Spaak Eelke, Watanabe Kei, Funahashi Shintaro, Stokes Mark G
Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom,
Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom.
J Neurosci. 2017 Jul 5;37(27):6503-6516. doi: 10.1523/JNEUROSCI.3364-16.2017. Epub 2017 May 30.
Working memory (WM) provides the stability necessary for high-level cognition. Influential theories typically assume that WM depends on the persistence of stable neural representations, yet increasing evidence suggests that neural states are highly dynamic. Here we apply multivariate pattern analysis to explore the population dynamics in primate lateral prefrontal cortex (PFC) during three variants of the classic memory-guided saccade task (recorded in four animals). We observed the hallmark of dynamic population coding across key phases of a working memory task: sensory processing, memory encoding, and response execution. Throughout both these dynamic epochs and the memory delay period, however, the neural representational geometry remained stable. We identified two characteristics that jointly explain these dynamics: (1) time-varying changes in the subpopulation of neurons coding for task variables (i.e., dynamic subpopulations); and (2) time-varying selectivity within neurons (i.e., dynamic selectivity). These results indicate that even in a very simple memory-guided saccade task, PFC neurons display complex dynamics to support stable representations for WM. Flexible, intelligent behavior requires the maintenance and manipulation of incoming information over various time spans. For short time spans, this faculty is labeled "working memory" (WM). Dominant models propose that WM is maintained by stable, persistent patterns of neural activity in prefrontal cortex (PFC). However, recent evidence suggests that neural activity in PFC is dynamic, even while the contents of WM remain stably represented. Here, we explored the neural dynamics in PFC during a memory-guided saccade task. We found evidence for dynamic population coding in various task epochs, despite striking stability in the neural representational geometry of WM. Furthermore, we identified two distinct cellular mechanisms that contribute to dynamic population coding.
工作记忆(WM)为高级认知提供了必要的稳定性。有影响力的理论通常假定WM依赖于稳定神经表征的持续性,但越来越多的证据表明神经状态具有高度动态性。在此,我们应用多变量模式分析来探索灵长类动物外侧前额叶皮层(PFC)在经典记忆引导扫视任务的三种变体过程中的群体动力学(在四只动物中进行记录)。我们在工作记忆任务的关键阶段观察到了动态群体编码的特征:感觉处理、记忆编码和反应执行。然而,在这些动态时期以及记忆延迟期,神经表征几何结构都保持稳定。我们确定了两个共同解释这些动力学的特征:(1)编码任务变量的神经元亚群随时间变化的改变(即动态亚群);以及(2)神经元内随时间变化的选择性(即动态选择性)。这些结果表明,即使在非常简单的记忆引导扫视任务中,PFC神经元也会表现出复杂的动力学以支持WM的稳定表征。灵活、智能的行为需要在不同时间跨度内维持和操纵传入信息。对于短时间跨度,这种能力被称为“工作记忆”(WM)。主流模型提出,WM由前额叶皮层(PFC)中稳定、持久的神经活动模式维持。然而,最近的证据表明,即使WM的内容保持稳定表征,PFC中的神经活动也是动态的。在此,我们在记忆引导扫视任务中探索了PFC中的神经动力学。我们发现,尽管WM的神经表征几何结构具有显著稳定性,但在不同任务时期仍存在动态群体编码的证据。此外,我们确定了两种不同的细胞机制,它们有助于动态群体编码。