The Spatiotemporal Dynamics of Oscillatory Activity in Humans Across Micro, Meso, and Macro Scales

Brain activity is characterized by oscillatory activity that spans at least two orders of magnitude. Previous investigations of the spatiotemporal dynamics of this wide range of oscillatory behavior has led to the concept that long-range intercortical interactions are expressed in low-frequency patterns while higher frequencies reﬂect more local intracortical connectivity. This inverse relationship between frequency and spatial coherence is seen as one of a small number of nearly universal rules governing brain activity. While there is substantial evidence for this proposition, there are surprisingly few direct, quantitative investigations of this phenomenon, especially in human cortex. To more completely characterize the spatial characteristics of ongoing brain activity, we investigated the coherence in diﬀerent brain states- awake and sleep, at diﬀerent frequencies, and with respect to a wide range of distances using standard pial surface macroelectrode arrays (1 cm spacing in an 8x8 cm grid), mesogrids (5 mm spacing), microgrids (1 mm spacing), and microelectrode arrays (400 micron spacing in 4x4mm arrays). As expected, we found that correlations and coherence decreases as a function of increasing interelectrode distance and as a function of frequency. We observed a robust linear relationship up until 1 cm; for distances 1 cm and greater, the relationship was largely non-linear. This relationship was not strongly aﬀected by speciﬁc cortical lobe, nor was the overall coherence signiﬁcantly diﬀerent between awake and asleep states. These data are congruent with the overall notion that frequency and spatial relationships are inversely related with faster frequencies being more focal and provides an important quantitative assessment of that relationship with implications for the spatial scale of neural processing and recordings. Abstract Previous investigations of the spatiotemporal dynamics of oscillatory behavior in the brain has lead to the concept that slower activity has coherence spanning over a wider area than that of higher frequency activity. This is seen as one of a small number of nearly universal rules which dictates activity in cortical and subcortical structures. There is substantial evidence for this proposition in the literature but surprisingly few direct investigations, especially in human cortex. Furthermore, the majority of investigations of this issue have focused on relatively large distances. For this reason we investigated the coherence in diﬀerent brain states- awake and sleep- at diﬀerent frequencies with respect to distance using both standard pial surface macroelectrode arrays (1 cm spacing in a 8x8 cm grid), macroelectrode arrays which penetrate the brain parenchyma and both microgrid (1 mm spacing) and NeuroPort microelectrode arrays (400 micron spacing in 4x4mm arrays). As expected, we found that coherence decreases as a function of increasing interelectrode distance; for both electrode types there was a decrement in coherence over space. For the macrogrids and distances greater than 1 cm, the relationship was largely non-linear. In contrast, at the microscale the drop in coherence was linear. This relationship was not strongly aﬀected by state, nor was the overall coherence signiﬁcantly diﬀerent between awake and asleep states. The impact of frequency on spatial relationship was variable from subject to subject but showed a trend toward more rapid declines in coherence in higher frequency bands. These data are congruent with the overall notion that frequency and spatial relationships are inversely related with faster frequencies being more focal. Abstract Previous investigations of the spatiotemporal dynamics of oscillatory behavior in the brain has led to the concept that slower activity has coherence spanning a wider area than that of higher frequency activity. This is seen as one of a small number of nearly universal rules which dictates activity in cortical and subcortical structures. There is substantial evidence for this proposition in the literature but surprisingly few direct investigations, especially in human cortex. Furthermore, the majority of investigations of this issue have focused on relatively large distances. To more completely characterize the spatial characteristics of ongoing brain activity, we investigated the coherence in diﬀerent brain states, awake and sleep, at diﬀerent frequencies and with respect to a wide range of distances using both standard pial surface macroelectrode arrays (1 cm spacing), macroelectrode arrays which penetrate the brain parenchyma and both microgrid (1 mm spacing) and NeuroPort microelectrode arrays (400 micron spacing). As expected, we found that coherence decreases as a function of increasing interelectrode distance.For distances 1 cm and greater, the relationship was largely non-linear, and smaller gaps behave more linearly. This relationship was not strongly aﬀected by recording location, nor was the overall coherence signiﬁcantly diﬀerent between awake and asleep states. The impact of frequency on spatial relationship was variable from subject to subject but showed a trend toward more rapid declines in coherence in higher frequency bands. These data are congruent with the overall notion that frequency and spatial relationships are inversely related with faster frequencies being more focal.