Experimental observation of phase-flip transitions in the brain

The phase-flip transition has been demonstrated in a host of coupled nonlinear oscillator models, many pertaining directly to understanding neural dynamics. However, there is little evidence that this phenomenon occurs in the brain. Using simultaneous microelectrode recordings in the nonhuman primate cerebral cortex, we demonstrate the presence of phase-flip transitions between oscillatory narrow-band local field potential signals separated by several centimeters. Specifically, we show that sharp transitions between in-phase and antiphase synchronization are accompanied by a jump in synchronization frequency. These findings are significant for two reasons. First, they validate predictions made by model systems. Second, they have potentially far reaching implications for our understanding of the mechanisms underlying corticocortical communication, which are thought to rely on narrow-band oscillatory synchronization with specific relative phase relationships.

Figure 1

Schematic of the nonhuman primate brain and example data. (a) The brain is shown from anterior (Ant.) to posterior (Post.), with sulci labeled for reference. (PS) Principal sulcus. (AS) Arcuate sulcus. (CS) Central sulcus. (IPS) Intraparietal sulcus. (STS) Superior temporal sulcus. (LS) Lunate sulcus. (b) Bandpassed (8–25 Hz) local field potential signals for two trials during the ITI. The signals are from channel 5 (solid line) and channel 7 (dashed line). Time and voltage scales are provided at the bottom left of the plot.

Figure 2

Example phase-flip transition between channel 5 and channel 7. (a) Gabor functions (fit to each average cross-correlogram) at each time step ($x$ axis), with time lag on the $y$ axis and the correlation coefficient shown in color on the $z$ axis. (b) Relative phase (left $y$ axis) and synchronization frequency (right $y$ axis) over time.

Figure 3

Summary of the relative phase over time, for all signal pairs from example session. Each horizontal bar shows the relative phase for a single signal pair. Gray scale indicates the relative phase, from in phase (black) to antiphase (white).

Figure 4

Summary of the relative phase and synchronization frequency for six example signal pairs. The relative phase (dark gray; absolute value) is on the left $y$ axis. The synchronization frequency (light gray) is on the right $y$ axis. Channel numbers are indicated at the top of each figure. Signals are from somatosensory area 2 (channel 1), somatosensory area 1 (channel 2), somatosensory area 3 (channel 3), frontal area 5 (channels 4 and 5), prefrontal area 8L (channel 6), and prefrontal area 9/46d (channel 7).

Figure 5

Population data for signal pairs with prefrontal area 9/46d or prefrontal area 8L and the somatosensory areas (1, 2, and 3) and frontal area 5. (a) Synchronization frequencies for the early and late ITI for all signal pairs with prefrontal area 9/46d. (b) Synchronization frequencies for the early and late ITI for all signal pairs with prefrontal area 8L. (c) Relative phase angles for the early and late ITI for all signal pairs with prefrontal area 9/46d. (d) Relative phase angles for the early and late ITI for all signal pairs with prefrontal area 8L. Asterisk (*) indicates that medians are different at $p<0.0005$.