A Stable Population Code for Attention in Prefrontal Cortex Leads a Dynamic Attention Code in Visual Cortex
A Stable Population Code for Attention in Prefrontal Cortex Leads a Dynamic Attention Code in Visual Cortex
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DOI：
10.1523/jneurosci.0608-21.2021
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发表时间：
2021-09
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影响因子：
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通讯作者：
A. Snyder;Byron M. Yu;M. A. Smith
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作者：
A. Snyder;Byron M. Yu;M. A. Smith
注意力通常需要随着时间的推移保持稳定的精神状态，同时提高感知灵敏度。这些要求对神经群体提出了相互矛盾的要求，因为敏感性意味着对传入刺激的扰动的鲁棒响应，这与稳定性是对立的。皮质区的功能特化提供了一种解决这种冲突的潜在机制。我们推断，随着时间的推移，执行控制区域中的注意信号可能是高度稳定的，反映了认知状态的维持，从而释放了感觉区域，使其对感觉输入更加敏感（即，不稳定），这将反映在这些领域更动态的注意信号。为了测试这些预测，我们同时记录了在前额叶皮层（PFC）和视觉皮层V4区的恒河猴执行内源性空间选择性注意任务的神经种群。使用解码方法，我们发现PFC中注意力状态的神经代码随着时间的推移比V4中的注意力代码更稳定，这与我们的指导理论一致。此外，注意信号在PFC预测未来的注意状态的V4比反之亦然，符合自上而下的作用PFC的注意。这些结果表明，注意力机制的功能专业化，跨皮层区域的分工。PFC发出认知状态的信号，并随着时间的推移稳定地保持这种状态，而V4则以受该认知状态动态调节的方式对感觉输入做出响应。注意力需要保持稳定的精神状态，同时提高感知灵敏度。我们假设这两个需求（稳定性和敏感性）分别分布在前额叶和视觉皮层区域。具体来说，我们预测的注意力信号在视觉皮层将不稳定比在前额叶皮层，而且前额叶皮层信号将预测注意力信号在视觉皮层与假设的作用，前额叶皮层在自上而下的执行控制。我们的研究结果是一致的建议，从以前的工作中使用单独的记录在两个大脑区域在不同的动物执行不同的任务，并代表了第一个直接的证据，支持这一假设，同时多区域记录在个别动物。
Attention often requires maintaining a stable mental state over time while simultaneously improving perceptual sensitivity. These requirements place conflicting demands on neural populations, as sensitivity implies a robust response to perturbation by incoming stimuli, which is antithetical to stability. Functional specialization of cortical areas provides one potential mechanism to resolve this conflict. We reasoned that attention signals in executive control areas might be highly stable over time, reflecting maintenance of the cognitive state, thereby freeing up sensory areas to be more sensitive to sensory input (i.e., unstable), which would be reflected by more dynamic attention signals in those areas. To test these predictions, we simultaneously recorded neural populations in prefrontal cortex (PFC) and visual cortical area V4 in rhesus macaque monkeys performing an endogenous spatial selective attention task. Using a decoding approach, we found that the neural code for attention states in PFC was substantially more stable over time compared with the attention code in V4 on a moment-by-moment basis, in line with our guiding thesis. Moreover, attention signals in PFC predicted the future attention state of V4 better than vice versa, consistent with a top-down role for PFC in attention. These results suggest a functional specialization of attention mechanisms across cortical areas with a division of labor. PFC signals the cognitive state and maintains this state stably over time, whereas V4 responds to sensory input in a manner dynamically modulated by that cognitive state. SIGNIFICANCE STATEMENT Attention requires maintaining a stable mental state while simultaneously improving perceptual sensitivity. We hypothesized that these two demands (stability and sensitivity) are distributed between prefrontal and visual cortical areas, respectively. Specifically, we predicted attention signals in visual cortex would be less stable than in prefrontal cortex, and furthermore prefrontal cortical signals would predict attention signals in visual cortex in line with the hypothesized role of prefrontal cortex in top-down executive control. Our results are consistent with suggestions deriving from previous work using separate recordings in the two brain areas in different animals performing different tasks and represent the first direct evidence in support of this hypothesis with simultaneous multiarea recordings within individual animals.