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In 1999, an experiment found that at the moment of conscious perception of the face, the gamma rhythms measured at distant areas were synchronized. This result was published in the authoritative journal Nature (Rodriguez et al., 1999), which led many researchers to believe that gamma synchronization is the key to the emergence of consciousness. However, to date, there have been two papers demonstrating that when general anesthetics and deep sleep cause loss of consciousness, the gamma power actually increases (Murphy et al., 2011; Bola et al., 2018).
As mentioned in Chapter 31, consciousness has two components: arousal and awareness. Arousal is a necessary, but not sufficient, condition for the emergence of consciousness. The Nature paper only reveals that gamma rhythms are implicated in awareness. General anesthetics and deep sleep can dramatically suppress the level of arousal, such that consciousness cannot emerge even if the awareness reflected by the gamma power is high. This and subsequent chapters will show that the true protagonist of consciousness is the alpha rhythm.
The Role of Alpha in Consciousness
A night of sleep can be divided into several stages (Chapter 31). From N1 to N3, the sleep deepens, with increasing difficulty of arousal. The N3 stage is known as slow wave sleep (SWS) during which both arousal and awareness levels are low. The REM sleep has higher arousal and awareness levels than SWS (Figure 31f). Suppose alpha plays a key role in consciousness, we expect REM sleep should have stronger alpha power than SWS. Surprisingly, earlier studies obtained opposite results.
Traditional electroencephalography (EEG) measures only local voltage changes, that is, the positions where electrodes are placed. This approach does not reveal global synchronization at a specific frequency band. In 2001, a new method, called "global field synchronization" (GFS), was introduced (Koenig et al., 2001). By using GFS, Achermann et al. found that among all sleep stages, REM sleep was the most globally synchronized state (Figure 35a). This supports the view that global synchronization at the alpha band reflects consciousness level. The local alpha power is not a good indicator of consciousness.
Brain damages cause varying degrees of consciousness deficits. The most serious case is coma, followed by the vegetative state (VS) and then minimally conscious state (MCS). Coma is characterized by flat or nealy flat EEG, but in rare cases, the alpha-like activity may occur. It is generally believed that the alpha frequency pattern in comatose patients represents a de novo rhythm, distinct from the waking alpha rhythm (Parvathy et al., 2017). Patients with VS and MCS exhibit reduced power in the alpha range and increased power in the delta and theta range (Corchs et al., 2019).
When awake, the alpha power is strongest in the occipital lobe located at the back of the brain. There is a class of general anesthetics that act on GABAA receptors, such as propofol and sevoflurane, leading to the "anteriorization" of the alpha rhythm, that is, the alpha power decreases in the posterior part of the brain but increases in the forebrain (Vijayan et al., 2013). Further studies have found that the sevoflurane-induced unconsciousness is not related to the alpha anteriorization, but because it disrupts anterior-posterior phase relationships in the alpha bandwidth (Blain-Moraes et al., 2015).
Ketamine is another class of general anesthetics that do not cause alpha anteriorization. The key for ketamine to induce unconsciousness has been found to reduce the frontal-parietal connectivity in the alpha bandwidth (Blain-Moraes et al., 2014). Since neuronal synchronization underlies functional connectivity, this provides additional evidence that large-scale synchronization at the alpha band is crucial for the emergence of consciousness.
The Sources of Alpha Rhythms
The thalamus projects to the cerebral cortex via the "thalamocortical" (TC) neurons. A subset of TC neurons have a higher threshold for generating nerve impulses than typical neurons. These "high-threshold TC" (HTC) neurons are connected to each other by gap junctions (Lörincz et al., 2008; Hughes et al., 2011). They oscillate synchronously at the alpha band, representing a major source of alpha rhythms (Schreckenberger et al., 2004). On the other hand, the cerebral cortex can also independently produce alpha rhythms (Connemann et al., 2005; Bollimunta et al., 2011; Haegens et al., 2015; Ellis et al., 2017; Sokoliuk et al., 2019).
In the cortex, there are three types of GABAergic interneurons: parvalbumin (PV)-positive, somatostatin (SOM or SST)-positive and cholecystokinin (CCK)-positive. CCK cells are also called 5HT3R interneurons because they express 5-HT3 receptors. The PV cells oscillate at the gamma band (30-80 Hz) which is critical for cognition. They are also referred to as fast-spiking (FS) interneurons. SOM cells fire at 10-30 Hz with low threshold, thus also called low-threshold-spiking (LTS) interneurons (Mancilla et al., 2007). During theta oscillations, CCK cells fire at 8.8 ± 3.3 Hz on the ascending phase of theta rhythms (Klausberger et al., 2005). Note that SOM cells oscillate mainly in the beta band (13 - 30 Hz) while CCK cells oscillate predominantly in the alpha band.
It has been well documented that gamma oscillations of pyramidal neurons are synchronized by PV cells (see this article). Similarly, the alpha oscillations of pyramidal neurons could be paced by CCK cells. In support of this idea, the HTC neurons have been found to project directly to cortical inhibitory interneurons that target pyramidal neurons (Vijayan and Kopell, 2012, Figure 5). The inhibitory interneurons could be CCK cells as CCK binding sites consistently coincide with the cortical projections of thalamic nuclei: CCK binding in the primary visual cortex corresponds to the terminal field disposition of LGN while in somatosensory cortex, the pattern of CCK binding in layer IV coincides with thalamic inputs arising from the ventrobasal complex (Kritzer et al., 1987). Therefore, the posterior alpha rhythms could arise primarily from interaction between thalamic HTC neurons and CCK cells in the sensory cortex (Figure 35b).
CCK cells exist not only in the sensory cortex. In fact, they are most numerous within the medial prefrontal cortex (which includes ACC) (Whissell et al., 2015). The neuropeptide CCK is especially abundant in the ACC (Ere et al., 2004; Gustafsson et al., 2000). Like PV interneurons, CCK cells are connected by gap junctions (Ma et al., 2011). Therefore, CCK cells may be employed to synchronize the alpha rhythms of pyramidal neurons in both prefrontal and sensory cortices through the same mechanism as PV-mediated gamma synchronization (see this article). During the inhibition-based synchronization, pyramidal neurons should be firing in response to continuous excitatory inputs. In the cortex, the required excitatory inputs may come from regular TC neurons and other inputs (Figure 35b).
Although alpha rhythms have several independent sources, they are functionally connected. As mentioned in Chapter 31, the level of consciousness is reflected in the connectivity of the default mode network which, in turn, is correlated with large-scale synchronization at the alpha band.
The Role of Alpha in Attention
When you are conscious, you have the capacity to be aware of sensory stimuli. However, humans have five sensory systems: vision, hearing, touch, taste and smell. Right now, your eyes are focused on this book, while sounds may be humming around your ears, but at any moment you can perceive only one thing: the content of the book or the surrounding sounds. When you pay attention to this book, you do not hear the sound even though it still keeps reaching your ears. Attention allows the mind to select important sensory information. Without this ability, the mind would fall into chaos.
Numerous studies have established that the alpha rhythm plays a central role in attention (Klimesch, 2012; Mathewson et al., 2009; Schroeder et al., 2018; Deng et al., 2019; Misselhorn et al., 2019; Deiber et al., 2020). How does the alpha rhythm select sensory information? This question is addressed in the next chapter.
Author: Frank Lee