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Electronic Letters to:
- BehavioralSystemsCognitive:
Thomas Radman, Yuzhuo Su, Je Hi An, Lucas C. Parra, and Marom Bikson- Spike Timing Amplifies the Effect of Electric Fields on Neurons: Implications for Endogenous Field Effects
J. Neurosci. 2007; 27: 3030-3036[Abstract] [Full text] [PDF]
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Electronic letters published:
Is the EEG an epiphenomenon?
- David M. Alexander (21 October 2007)
Is the EEG an epiphenomenon? 21 October 2007 
David M. Alexander,
Research Scientist
Laboratory for Perceptual Dynamics, RIKEN Brain Science Institute, Wako-shi, Saitama, 351-0198, JapaSend letter to journal:
Re: Is the EEG an epiphenomenon?
dalex{at}brain.riken.jp David M. Alexander
That large-scale electrical field dynamics measured in the EEG play a causal role in brain function is a controversial claim in neuroscience. And yet this seems to follow from the recent article by Radman et al.(2007). The authors conclude that "extracellular gamma oscillations could facilitate coherence across a large population of neurons". The authors also cite research on transcranial electrical stimulation (Marshall et al., 2006), which demonstrates improvement in memory performance as a result of transcranially applied fields. The latter authors conclude: "our results challenge the common view that extracellular slow potential oscillations represent mere epiphenomena without physiological significance per se." As reported by Massimini et al. (2004), slow-wave sleep EEG has been shown to take the form of a global spatio-temporal wave . Such waves are able to act as an 'external' source of electric fields to individual minicolumns in the cortex. There is now sufficient evidence to outline the case that large-scale electricalfield dynamics do indeed play a causal role in brain activity, and to propose confirmatory experiments.
1. Radman et al. (2007) applied external electric fields to CA1 hippocampal pyramidal slices in vitro. They found that DC and oscillatory fields (of appropriate phase) advance the timing of spikes emitted. The externally applied field strengths were smaller than those measured in vivo. Related results have been found for CA3 pyramidal cells (Deans et al. 2007). Under the influence of weak gamma-band oscillatory fields, the peak power of the cells' activity shifted to the frequency of the externally applied field and increased in magnitude. Externally applied fields with a frequency of 10 Hz or below had similar effects as DC fields. Consistent results and conclusions have been reported by Fujisawa et al. (2004). An earlier paper by Taylor et al. (1984) presents evidence that the membrane potentials of CA3 pyramidal cells in vivo are influenced by antidromic spikes via extracellular electric fields. This finding opens the intriguing possibility that electric field coupling may also play a role in long-term potentiation (Taylor et al., 1984).
2. The EEG has long been known to result from the massed activity of the electric fields of hundreds of thousands of neurons, dominated by cortical activity nearest the scalp (Tallon-Baudry et al., 1999). Pyramidal cells in the cortex form densely packed vertical bundles, usually including dendritic shafts extending from cell bodies located in layers II, III and V (Rockland and Ichonohe, 2004). In monkey V1, for example, these minicolumns are comprised of approximately thirty adjacent vertical shafts within the space of ~23 um in layers II/III (Peters and Sethares, 1996). Such densely packed dendritic volumes in the cortex have the requisite physical properties to enable the electric field coupling proposed to occur in the hippocampus.
3. Modern EEG techniques can be used to measure cortical activity at a variety of scales. At one extrema, source localization techniques attempt to measure dipoles of activity within the grey matter (Koles, 1998; Michel et al., 2004). A contrasting approach is the measurement of global spatio-temporal waves in scalp EEG. A number of studies have shown global wave activity in scalp EEG/MEG to be task/activity dependent, including working memory activation (Sauseng et al., 2002; Alexander et al., in press), listening to auditory tones (Ribary et al., 1991), auditory discrimination (Alexander et al., 2006), resting states (Ito et al., 2007; Manjarrez et al., 2007) and sleep (Massimini et al., 2004). Global spatio-temporal waves have been found at a range of frequencies, including gamma (using MEG; Ribary et al., 1991), alpha (Alexander et al., 2006; Ito et al., 2007; Manjarrez et al., 2007), theta (Alexander et al., 2007), delta (Alexander et al., 2006; in press) and slow wave bands (Massimini et al., 2004).
4. Transcranial stimulation has been used to alter cortical activity and learning (Hallett, 2007; Floel and Cohen, 2007). In this sense, transcranial electrical stimulation is 'reverse EEG'. In an intriguing study, application of slow-wave (0.75 Hz) transcranial electrical stimulation during early slow-wave sleep was shown to improve declarative memory retention (Marshall et al., 2006). The subjects were stimulated with positive currents at fronto-lateral locations. The critical link from this finding to the EEG literature on global spatio-temporal waves is the finding by Massimini et al. (2004) that slow wave activity in the EEG during sleep takes the form of a global spatio-temporal wave. The waves during slow-wave sleep originate predominantly from pre-frontal regions.
In summary, the literature on electric field coupling of neighbouring hippocampal pyramidal cells shows that endogenous electric fields can play a causal role in brain activity. In the case of the cortex, a global spatio-temporal wave passing over a particular minicolumn in the cortex will perturb the electrical field of that minicolumn, altering the firing patterns of its constituent neurons. Global patterns measured in EEG dynamics can play a causal role in brain activity; they are not merely epiphenomenal. Future studies, measuring EEG during transcranial stimulation, should confirm this causal role for global cortical dynamics that have been measured at a range of frequencies in the EEG.
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