巩固的途径
上文描述了四种记忆快速巩固的情形, 反映了不同认知过程或经验对记忆巩固速度的促进。这些促进记忆快速巩固的方式之间也存在关联:先前学习经验对记忆巩固的促进依赖图式, 两种特殊编码方式则需要已有知识的参与, 而图式的一个典型定义就是能促进新信息加工的结构化知识(Ghosh & Gilboa, 2014); 睡眠中记忆会自发地再激活(Diekelmann & Born, 2010), 而提取则是主动复现先前记忆(McDermott, 2021), 两者都与记忆的再激活有关。因此, 记忆快速巩固可能具有两种不同的途径。
4.1 基于图式的学习
作为一个在心理学中被广泛使用的术语, 图式缺少明确统一的定义, 研究者更多是从功能上来对其进行描述, 且其含义在不同时期、不同研究领域也存在差异。Head和Holmes (1911)最初提出的图式是一种能够帮助理解新信息的认知结构。之后Bartlett (1932)将图式引入记忆领域, 认为提取不只是复现先前经验, 也会根据图式来重新建构。当Piaget (1952)在发展心理学研究中使用这一术语时, 其提出的同化(Assimilation)和顺应(Accommodation)则更强调图式的动态性和适应性。近年来, 在考察已有知识对新学习的影响时, 特别是在认知神经科学领域的相关研究中, 研究者们通常将图式宽泛地解释为皮层上一组相互紧密连接而常常共同激活的神经网络(Gilboa & Marlatte, 2017; van Kesteren et al., 2012)。这种宽泛的定义将不同类型的先验知识都归为图式, 表明这些知识可能以一种相似的方式影响新学习。根据这一定义, 前文中描述的先前学习经验和特殊编码方式则都可以看作是基于图式的学习。
大量研究证实内侧前额叶在图式相关的记忆巩固中具有重要作用(van Kesteren et al., 2012; Zheng et al., 2021)。例如, 与图式相关联的刺激在编码阶段(Liu et al., 2017; Sommer et al., 2022)以及之后的休息过程中(Liu et al., 2018), 都会在海马与内侧前额叶之间诱发更强的功能连接。而在提取过程中, 相对于与图式不一致的刺激, 与图式一致的刺激会使内侧前额叶激活增强而海马激活减弱(Bonasia et al., 2018; van Kesteren et al., 2010)。
图式如何通过内侧前额叶来加速记忆巩固呢?有研究者认为图式提供了一种组织支架来整合吸收新的信息(Audrain & McAndrews, 2022; Gilboa & Marlatte, 2017)。当新信息与已有图式相一致时, 两者在内侧前额叶区域激活的神经表征会出现部分重叠(Schlichting et al., 2015; Tompary & Davachi, 2017), 使得新信息在赫布(Hebbian; Hebscher et al., 2019)学习中具有优势, 加速信息的整合吸收。在一项fMRI研究中, Audrain和McAndrews (2022)发现相对于物体与背景不一致的刺激, 物体与背景相一致的刺激在3天之后变得更“粗糙”, 即损失了更多细节信息。而多体素模式分析(Multi-Voxel Pattern Analysis)结果也表明, 一致的刺激在内侧前额叶激活模式上的相似性随着时间出现了更显著的增加。进一步分析发现, 一致刺激的表征相似性在同类背景之间大于不同类背景, 由于一类背景代表一种图式, 就说明对这些刺激的学习可能是按照图式提供的支架来进行整合吸收的。
根据图式提供的组织结构来整合新的信息还能减少信息之间的干扰。在一项研究中, Wing等人(2022)考察本地鸟类爱好者与控制组被试对本地和外地鸟类图片的记忆, 并分析这些图片项目之间多个维度的相似性对再认的影响。结果鸟类爱好者不仅对熟悉的鸟类图片再认成绩更好, 对不熟悉的鸟类同样也表现出更好的再认成绩(Wing et al., 2022)。项目相似性的分析则表明, 鸟类爱好者的再认主要受分类学特征相似性的影响, 而控制组的再认则主要受外表颜色相似性的影响。这说明图式的存在使人能够将刺激按照更多维度进行组织, 减少了每个子分类中相互干扰竞争的项目数量。新获得的情景记忆能够依靠海马的模式分离(Pattern Separation; Rolls & Kesner, 2006)来区分相似输入。但记忆在快速巩固过程中迅速减少了对海马的依赖, 此时图式可能起到了一定的替代作用。
CLS认为记忆巩固缓慢的一个重要原因是需要防止快速吸收不一致信息而对已有知识结构造成严重破坏(Kumaran et al., 2016; McClelland etal., 1995)。而图式的存在让大脑能够提前对新信息进行检测, 然后根据其与已有图式的匹配程度采取不同的加工方式。van Kesteren等人(2012)提出的SLIMM (Schema-Linked Interactions between Medial Prefrontal and Medial Temporal Regions) 模型指出, 腹内侧前额叶能够同时接收来自皮层和内侧颞叶的信息, 因此能够检测新的输入与已有图式之间的一致程度。当信息与已有图式不一致时, 腹内侧前额叶会激活包括海马在内的内侧颞叶编码系统, 对事件的细节进行编码; 当信息与已有图式一致时, 则会抑制内侧颞叶的激活并进行直接的皮层学习(van Kesteren et al., 2010)。通过对新信息的分类加工, 大脑既能高效吸收新的信息, 又不会破坏已有知识结构。
特殊编码方式对记忆巩固的促进可能也与图式对干扰的抑制有关。前文中提到的两种编码方式促进记忆快速巩固的证据主要来自对失忆症病人学习的改善(Coutanche & Thompson-Schill, 2014; D’Angelo et al., 2015; Quamme et al., 2007)。而有研究者指出这类病人的学习障碍是由于海马的缺失使他们无法处理信息之间的干扰, 从而阻碍了记忆的巩固(Cowan et al., 2004; Dewar et al., 2009)。研究也表明, 抑制干扰是一种缓解病人学习障碍的有效途径(Duff et al., 2020)。例如, 让被试在学习之后独自待在安静黑暗的房间当中能够显著缩小病人与健康被试记忆成绩之间的差异(Cowan et al., 2005; Dewar et al., 2009)。快速映射和一体化编码并没有直接减少干扰, 但都在一定程度上利用了图式或先前知识, 快速映射依赖同类刺激的呈现(Coutanche & Thompson-Schill, 2014), 而一体化编码则利用先前知识来最大GpKzLsYIWe3q1eEvzvyLJ2TRgFMJj6yS8fIFzXk9/Mw=程度上合理化新的概念(Meßmer et al., 2023)。因此这两种特殊编码方式可能都利用图式处理了信息之间的干扰, 进而促进了皮层学习。
4.2 重复再激活
MTT认为记忆每一次再激活都会形成新的痕迹, 足够多的记忆痕迹才能支持统计学习(Statistical Learning), 从而在皮层上形成稳定的抽象表征(Nadel & Moscovitch, 1997)。类似地, CLS认为皮层上参数表征的形成需要海马提供足够多的记忆样本(Kumaran et al., 2016; McClelland et al., 1995)。对先前研究者来说, 这解释了为何记忆巩固需要大量时间, 但从记忆快速巩固的视角来看, 这也意味着重复再激活能加速记忆巩固。例如, 痕迹竞争理论(Competitive Trace Theory; Reagh & Yassa, 2014)认为, 再激活是影响记忆巩固进程的重要因素, 每一次再激活都会形成相似的记忆痕迹, 这些痕迹的相互竞争使得重叠的部分增强而不同的部分削弱, 从而驱动记忆的神经基础和性质发生转变。
睡眠促进记忆快速巩固的机制很可能是睡眠过程中记忆的重复再激活。首先, 白天的经历在睡眠过程中会自发地再激活。大鼠海马中存在对特定空间位置放电的位置细胞(Place Cells; Alme et al., 2014), 而研究发现睡眠过程中这些位置细胞会按照白天激活的顺序反复放电(Skaggs & McNaughton, 1996; Wang et al., 2020), 说明白天的经历会在睡眠过程中多次回放。且这种记忆回放并不是按照原来的速度进行, 而是以20倍左右(Michelmann et al., 2019; O’Neill et al., 2010)甚至60倍(Wimmer et al., 2020)以上的速度“快进”, 使得记忆能够在短时间内多次激活。海马中记忆回放时会伴随着尖波涟漪(Sharp-Wave Ripples)的出现, 并通过这一信号向皮层区域传递信息(Nitzan et al., 2022; Skelin et al., 2021), 使海马中的记忆回放能够传递到皮层, 增强相关皮层神经元之间的联结强度, 进而促进记忆巩固(Xue, 2022)。
其次, 睡眠过程中记忆的再激活与记忆巩固效果直接相关。研究表明, 在睡眠过程中通过呈现与先前特定记忆相关联的声音或气味来激活这一记忆, 即目标记忆再激活技术(Targeted Memory Reactivation; Rasch et al., 2007), 能够有效促进记忆巩固(Ngo & Staresina, 2022; Rakowska et al., 2021)。近期一项元分析也证实了这一结论(Hu etal., 2020)。在动物研究中, 研究者使用侵入式手段干扰或阻碍海马记忆回放相关的放电会损害大鼠的记忆巩固, 显著降低它们在记忆任务中的表现(Girardeau et al., 2009; Nakashiba et al., 2009)。相反, 在海马回放阶段检测到尖波涟漪时使用相似频率的刺激延长这种放电模式则能显著提升大鼠在记忆任务中的表现(Fernández-Ruiz et al., 2019)。基于相似的思路, de Sousa等人(2019)让大鼠进行条件恐惧学习并使用光遗传学方法标记皮层上与之相关的神经元, 之后在大鼠睡眠或清醒状态下使用高频刺激激活这些神经元。结果只有在睡眠状态下的刺激使新习得的恐惧记忆出现了巩固相关的变化, 即海马激活减少、皮层激活增加, 并在恐惧行为上出现情景泛化。
与睡眠过程中记忆回放阶段类似, 研究者在记忆提取过程中也发现了尖波涟漪(Vaz et al., 2019)。使用颅内脑电技术, 该研究发现在正确回忆的试次中, 内侧颞叶区域出现了更强的短暂高频震荡信号, 其频率与此前在睡眠过程中出现的信号高度一致(Axmacher et al., 2008; Staresina etal., 2015)。并且, 这种震荡信号的出现在时间上与刺激编码阶段皮层激活模式的复现相耦合(Vaz et al., 2019)。这一结果说明, 提取过程包含了与睡眠阶段类似的记忆再激活。由于尖波涟漪与记忆的再激活和巩固密切相关(Fernández-Ruiz et al., 2019; Girardeau et al., 2009), 有研究者提出睡眠和提取可能具有共同的记忆巩固机制(Staresina & Wimber, 2019)。睡眠过程中, 记忆能够多次再激活(Brodt et al., 2023), 提取过程中也存在类似的机制来促进记忆快速巩固。Antony等人(2017)提出, 由于记忆提取包括检索过程, 大量关联的信息也被激活(Carpenter, 2011; Pyc & Rawson, 2010)。如Carpenter (2011)让被试通过提取或重学方式学习一系列关联词对(如, “母亲−孩子”), 在之后的再认测试中混入未出现过的诱饵词(如, “父亲”), 结果相对于重学组, 提取组出现了更高的虚报率。这说明与目标相关联的信息在提取过程中也得到了一定的激活。反过来, 这些信息的激活也会扩散到目标记忆, 使其反复激活, 产生与睡眠中重复的记忆回放相似的效果, 驱动记忆从海马向皮层转移(Antony et al., 2017)。后续研究也证实, 测试效应依赖目标相关的语义网络(Ferreira et al., 2019; Ferreira & Wimber, 2023), 例如, 当记忆材料是无意义的抽象图形时, 提取并不能促进记忆的保持(Ferreira & Wimber, 2023)。
4.3 两种途径之间的关系
在个体与环境的交互中, 大脑并不是被动地接受和记录信息。图式和重复再激活对记忆巩固速度的影响就为巩固提供了自上而下的调节机制, 使其不只是从海马到皮层的单一方向加工(Gilboa & Moscovitch, 2021)。图式调节机制让个体更容易学习与已有图式相一致或关联的信息, 使得记忆巩固受到个体已有知识结构的影响。类似地, 睡眠中大脑自发激活的记忆也并非随机, 而是更偏向于情绪性(Denis et al., 2022; Jones et al., 2019)以及奖赏性(Asfestani et al., 2020; Sterpenich et al., 2021)的记忆, 这使得记忆巩固速度受到个体目标和动机的调节因而更具有适应价值。
虽然两条途径都能促进记忆的快速巩固, 但也存在显著差异:图式途径依赖已有知识结构, 记忆巩固的结果是对已有知识结构的调整, 使其能够整合吸纳新的输入; 而重复再激活则无需这一前置条件, 记忆巩固的结果是形成一个专门容纳新输入的抽象表征。
在实际学习场景中, 两种快速巩固途径并不互斥, 也能并列进行、协同作用。首先, 在基于图式的快速巩固当中, 可能也需要睡眠的配合。在Tse等人(2007)开创性的研究当中, 经过反复训练获得图式之后, 新的记忆只需要一次练习就能稳定地存储在皮层而不再依赖海马。但该研究也发现, 要快速习得新的记忆, 学习后的睡眠可能是必不可少的。当研究者在学习之后3小时就切除大鼠海马时, 手术前只经过一次学习的记忆就完全丢失了。由于海马−皮层神经元同步活动通常出现在编码后的睡眠阶段(Navarrete et al., 2020; Pedrosa et al., 2022), 因此作者认为记忆快速从海马转移到皮层可能也依赖睡眠过程(Tse et al., 2007)。后续研究也证实, 睡眠过程中的脑活动能够预测图式相关记忆的保持, 以及这些记忆对海马的依赖程度(Hennies et al., 2016; Tamminen etal., 2010)。其次, 提取对记忆快速巩固的促进也与图式有关。虽然提取过程中包含了记忆的再激活(Staresina & Wimber, 2019; Vaz et al., 2019), 但一次再激活并不足以使记忆快速巩固, 基于图式网络的激活扩散使得目标记忆被重复激活, 是提取能够促进记忆快速巩固的重要条件(Antony etal., 2017; Ferreira & Wimber, 2023)。
另外, 记忆巩固的前提是先得到编码, 更好的编码通常伴随着更快更好的巩固(Herbert & Burt, 2004; Fitzroy et al., 2021)。因此, 影响记忆编码的因素, 如注意、加工深度等可以通过影响编码阶段来间接影响记忆巩固速度。而本文介绍的几种情形则是直接影响记忆巩固, 图式和睡眠都会影响编码后巩固相关的脑活动(Cowan et al., 2020; Sommer, 2017), 两种特殊编码方式以及提取虽然主要涉及在线加工, 但其神经过程被认为与离线巩固相一致 (Antony et al., 2017; Merhav et al., 2015)。
5 未来展望
传统上记忆巩固被认为是一个十分缓慢的过程, 不同的记忆巩固理论均对此做出了解释。然而新的研究发现, 在某些情况下记忆能够迅速巩固。对相关证据进行梳理并分析其内部关联之后, 本文总结了记忆快速巩固的两种, 即基于图式的学习和重复再激活。这是对原有记忆巩固框架的一次完善, 而要进一步构建一个涵盖不同速度记忆巩固的统一理论, 未来研究可以从以下方面继续探索。
5.1 海马在皮层学习中的作用
记忆巩固之后就不再依赖海马, 但经典的记忆巩固理论都认为海马在记忆巩固过程中具有重要作用(McClelland et al., 1995; Nadel & Moscovitch, 1997)。在记忆快速巩固的情况下, 特别是基于图式的学习中, 研究者更强调直接的皮层学习(Sharon et al., 2011; van Kesteren et al., 2012)。这个过程中腹内侧前额叶受到了更多的重视(Giuliano et al., 2021;van Kesteren et al., 2010, 2012), 而海马在其中的作用却并不明确。在一项研究中, 研究者使用正常顺序和顺序被打乱的电影片段来操作图式, 结果发现以正常顺序观看前半部分电影的被试在编码后续情节时腹内侧前额叶与皮层区域的功能连接更强, 而与海马功能连接更弱(van Kesteren et al., 2010), 且这种差异在编码后的静息状态持续存在。这似乎说明图式减少了学习对海马的依赖, 甚至SLIMM模型认为, 当新的学习与已有图式相一致时, 能够越过海马进行直接的皮层学习(van Kesteren et al., 2012)。
SLIMM模型获得了一些研究的支持, 如有研究证实与图式一致和冲突都会促进记忆, 且基于不同的机制, 分别对应皮层语义学习与海马情景学习(Greve et al., 2019)。但基于图式的学习是否依赖海马, 后续研究则得出了不同结果。为了避免van Kesteren等(2010)所使用的自然图式可能存在的个体差异, 后续研究者在实验中训练被试形成新的人工图式, 然后再考察这些图式对后续学习的影响。结果发现图式会促进腹内侧前额叶与海马的协同激活(Liu et al., 2017; Sommer, 2017; Sommer et al., 2022)。因此另一种观点认为, 皮层学习也需要海马的参与, 腹内侧前额叶的作用则是处理信息冲突, 通过提取皮层相关信息来整合新的海马输入(Eichenbaum, 2017; Preston & Eichenbaum, 2013)。除此之外, 一种折中的观点认为海马不同部位在基于图式的学习中具有不同作用(Guo et al., 2023; Guo & Yang, 2020)。在两项最近的研究中, 提取阶段(Guo et al., 2023)的激活以及编码后的脑功能连接(Guo & Yang, 2020)都显示出海马前部与后部的功能差异, 海马前部更多参与图式一致信息的学习, 而海马后部则与图式不一致信息的学习关系更加密切。
关于海马的争议也体现在对失忆症病人的研究当中。一方面, 病人在某些情况下也能习得新的语义记忆, 说明大脑中存在不依赖海马的学习机制(Merhav et al., 2014)。但另一方面, 即使在有利的编码和测试条件下, 他们的学习效率也难以达到健康被试的水平(综述见Duff et al., 2020), 或者达到了这一水平(Sharon et al., 2011)却难以重复(Cooper et al., 2019)。巩固是记忆对海马依赖程度逐渐降低的过程, 而巩固速度也许就取决于记忆获得过程中海马的参与程度。
5.2 记忆快速巩固中的干扰抑制
在分析图式和特殊编码方式促进记忆快速巩固的过程中, 我们描述了图式对干扰的抑制, 即过滤信息以及提供组织架构来对信息进行分类。而在睡眠和提取过程中, 也同样包含对干扰的抑制。睡眠在促进记忆保持的同时, 还具有另一个重要功能, 即遗忘琐碎信息(Poe, 2017)。根据突触稳态假说(Synaptic Homeostasis Hypothesis; Tononi & Cirelli, 2014), 清醒状态时随着信息不断输入, 大脑整体突触联结强度逐渐增加, 而在睡眠过程中, 突触联结强度逐渐降低并恢复至基线水平, 以避免联结饱和, 同时节省资源。于是, 睡眠过程中的记忆回放是在整体突触联结强度降低的情况下对局部突触联结的增强(De Vivo et al., 2017; Li et al., 2017)。这有效提高了目标记忆表征的信噪比(González-Rueda et al., 2018; Tononi & Cirelli, 2014)。
类似的机制也存在于提取过程当中(Antony et al., 2017)。提取不仅能促进记忆保持, 同时也会诱发遗忘, 即提取目标记忆会抑制与其具有竞争关系的其他记忆痕迹(Anderson et al., 1994; Wimber et al., 2015)。由于记忆提取通常并不精准, 检索过程中会同时激活大量相关联的信息(Carpenter, 2011; Pyc & Rawson, 2010)。而在这样一个激活扩散模型(Norman et al., 2007)中, 不同激活强度的信息会导致截然相反的结果。高度激活的信息得到进一步强化而被整合进以线索为中心的激活网络; 而中等强度激活的信息则被削弱, 从而远离网络中心(Norman et al., 2007; Ritvo et al., 2019)。这就导致在提取过程中原本具有更高激活强度的目标记忆得到进一步增强, 而激活较弱的干扰信息被进一步削弱。
不同的记忆快速巩固情形中都包含了对干扰的处理, 说明抑制干扰可能是记忆快速巩固的必要条件。而这也许是提取与重复学习对记忆影响存在差异的另一重要原因。对于遗忘, 一直存在消退和干扰两种解释(Altmann & Gray, 2002)。各种巩固理论更多描述的是记忆如何对抗消退, 但也有新的观点认为记忆能够保留的关键是处理干扰(Yonelinas et al., 2019)。未来的巩固研究中, 应该更加重视干扰抑制与记忆巩固速度之间的关系。
5.3 记忆快速巩固的两面性
目前, 研究者普遍认同巩固过程中包含了记忆性质从情景记忆到语义记忆的连续变化(Dudai et al., 2015; Sekeres et al., 2018), 即细节特征逐渐丢失, 而图式则从共同特征中抽象出来。但在情景−语义连续维度上, 处于不同位置的记忆在人适应外界复杂多样的环境时都具有各自独特的作用。因此, 促进记忆快速巩固的学习方式一方面促进了记忆的存储, 另一方面也存在着一些“副作用”。
首先, 已有知识或图式能够促进记忆快速巩固的同时也容易导致错误记忆的形成(van Kesteren & Meeter, 2020)。如在Deese-Roediger- McDermott (DRM)范式中, 研究者让被试学习多个与未呈现的目标词(如“寒冷”)相关联的项目(如“冬天”、“冰雪”、“北极”等)。结果在之后的记忆测试中, 被试将目标词再认为旧词的概率接近那些实际呈现过的项目(Roediger & McDermott, 1995)。这种错误记忆的发生与图式密切相关, 腹内侧前额叶受损(Warren et al., 2014)或者使用经颅磁刺激干扰该部位(Berkers et al., 2017)都会显著减少错误记忆的发生。其次, 提取对记忆的影响具有两面性(Roediger & Abel, 2022)。除了前文提到的提取诱发遗忘(Anderson et al., 1994; Wimber et al., 2015), 提取已经巩固的记忆还会使该记忆变得不稳定而需要再次巩固, 即记忆再巩固(Reconsolidation; Kim et al., 2021; McKenzie & Eichenbaum, 2011)。此时若遭遇错误信息, 先前记忆就容易被更改, 例如提取使目击者记忆更容易受到错误信息的影响(Chan et al., 2009; Gordon etal., 2020)。
对记忆快速巩固两面性更清晰的认识, 让我们能够从适应环境的视角来看待记忆巩固的快与慢, 更好地理解记忆巩固的意义和目的(Sun et al., 2023)。而在实践中, 也有助于避免甚至利用某些副作用来实现更好的目的。例如记忆再巩固的特点已被研究者用来干扰已经巩固的痛苦记忆(Galarza Vallejo et al., 2019)和治疗成瘾行为(Milton & Everitt, 2010)。
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Rapid memory consolidation: Schema-based learning
and repeated reactivation
ZHOU Fan1, TIAN Haoyue2, JIANG Yingjie2,3
(1 School of Educational Science, Shenyang Normal University, Shenyang 110034, China)
(2 School of Psychology, Northeast Normal University, Changchun 130024, China)
(3 Jilin Provincial Higher Education Key Laboratory of Cognitive and Brain Science, Changchun 130024, China)
Abstract: Memory consolidation has traditionally been perceived as a slow process, extending over years, even decades. However, new research indicates that memory can consolidate rapidly when new information is consistent with existing schemas or employs specific encoding methods. Moreover, the influence of sleep and retrieval on memory is believed to be linked to rapid consolidation. This paper reviews studies on rapid memory consolidation and summarizes two potential mechanisms driving this swift process: schema-based learning and repeated reactivation. Future investigations could delve into the role of hippocampus in cortical learning, the significance of interference suppression in memory consolidation, and, by adopting an adaptive perspective on the interplay between fast and slow memory consolidation processes, unravel the nature of rapid memory consolidation as a double-edged sword.
Keywords: memory consolidation, hippocampus, schema, reactivation