Intracranial Recordings Reveal Human Alpha Rhythm Propagation and Generation
Key findings
- The question of which brain structures generate alpha rhythm is still hotly debated, and researchers at Massachusetts General Hospital have collected the first direct evidence by making intracranial recordings in epilepsy patients undergoing surgery
- Alpha oscillations were observed to propagate as traveling waves from anterosuperior to the posteroinferior cortex
- Simultaneous recordings from cortex and pulvinar nucleus provided multiple measures suggesting that cortical activity, not thalamic activity, drives alpha rhythm
- In the somatosensory cortex, alpha currents were strongest in the supragranular layers; thus, the direction of propagation was again higher- to lower-order cortex
- Alpha rhythm appears to contribute to feedback processing within and across brain regions and structures
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Alpha oscillations are the most prominent electroencephalogram signal during wakefulness and are thought to be key to cognition. The alpha rhythm has been studied for decades, but there's still intense debate among neuroscientists about which brain structures generate it. There are two key hypotheses:
- The thalamus is the primary alpha "pacemaker"; alpha rhythm is driven by the pulvinar (a thalamic nucleus that projects to posterior cortical regions) and/or the lateral geniculate nucleus
- Within the cortex, alpha rhythm originates from infragranular layers, driven by pyramidal cells in layer V
Neither of these hypotheses had been tested directly in humans until Sydney S. Cash, MD, PhD, associate in the Department of Neurology at Massachusetts General Hospital, and colleagues made intracranial recordings in patients undergoing surgery for refractory epilepsy. Their report, published in the Proceedings of the National Academy of Sciences, provides insight into how the alpha rhythm coordinates activity throughout the brain.
Spatial Progression of Alpha Oscillations
In the first part of the study, the research team made electrocorticographic recordings of spontaneous alpha oscillations in the occipital, posterior temporal and posterior parietal cortices of five patients during quiet wakefulness.
In all patients, alpha oscillations were propagated as traveling waves from anterosuperior cortex toward posteroinferior areas. Electrocorticographic recordings in a healthy macaque during an eye closure task demonstrated a highly similar propagation direction and speed.
Role of the Thalamus
In a separate cohort of nine patients, intracranial electroencephalography was used to make simultaneous recordings from the cortex and the pulvinar.
Multiple analyses showed that cortical activity, not thalamic activity, drove alpha oscillations. This disputes the hypothesis about a thalamic pacemaker.
Localization in the Cortex
To determine which cortical layers generate the alpha rhythm, the researchers placed laminar microelectrodes in the somatosensory cortex of three additional patients. In all regions and in all patients, alpha currents were strongest within supragranular cortical layers.
Interestingly, the direction of propagation was posterior to anterior. This finding might appear to conflict with the results in the posterior cortex (where alpha oscillations were propagated anterior to posterior). However, higher-order somatosensory areas are posterior to primary somatosensory cortex, so in both sets of experiments, alpha propagated from higher- to lower-order cortex.
Both the laminar microelectrode recordings and the electrocorticographic recordings suggested that layer II/III pyramidal cells are the primary alpha generators within the cortex during quiet wakefulness.
Summary
The alpha rhythm appears to contribute to feedback processing within and across brain regions and structures. It probably reflects short-range supragranular feedback that propagates from higher- to lower-order cortex and cortex to the thalamus.
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