Long-term meditators self-induce high-amplitude gamma synchrony during mental practice, by Antoine Lutz, Lawrence L. Greischar, Nancy B. Rawlings, Mathieu Ricard and Richard J. Davidson, in The Proceedings of the National Academy of Sciences USA 101(46)16369-16373, 2004

The challenge in studying consciousness has always been to match subjective, first person accounts with objective, third person measurements. Consciousness is, after all, publically unobservable. So there exists a dichotomy between phenomenological descriptions on the one hand and, on the other hand technologies such as fMRI and EEG which map brain activities correlating with cognition and consciousness.

First person phenomenological descriptions have largely stayed outside scientific and Western philosophical approaches, with the exception of William James and Husserlian types of introspection which recount the detailed content of consciousness. But the content of consciousness is not necessarily the same as consciousness itself. Indeed, an ongoing controversy has been whether one could be conscious of nothing. In an interesting debate at a Tucson conference a few years ago, Jonathan Shear argued for the affirmative, pointing out that meditators commonly cleared their mind of content but were nevertheless highly conscious of being. Other forms of meditation focus the practitioner�s mind on specific objects or actions, such as breathing or reciting mantras. In either type of case, an altered state of heightened awareness “of heightened consciousness” is said to be achieved. One might think that EEG or brain imaging of meditative states would be revealing, however previous studies have been largely unremarkable, suggesting for example a modest increase in slow alpha or theta wave EEG activity during meditation. However in those studies meditators were focusing on specific objects or activities. Moreover, higher frequency EEG activity such as gamma wave synchrony (greater than 25 Hz) was omitted.

Meanwhile, a controversy over gamma synchrony simmers. Synchronized gamma EEG is composed of field potentials measured from scalp or implanted electrodes which may be coherent both in local brain regions and more globally across the brain in a range from 30 to 70 Hz, known euphemistically as �coherent 40 Hz oscillations�. In the mid 1980s Wolf Singer�s lab showed that gamma synchrony corresponded with specific recognition in cat visual cortex. As other similar findings followed, coherent 40 Hz became the favorite electrophysiological correlate of cognition and consciousness. Gamma synchrony/40 Hz coherence was found to correspond with attention, face and linguistic recognition, visual binding, task performance, working memory, dreaming and the state of consciousness (e.g. by virtue of its selective disappearance with general anesthesia).

However a backlash set in, fueled largely, as far as I can tell, by the failure to account for gamma synchrony by axonal action potentials (�spikes�), the favorite level of reduction in much of neuroscience. The prevalent view has been that consciousness and cognition emerge from functional networks of neurons (�assemblies�, �modules�, �cartels�, �coalitions� etc.) linked by axonal output�to�dendritic input chemical neurotransmitter synapses. Donald Hebb showed in 1947 that altered sensitivities of such synapses would sculpt transient network assemblies, each of which could temporarily take the stage of attention and consciousness by dominant firing. So when 40 Hz correlations were discovered, the presumption was that sequences of axonal-dendritic Hebbian assemblies were firing synchronously at gamma range/40 Hz frequencies.

But synchrony among axonal spikes, and integration of spikes into network-like phenomena proved to be elusive. Francis Crick and Christof Koch, who in 1990 had helped launch the 40 Hz/consciousness bandwagon, were among the first to abandon ship. In some circles, gamma synchrony/40 Hz was discredited as an essential feature of consciousness, despite the continued correlations of gamma synchrony/40 Hz field potentials with cognition and consciousness. No spikes, no deal.

In recent years gamma synchrony has indeed been shown to derive not from axonal spikes and axonal-dendritic synapses, but from post-synaptic activities of dendrites. Specifically, gamma synchrony/40 Hz is driven by networks of cortical inter-neurons connected by dendro-dendritic “electrotonic” gap junctions, windows between adjacent cells. Groups of neurons connected by gap junctions share a common membrane and fire synchronously, behaving (as Eric Kandel says) �like one giant neuron.� Gap junctions have long been recognized as prevalent and important in embryological brain development, but gradually diminish in number (and presumably importance) as the brain matures. Five years ago gap junctions were seen as irrelevant to cognition and consciousness. However more recently, relatively sparse gap junction networks in adult brains have been appreciated and shown to mediate gamma synchrony/40 Hz.1-11 Such networks are transient, coming and going like the wind (and Hebbian assemblies), as gap junctions form, open, close and reform elsewhere (regulated by intraneuronal activities). Therefore neurons (and glia) fused together by gap junctions form continually varying syncytia, or Hebbian �hyper-neurons� whose common membranes depolarize coherently and may span wide regions of cortex. (The internal cytoplasm of hyper-neurons is also continuous, prompting suggestions they may host brain-wide quantum states.) By virtue of their relation to gamma synchrony, gap junction hyper-neurons may be the long-sought neural correlate of consciousness (NCC).

Which brings us to the study by Antoine Lutz and colleagues in the Proceedings of the National Academy of Sciences USA, a prestigious and austere (one might even say stodgy) journal of extremely high repute. The authors compared EEG in two subject groups before and during meditation�not of an object or activity, but of a pure feeling of unreferenced compassion. Dare I say this pure feeling might be deemed a quale?

One subject group was composed of young students trained for a week in meditative technique; the second group consisted of Tibetan Buddhist practitioners with 15 to 40 years of meditation training and practice. The EEG methodology was rigorous, and the results were clear. Compared to novice meditators, the highly trained Tibetan Buddhist meditators had markedly higher amplitude, long-range global gamma synchrony in bilateral frontal and parietal/temporal regions. An increase in gamma synchrony was also observed in baseline measurement (before meditation) which became enhanced and more global during meditation in the trained Tibetan meditators.

For technical reasons (possible muscle artifact and 60 Hz AC interference) the absolute frequency spectrum was not determined, though the experimenters hinted of a significant rise in synchrony and amplitude in the 80 to 120 Hz range during the Tibetans� meditation. The coherence and power in the range of 25 to 42 Hz was significantly increased statistically. (Coherence is usually defined as synchrony with a very brief lag, on the order of a few milliseconds). Amplitude of the synchronized gamma activity was greater than any previously reported nonpathological (i.e. non seizure-based) gamma synchrony.

So, what does this tell us about consciousness? Well first, there is an increase in gamma synchrony amplitude and coherence during what I think is fair to call an enhanced state of consciousness�pure intense experience unfettered by cognitive contents. This supports the notion of gamma synchrony as an electrophysiological correlate of consciousness.

Second, the trained Tibetan meditators had baseline increases in gamma synchrony and amplitude, suggesting long-term changes in their brains from years of meditation. One might say they are more highly conscious in a baseline state, achieving even greater intensity of consciousness during meditation.

In a book titled The Quantum and the Lotus by Mathieu Ricard and Trinh Xuan Thuan (Crown Publishers, 2001), Ricard (a molecular biologist turned Buddhist meditator and co-author of the Lutz study) describes the Buddhist concept of three levels of consciousness, including the most important �fundamental luminosity of the mind�. This is a �state of pure awareness that transcends the perception of a subject/object duality and breaks free from the constraints and traps of discursive thought.� Moreover this form of consciousness, according to Mathieu Ricard, can exist independently of the brain, and in fact pervades the universe. Presumably, the meditative state marked by enhanced gamma synchrony represents an immersion of the subjects in this fundamental luminosity. (Such a connection may possibly be explained through the quantum approach to consciousness. For example the Penrose-Hameroff model suggests a connection between brain processes and a funda-mental Platonic realm embedded in the space-time continuum.12,13)

Back to the brain. The enhanced gamma synchrony during the meditative state (as the authors tell us) is most likely due to a) an increase in the size of coherently responding neural assemblies, and/or b) increased precision in the coherence of responding neural assemblies.

Before addressing these possibilities, consider the origin of coherence. Even assuming that cortical neuronal assemblies interconnected by gap junctions (�hyper-neurons�) are the neural correlate of gamma synchrony, there are two possibilities for the coherence. One is that ascending or re-entrant thalamo-cortical inputs drive the cortical neuronal assemblies, like a piano player might rhythmically strike keys on a piano. The other is that the cortical neuronal assembly (hyper-neuron) itself is the source of coherence, due either to some internal reverberative feedback or common underlying mechanism in the extended membrane and/or cytoplasm/cytoskeleton. There are arguments against the thalamo-cortical drive mechanism for coherence based on delays in chemical neurotransmission and the slightly varying lengths of thalamo-cortical axons required to reach appropriate regions of cortex. In addition, thalamo-cortical drive would mean that the thalamus (rather than cortex) was responsible for choosing areas of cortex for consciousness (though proponents of this view point to cortical-thalamic feedback). These are open questions, though the fact that meditators whose consciousness is devoid of sensory inputs from the external world exhibit more highly coherent cortical excitations suggests that thalamic inputs reduce, rather than promote, gamma synchrony. Thus both enhanced a) size and b) coherence precision of cortical assemblies seem likely.

Like most good research, this study raises more questions than it answers. How is the content�in this case the pure quale of compassion�represented? Is it in the specific coherent frequency? Is it in the specific neural regions entrained in the coherent process? Is it in some finer-grained process? Are the coherence, amplitude and/or frequency related to intensity of experience?

One could say (I would not) that the gamma synchrony/coherent 40 Hz corresponding with contentless meditation implied a blank slate, perhaps like a radio station carrier wave, that the coherent amplitude increase was due to lack of interference stemming from lack of cognitive processing. But the trained meditators were conscious�highly conscious�of the feeling of pure compassion. So my impression, as suggested above, is that their enhanced gamma synchrony reflected a release from external (e.g. thalamic) distractions, allowing pure qualia to fill consciousness. Why gamma synchrony (or any brain activity) should be conscious is, of course the �hard problem�. As those familiar with my views might suppose, my guess is that conscious experience derives from quantum mechanisms in cytoskeletal structures within coherently excited components of hyper-neurons. These in turn facilitate a more direct absorption in what Buddhists call fundamental luminosity. My guess is also that intensity of experience corresponds not only with coherence, but also frequency, that the 80 to 120 Hz coherence is present in the trained meditators and represents the highest form of consciousness.

The experimenters plan on further work, with refined analysis of the meditative practice and feeling of unreferenced compassion. Among other issues, I personally would like to see them look closely at the higher frequencies they tantalized us with in this paper.

In any case this is a landmark study and the researchers are to be congratulated, and thanked! They cite the work of the late Francisco Varela who pioneered the connection between meditation and neuroscience. Francisco would be pleased indeed.

Copyright © 2005 S. Hameroff

Stuart Hameroff M.D.
Professor, Departments of Anesthesiology and Psychology
Director, Center for Consciousness Studies
The University of Arizona, Tucson, Arizona

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