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Spike-timing-dependent plasticity induction reveals dissociable supplementary– and premotor–motor pathways to automatic imitation
Proceedings of the National Academy of Sciences of the United States of America ( IF 9.4 ) Pub Date : 2024-06-25 , DOI: 10.1073/pnas.2404925121
Sonia Turrini 1 , Francesca Fiori 1, 2 , Naomi Bevacqua 1, 3 , Chiara Saracini 4 , Boris Lucero 4 , Matteo Candidi 3 , Alessio Avenanti 1, 4
Affiliation  

Humans tend to spontaneously imitate others’ behavior, even when detrimental to the task at hand. The action observation network (AON) is consistently recruited during imitative tasks. However, whether automatic imitation is mediated by cortico-cortical projections from AON regions to the primary motor cortex (M1) remains speculative. Similarly, the potentially dissociable role of AON-to-M1 pathways involving the ventral premotor cortex (PMv) or supplementary motor area (SMA) in automatic imitation is unclear. Here, we used cortico-cortical paired associative stimulation (ccPAS) to enhance or hinder effective connectivity in PMv-to-M1 and SMA-to-M1 pathways via Hebbian spike-timing-dependent plasticity (STDP) to test their functional relevance to automatic and voluntary motor imitation. ccPAS affected behavior under competition between task rules and prepotent visuomotor associations underpinning automatic imitation. Critically, we found dissociable effects of manipulating the strength of the two pathways. While strengthening PMv-to-M1 projections enhanced automatic imitation, weakening them hindered it. On the other hand, strengthening SMA-to-M1 projections reduced automatic imitation but also reduced interference from task-irrelevant cues during voluntary imitation. Our study demonstrates that driving Hebbian STDP in AON-to-M1 projections induces opposite effects on automatic imitation that depend on the targeted pathway. Our results provide direct causal evidence of the functional role of PMv-to-M1 projections for automatic imitation, seemingly involved in spontaneously mirroring observed actions and facilitating the tendency to imitate them. Moreover, our findings support the notion that SMA exerts an opposite gating function, controlling M1 to prevent overt motor behavior when inadequate to the context.

中文翻译:


尖峰时间依赖性可塑性诱导揭示了自动模仿的可分离补充和运动前运动途径



人类倾向于自发地模仿他人的行为,即使这不利于手头的任务。在模仿任务中持续招募动作观察网络(AON)。然而,自动模仿是否是由 AON 区域到初级运动皮层 (M1) 的皮质-皮质投射介导的仍然是推测。同样,涉及腹侧前运动皮层 (PMv) 或辅助运动区 (SMA) 的 AON-to-M1 通路在自动模仿中的潜在可分离作用尚不清楚。在这里,我们使用皮质-皮质配对关联刺激 (ccPAS) 通过 Hebbian 尖峰时序依赖性可塑性 (STDP) 来增强或阻碍 PMv-to-M1 和 SMA-to-M1 通路的有效连接,以测试它们与自动神经网络的功能相关性。和自愿运动模仿。 ccPAS 影响任务规则和支持自动模仿的优势视觉运动关联之间竞争下的行为。至关重要的是,我们发现操纵两条通路强度的分离效应。虽然加强 PMv-to-M1 预测可以增强自动模仿,但削弱它们则会阻碍自动模仿。另一方面,加强 SMA 到 M1 的预测减少了自动模仿,但也减少了自愿模仿过程中与任务无关的线索的干扰。我们的研究表明,在 AON-to-M1 投影中驱动 Hebbian STDP 会对依赖于目标途径的自动模仿产生相反的影响。我们的结果提供了 PMv-to-M1 预测在自动模仿中的功能作用的直接因果证据,似乎涉及自发镜像观察到的行为并促进模仿它们的倾向。 此外,我们的研究结果支持这样的观点,即 SMA 发挥相反的门控功能,控制 M1 以防止在不适合环境时出现明显的运动行为。
更新日期:2024-06-25
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