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A brain consists of many functionally specialized areas. Synchronization among relevant areas is critical for efficient performance of a specific task. For instance, in the awake cat, a sudden change of a visual pattern induces synchronization between areas of the visual and parietal cortex, and between areas of the parietal and motor cortex. Despite the long distance between synchronized areas, the synchronization occurs with zero phase lag (Roelfsema et al., 1997), which is remarkable considering that synaptic transmission and axon conduction will cause delay. The zero lag synchronization has also been observed in hippocampal-prefrontal synchrony during working memory, and prefrontal-amygdala synchrony during anxiety (Harris and Gordon, 2015).
Coupling by Radio Waves
Synchronization among a population of neurons indicates that these neurons are somehow "coupled", namely, they must interact with each other. The gap junctions (also known as "electrical synapses") have been demonstrated to mediate the coupling between adjacent neurons for synchronization. In many cases, short interneurons are also employed to achieve local synchronization (see this article). However, the long range synchronization cannot be accomplished by gap junctions or interneurons. A number of models have been proposed (reviewed in Uhlhaas, 2009), but they still lack experimental support. Perhaps the simplest way to achieve long range zero lag synchronization is via electromagnetic (EM) waves which travel at light speed.
The radio waves emitted from mobile phones are strong enough to increase cortical excitability and thus the alpha rhythms (Valentini et al., 2007). The frequency of the EM waves radiated by accelerated ions through ion channels is about 10 MHz, which falls in the radio frequency. It has been estimated that synchronization of about 104 neurons can transmit radio waves with the power comparable to mobile phones (see this article). Therefore, local synchronization via gap junctions or short interneurons can emit sufficiently strong radio waves to trigger neuronal firing in distant areas, possibly via microtubule antennas in the axon initial segment. Such EM coupling occurs at light speed. Furthermore, the radio waves emitted from one brain area can immediately be received by any neurons in the brain, but only the targeted (relevant) neurons may join the long range synchronization.
Targeting by Neuronal Resonance
Most central neurons respond selectively to inputs at a preferred frequency. This feature is known as "resonance", which arises from both passive and active membrane properties. The passive property always filters out high frequencies, while the active property may filter out low frequencies, thereby resulting in a preferred frequency (Hutcheon and Yarom, 2000; PDF; Figure 10-5). The active property is determined by ion channels, particularly the HCN channel which regulates the spiking frequencies from 1 Hz to 13 Hz, encompassing delta, theta and alpha bands (Section 7.5). The gamma band (30 - 80 Hz) is regulated by Kv1 (Sciamanna and Wilson, 2011). Another K+ channel, Kv3, is important for faster spiking (Erisir et al., 1999). Hence, a group of neurons can oscillate at the same frequency, as long as they have the same intrinsic property.
Targeting by Microtubule Antennas
As mentioned in this article, the number of microtubules per fascicle ranges from three to five in the motor neurons of the spinal cord, but can reach 22 in the pyramidal neurons of the cerebral cortex. Motor neurons are generally not involved in long range synchronization. They are also less prone to Tau pathology. The Tau proteins can induce microtubule bundling (Scott et al., 1992). They could play important roles in the modulation of fascicle strctures for the best performance of microtubule antennas.
Many pyramidal neurons in layer V of the neocortex (Figure 10-6) exhibit intrinsic firing frequencies at the theta and alpha bands (5 - 12 Hz) (Silva et al., 1991). These neurons could be a major target of long range synchronization. Incidentally, in Alzheimer's disease, Tau pathology occurs preferentially in the neocortical layers V and VI (Hof et al., 1992). The next section will present further evidence that Tau could modulate the interaction between microtubule fascicles and the incoming EM waves.
Author: Frank Lee