Center for Neuroscience and Cognitive Systems, Istituto Italiano di Tecnologia, Corso Bettini 31, 38068 Rovereto, Italy; Neurology Service, San Francisco Veterans Affairs Medical Center, 4150 Clement Street, San Francisco, CA 94121, USA; Department of Neurology, University of California, San Francisco, 1700 Owens Street, San Francisco, CA 94158, USA; Neuroscience Center, University of North Carolina, Chapel Hill, 116 Manning Drive, Chapel Hill, NC 27599, USA.
Center for Neuroscience and Cognitive Systems, Istituto Italiano di Tecnologia, Corso Bettini 31, 38068 Rovereto, Italy; Department of Pharmacy and Biotechnology, University of Bologna, Via Irnerio 48, 40126 Bologna, Italy; Institute of Neural Information Processing, Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf (UKE), Falkenried 94, 20251 Hamburg, Germany.
Curr Biol. 2024 May 6;34(9):1831-1843.e7. doi: 10.1016/j.cub.2024.03.023. Epub 2024 Apr 10.
The coordination of neural activity across brain areas during a specific behavior is often interpreted as neural communication involved in controlling the behavior. However, whether information relevant to the behavior is actually transferred between areas is often untested. Here, we used information-theoretic tools to quantify how motor cortex and striatum encode and exchange behaviorally relevant information about specific reach-to-grasp movement features during skill learning in rats. We found a temporal shift in the encoding of behaviorally relevant information during skill learning, as well as a reversal in the primary direction of behaviorally relevant information flow, from cortex-to-striatum during naive movements to striatum-to-cortex during skilled movements. Standard analytical methods that quantify the evolution of overall neural activity during learning-such as changes in neural signal amplitude or the overall exchange of information between areas-failed to capture these behaviorally relevant information dynamics. Using these standard methods, we instead found a consistent coactivation of overall neural signals during movement production and a bidirectional increase in overall information propagation between areas during learning. Our results show that skill learning is achieved through a transformation in how behaviorally relevant information is routed across cortical and subcortical brain areas and that isolating the components of neural activity relevant to and informative about behavior is critical to uncover directional interactions within a coactive and coordinated network.
在特定行为过程中,大脑区域之间的神经活动协调通常被解释为控制行为所涉及的神经通讯。然而,行为相关的信息是否实际上在区域之间传递通常未经测试。在这里,我们使用信息论工具来量化大鼠在技能学习过程中,运动皮层和纹状体如何对特定抓握运动特征的行为相关信息进行编码和交换。我们发现,在技能学习过程中,行为相关信息的编码发生了时间上的转变,以及行为相关信息流的主要方向发生了反转,从运动前的皮层到纹状体,到熟练运动时的纹状体到皮层。用于量化学习过程中整体神经活动演变的标准分析方法——例如神经信号幅度的变化或区域之间整体信息交换——未能捕捉到这些行为相关信息的动态。使用这些标准方法,我们反而发现运动产生过程中整体神经信号的一致协同激活,以及学习过程中区域之间整体信息传播的双向增加。我们的研究结果表明,技能学习是通过行为相关信息在皮层和皮层下脑区之间的路由方式的转变来实现的,并且分离与行为相关且具有信息量的神经活动的组成部分对于揭示协调和协同网络内的定向相互作用至关重要。