Energy constraints determine the selection of reaching movement trajectories in macaque monkeys.

IF 2.7 3区 医学 Q3 NEUROSCIENCES
eNeuro Pub Date : 2025-09-22 DOI:10.1523/ENEURO.0385-24.2025
Shrabasti Jana, Lucio Condro, Frédéric V Barthélemy, Junji Ito, Alexa Riehle, Sonja Grün, Thomas Brochier
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引用次数: 0

Abstract

Reaching movements, while seemingly simple, involve complex motor control mechanisms that select specific trajectories from infinite possibilities. Despite the inherent variability in volitional movements, both humans and monkeys frequently exhibit stereotyped trajectories. The literature has offered numerous explanations for invariant trajectory shapes, including a common planning space in hand-space or joint-space, as well as factors like kinetic energy (KE) minimization and sensory feedback. However, since most studies have relied on single-session data, crucial insights into the motor principles guiding trajectory selection and their evolution through extended practice remain underexplored. This study fills this gap by investigating how specific trajectories are selected and evolve with practice across multiple sessions, using data from two rhesus monkeys (one male, one female) performing a reaching task in a biomechanically constrained 2D setup. Our behavioral study challenges the idea of a common planning space, revealing instead a significant influence of KE on trajectory shapes. Through a novel biomechanical modeling, we quantified KE for a wide range of trajectory shapes. We discovered that trajectory selection and evolution is not simply about minimizing KE or achieving straight paths. Instead, the monkeys' motor systems appear to prioritize maintaining a "safe KE range," where slight changes in trajectory shapes have minimal impact on energy expenditure. These findings provide new insights into the adaptive motor control strategies, suggesting that trajectory selection involves balancing energy efficiency and flexibility. Our study enhances the understanding of trajectory selection principles, with implications for rehabilitation strategies, robotics and broader study of motor control mechanisms.Significance statement This study provides new insights into motor control by analyzing and modeling monkey behavior, revealing that kinetic energy (KE) significantly influences trajectory shape. Our findings challenge the conventional views that trajectory selection primarily aims to maximize straightness or minimize KE. Instead, our analyses show that the motor system seeks to maintain a "safe KE range," where small trajectory differences do not significantly impact energy expenditure. We reach this conclusion through a novel biomechanical modeling approach, which quantifies KE across a wide range of trajectory shapes for specific movements. By combining behavioral analysis with modeling, we demonstrate that trajectory selection balances efficiency and flexibility, offering valuable implications for developing rehabilitation strategies and robotic assistive devices that align with natural movement principles.

能量约束决定了猕猴到达运动轨迹的选择。
到达运动,虽然看似简单,涉及复杂的运动控制机制,从无限的可能性中选择特定的轨迹。尽管意志运动具有内在的可变性,但人类和猴子都经常表现出刻板的轨迹。文献提供了许多不变轨迹形状的解释,包括手空间或关节空间中的共同规划空间,以及动能(KE)最小化和感觉反馈等因素。然而,由于大多数研究都依赖于单次会话数据,因此对指导轨迹选择的运动原理及其通过扩展实践的进化的关键见解仍未得到充分探索。本研究利用两只恒河猴(一雄一雌)在生物力学受限的2D设置中执行到达任务的数据,通过调查如何在多个会话中选择和发展特定的轨迹来填补这一空白。我们的行为研究挑战了公共规划空间的概念,揭示了KE对轨迹形状的重要影响。通过一种新的生物力学模型,我们量化了各种轨迹形状的KE。我们发现轨迹选择和进化不仅仅是最小化KE或实现直线路径。相反,猴子的运动系统似乎优先考虑维持一个“安全的KE范围”,在这个范围内,轨迹形状的微小变化对能量消耗的影响最小。这些发现为自适应运动控制策略提供了新的见解,表明轨迹选择涉及平衡能量效率和灵活性。我们的研究增强了对轨迹选择原则的理解,对康复策略、机器人技术和更广泛的运动控制机制研究具有重要意义。本研究通过对猴子行为的分析和建模,为运动控制提供了新的见解,揭示了动能(KE)对轨迹形状的显著影响。我们的研究结果挑战了传统的观点,即轨迹选择的主要目的是最大化直线度或最小化KE。相反,我们的分析表明,电机系统寻求维持一个“安全KE范围”,其中小的轨迹差异不会显著影响能量消耗。我们通过一种新的生物力学建模方法得出了这一结论,该方法量化了特定运动的大范围轨迹形状的KE。通过将行为分析与建模相结合,我们证明了轨迹选择平衡了效率和灵活性,为开发符合自然运动原则的康复策略和机器人辅助设备提供了有价值的启示。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
eNeuro
eNeuro Neuroscience-General Neuroscience
CiteScore
5.00
自引率
2.90%
发文量
486
审稿时长
16 weeks
期刊介绍: An open-access journal from the Society for Neuroscience, eNeuro publishes high-quality, broad-based, peer-reviewed research focused solely on the field of neuroscience. eNeuro embodies an emerging scientific vision that offers a new experience for authors and readers, all in support of the Society’s mission to advance understanding of the brain and nervous system.
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