Department of Psychological and Brain Sciences, Dartmouth College, Hanover 03755, New Hampshire.
Neurosciences Program, Stanford University, Stanford 94305, California.
J Neurosci. 2024 Jan 10;44(2):e2442212023. doi: 10.1523/JNEUROSCI.2442-21.2023.
Cortical neurons exhibit multiple timescales related to dynamics of spontaneous fluctuations (intrinsic timescales) and response to task events (seasonal timescales) in addition to selectivity to task-relevant signals. These timescales increase systematically across the cortical hierarchy, for example, from parietal to prefrontal and cingulate cortex, pointing to their role in cortical computations. It is currently unknown whether these timescales are inherent properties of neurons and/or depend on training in a specific task and if the latter, how their modulations contribute to task performance. To address these questions, we analyzed single-cell recordings within five subregions of the prefrontal cortex (PFC) of male macaques before and after training on a working-memory task. We found fine-grained but opposite gradients of intrinsic and seasonal timescales that mainly appeared after training. Intrinsic timescales decreased whereas seasonal timescales increased from posterior to anterior subregions within both dorsal and ventral PFC. Moreover, training was accompanied by increases in proportions of neurons that exhibited intrinsic and seasonal timescales. These effects were comparable to the emergence of response selectivity due to training. Finally, task selectivity accompanied opposite neural dynamics such that neurons with task-relevant selectivity exhibited longer intrinsic and shorter seasonal timescales. Notably, neurons with longer intrinsic and shorter seasonal timescales exhibited superior population-level coding, but these advantages extended to the delay period mainly after training. Together, our results provide evidence for plastic, fine-grained gradients of timescales within PFC that can influence both single-cell and population coding, pointing to the importance of these timescales in understanding cognition.
皮质神经元表现出多种与自发性波动（内在尺度）和对任务事件的反应（季节性尺度）相关的时间尺度，除了对任务相关信号的选择性。这些时间尺度在皮质层次结构中系统地增加，例如，从顶叶到前额叶和扣带回皮质，表明它们在皮质计算中的作用。目前尚不清楚这些时间尺度是神经元的固有特性，还是取决于特定任务的训练，如果是后者，它们的调制如何有助于任务表现。为了解决这些问题，我们分析了雄性猕猴前额叶皮质 (PFC) 的五个亚区在进行工作记忆任务训练前后的单细胞记录。我们发现了精细但相反的内在和季节性时间尺度梯度，主要出现在训练之后。内在时间尺度从背侧和腹侧 PFC 的后向前亚区降低，而季节性时间尺度增加。此外，训练伴随着表现出内在和季节性时间尺度的神经元比例增加。这些效应与由于训练而出现的反应选择性相似。最后，任务选择性伴随着相反的神经动力学，即具有任务相关选择性的神经元表现出较长的内在时间尺度和较短的季节性时间尺度。值得注意的是，具有较长内在时间尺度和较短季节性时间尺度的神经元表现出更高的群体水平编码，但这些优势主要在训练后延伸到延迟期。总之，我们的研究结果提供了 PFC 中具有可塑性、精细时间尺度梯度的证据，这些梯度可以影响单个细胞和群体编码，表明这些时间尺度在理解认知中的重要性。
