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揭示人类海马体在程序性运动学习中的作用:来自内隐感觉运动适应的见解。

Uncovering the role of the human hippocampus in procedural motor learning: Insights from implicit sensorimotor adaptation.

作者信息

Griffa Guillermina, Solano Agustin, Deleglise Alvaro, De Pino Gabriela, Jacobacci Florencia, Della-Maggiore Valeria

机构信息

Universidad de Buenos Aires-CONICET. Instituto de Fisiología y Biofísica Bernardo Houssay (IFIBIO Houssay), Facultad de Medicina, Departamento de Ciencias Fisiológicas, Ciudad de Buenos Aires C1121ABG, Argentina.

Instituto de Ciencias Fisicas (ICIFI), Escuela de Ciencia y Tecnología (ECyT), Universidad Nacional de San Martin (UNSAM), San Martin, Buenos Aires, CP 1650, Argentina.

出版信息

J Neurosci. 2025 Jul 31. doi: 10.1523/JNEUROSCI.2119-24.2025.

Abstract

Recent evidence suggests that the human hippocampus, traditionally associated with declarative memory, plays a role in motor sequence learning (MSL). However, the classic MSL paradigm depends initially on declarative learning. Thus, it is critical to discern whether the participation of the hippocampus relates to its canonical role or to processing a general aspect of learning that transcends the declarative/non-declarative distinction. To address this issue, here we turned to visuomotor adaptation -a type of motor learning involving skill recalibration- which unlike MSL can be easily manipulated to eliminate the explicit component. We examined the broader involvement of the hippocampus in procedural motor learning by using diffusion MRI in a sample of males and females to assess structural plasticity associated with memory consolidation in visuomotor adaptation (VMA) and an implicit-only version (IVMA). We found that both VMA and IVMA engaged the left posterior hippocampus in a learning-specific manner. Remarkably, while VMA induced only transient hippocampal alterations, IVMA elicited structural changes that persisted overnight, underscoring the reliance on implicit learning for enduring neuroplasticity. As expected, training on both tasks impacted the microstructure of the cerebellum, the motor and posterior parietal cortex. Notably, the temporal dynamics of changes in these regions paralleled those of the left hippocampus, suggesting that motor and limbic regions operate together as part of the same network. Collectively, our findings support an active role of the hippocampus in implicit motor learning and argue for a unified function in memory encoding regardless of the declarative or non-declarative nature of the task. Brenda Milner's work on patient H.M. introduced the concept of specialized memory systems in the brain but also inevitably initiated a dichotomy in cognitive neuroscience, with episodic learning viewed as hippocampus-dependent, and procedural learning as hippocampus-independent. This distinction fragmented the field of cognitive neuroscience, with studies on declarative and procedural memory progressing along parallel paths. Here, we show that a purely implicit motor task induces learning-specific structural plasticity in the human hippocampus. Notably, the temporal dynamics of these hippocampal changes were mirrored by key motor regions involved in acquisition, pointing to a close interaction between memory systems. Our findings provide evidence supporting the involvement of the human hippocampus in procedural motor memory and argue for common mechanisms supporting memory formation.

摘要

最近的证据表明,传统上与陈述性记忆相关的人类海马体在运动序列学习(MSL)中发挥作用。然而,经典的MSL范式最初依赖于陈述性学习。因此,至关重要的是要辨别海马体的参与是与其典型作用相关,还是与处理超越陈述性/非陈述性区分的学习的一般方面相关。为了解决这个问题,我们在此转向视觉运动适应——一种涉及技能重新校准的运动学习类型——与MSL不同,它可以很容易地被操纵以消除明确成分。我们通过在男性和女性样本中使用扩散磁共振成像来评估与视觉运动适应(VMA)和仅隐性版本(IVMA)中的记忆巩固相关的结构可塑性,研究了海马体在程序性运动学习中的更广泛参与。我们发现,VMA和IVMA均以学习特异性方式激活左后海马体。值得注意的是,虽然VMA仅引起海马体的短暂改变,但IVMA引发了持续一整夜的结构变化,突出了对持久神经可塑性的隐性学习的依赖。正如预期的那样,两项任务的训练都影响了小脑、运动和后顶叶皮层的微观结构。值得注意的是,这些区域变化的时间动态与左海马体的变化平行,表明运动和边缘区域作为同一网络的一部分共同运作。总体而言,我们的研究结果支持海马体在隐性运动学习中的积极作用,并主张无论任务的陈述性或非陈述性性质如何,在记忆编码中都具有统一功能。布伦达·米尔纳对患者H.M.的研究引入了大脑中专门记忆系统的概念,但也不可避免地在认知神经科学中引发了二分法,情景学习被视为依赖海马体,而程序性学习被视为不依赖海马体。这种区分使认知神经科学领域碎片化,对陈述性和程序性记忆的研究沿着平行路径进行。在这里,我们表明,一项纯粹的隐性运动任务会在人类海马体中诱导特定于学习的结构可塑性。值得注意的是,这些海马体变化的时间动态被参与习得的关键运动区域所反映,表明记忆系统之间存在密切相互作用。我们的研究结果提供了证据支持人类海马体参与程序性运动记忆,并主张存在支持记忆形成的共同机制。

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