McKnight Brain Institute, Department of Neuroscience, University of Florida , Gainesville, Florida.
Engineering School of Sustainable Infrastructure and Environment, University of Florida , Gainesville, Florida.
J Neurophysiol. 2019 Feb 1;121(2):444-458. doi: 10.1152/jn.00636.2018. Epub 2018 Dec 5.
Oscillations in the hippocampal local field potential at theta and gamma frequencies are prominent during awake behavior and have demonstrated several behavioral correlates. Both oscillations have been observed to increase in amplitude and frequency as a function of running speed. Previous investigations, however, have examined the relationship between speed and each of these oscillation bands separately. Based on energy cascade models where "…perturbations of slow frequencies cause a cascade of energy dissipation at all frequency scales" (Buzsaki G. Rhythms of the Brain, 2006), we hypothesized that cross-frequency interactions between theta and gamma should increase as a function of speed. We examined these relationships across multiple layers of the CA1 subregion, which correspond to synaptic zones receiving different afferents. Across layers, we found a reliable correlation between the power of theta and the power of gamma, indicative of an amplitude-amplitude relationship. Moreover, there was an increase in the coherence between the power of gamma and the phase of theta, demonstrating increased phase-amplitude coupling with speed. Finally, at higher velocities, phase entrainment between theta and gamma increases. These results have important implications and provide new insights regarding how theta and gamma are integrated for neuronal circuit dynamics, with coupling strength determined by the excitatory drive within the hippocampus. Specifically, rather than arguing that different frequencies can be attributed to different psychological processes, we contend that cognitive processes occur across multiple frequency bands simultaneously with organization occurring as a function of the amount of energy iteratively propagated through the brain. NEW & NOTEWORTHY Often, the theta and gamma oscillations in the hippocampus have been believed to be a consequence of two marginally overlapping phenomena. This perspective, however, runs counter to an alternative hypothesis in which a slow-frequency, high-amplitude oscillation provides energy that cascades into higher frequency, lower amplitude oscillations. We found that as running speed increases, all measures of cross-frequency theta-gamma coupling intensify, providing evidence in favor of the energy cascade hypothesis.
在清醒行为期间，海马体局部场电位在 theta 和 gamma 频率处的波动很明显，并且已经证明了其与多种行为具有相关性。这两种波动都被观察到随着跑步速度的增加而增加幅度和频率。然而，之前的研究分别检查了速度与这些振荡频带中每一个的关系。基于能量级联模型，其中“……慢频率的扰动导致在所有频率尺度上的能量耗散级联”（Buzsaki G. Rhythms of the Brain，2006），我们假设 theta 和 gamma 之间的交叉频率相互作用应该随着速度的增加而增加。我们在 CA1 子区域的多个层中检查了这些关系，这些层对应于接收不同传入的突触区。在各层中，我们发现 theta 功率和 gamma 功率之间存在可靠的相关性，表明存在幅度-幅度关系。此外，gamma 功率和 theta 相位之间的相干性增加，表明随着速度的增加，相位-幅度耦合增加。最后，在较高的速度下，theta 和 gamma 之间的相位锁定增加。这些结果具有重要意义，并为 theta 和 gamma 如何整合用于神经元电路动力学提供了新的见解，耦合强度由海马体内的兴奋性驱动决定。具体而言，我们认为，不是不同的频率可以归因于不同的心理过程，而是认知过程同时发生在多个频带中，组织发生的方式是作为通过大脑传播的能量的量的函数。新的和值得注意的是，海马体中的 theta 和 gamma 振荡通常被认为是两个略有重叠现象的结果。然而，这种观点与另一种假设相矛盾，即低频、高幅度的振荡提供能量，该能量级联成更高频率、更低幅度的振荡。我们发现，随着跑步速度的增加，所有跨频 theta-gamma 耦合的测量值都加强了，这为能量级联假说提供了证据。
