The encoding of information in spike phase relative to local field potential (LFP) oscillations offers several theoretical advantages over equivalent firing rate codes. One notable example is provided by place and grid cells in the rodent hippocampal formation, which exhibit phase precession—firing at progressively earlier phases of the 6–12 Hz movement‐related theta rhythm as their spatial firing fields are traversed. It is often assumed that such phase coding relies on a high amplitude baseline oscillation with relatively constant frequency. However, sustained oscillations with fixed frequency are generally absent in LFP and spike train recordings from the human brain. Hence, we examine phase coding relative to LFP signals with broadband low‐frequency (2–20 Hz) power but without regular rhythmicity. We simulate a population of grid cells that exhibit phase precession against a baseline oscillation recorded from depth electrodes in human hippocampus. We show that this allows grid cell firing patterns to multiplex information about location, running speed and movement direction, alongside an arbitrary fourth variable encoded in LFP frequency. This is of particular importance given recent demonstrations that movement direction, which is essential for path integration, cannot be recovered from head direction cell firing rates. In addition, we investigate how firing phase might reduce errors in decoded location, including those arising from differences in firing rate across grid fields. Finally, we describe analytical methods that can identify phase coding in the absence of high amplitude LFP oscillations with approximately constant frequency, as in single unit recordings from the human brain and consistent with recent data from the flying bat. We note that these methods could also be used to detect phase coding outside of the spatial domain, and that multi‐unit activity can substitute for the LFP signal. In summary, we demonstrate that the computational advantages offered by phase coding are not contingent on, and can be detected without, regular rhythmicity in neural activity.

中文翻译：

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无节奏情况下相位编码的优点和检测。

相对于局部场电位（LFP）振荡的尖峰相位信息编码与等效发射率编码相比具有多个理论上的优势。啮齿动物海马结构中的位置细胞和网格细胞提供了一个值得注意的例子，它们表现出相位进动——随着它们的空间发射场被遍历，在 6-12 Hz 运动相关的 θ 节律的逐渐早期的阶段发射。通常假设这种相位编码依赖于具有相对恒定频率的高振幅基线振荡。然而，人脑的 LFP 和尖峰序列记录中通常不存在固定频率的持续振荡。因此，我们检查相对于具有宽带低频（2-20 Hz）功率但没有规则节奏的 LFP 信号的相位编码。我们模拟了一群网格细胞，这些网格细胞表现出与从人类海马体深度电极记录的基线振荡相对的相位进动。我们证明，这允许网格细胞放电模式复用有关位置、跑步速度和运动方向的信息，以及以 LFP 频率编码的任意第四个变量。鉴于最近的研究表明，对于路径整合至关重要的运动方向无法从头部方向的细胞放电率中恢复，这一点尤其重要。此外，我们还研究了发射阶段如何减少解码位置中的错误，包括由于网格场之间的发射率差异而产生的错误。最后，我们描述了可以在没有高振幅 LFP 振荡的情况下以近似恒定频率识别相位编码的分析方法，如来自人脑的单个单元记录，并且与飞行蝙蝠的最新数据一致。我们注意到这些方法也可用于检测空间域外的相位编码，并且多单元活动可以替代 LFP 信号。总之，我们证明了相位编码提供的计算优势并不取决于神经活动的规则节律性，并且可以在没有规则节律性的情况下被检测到。