Neural correlates of regional EEG power change
Introduction
The electroencephalogram (EEG) represents the summed postsynaptic potentials of cortical neurons (Niedermeyer and Lopes da Silva, 1987). The generator mechanisms of EEG rhythm in various frequency bands, however, are not well understood.
In normal subjects, the EEG rhythm at 8–12 Hz is usually most conspicuous over the parieto-occipital area (Berger, 1929, Pfurtscheller and Lopes da Silva, 1999) and is called the occipital alpha band rhythm. The EEG alpha band rhythm may be associated with the alert and yet relaxed state and is commonly used as an indirect measure of the functional organization of brain. It is well known that normal awake alpha band rhythms are ‘blocked’ (substantially reduced in amplitude) by eye opening and moderate to difficult mental tasks (Berger, 1930, Berger, 1932, Nunez et al., 2001, Vijn et al., 1991). Thus, some authors suggested that the occipital alpha band rhythm might be considered as an idling rhythm of visual areas (Kuhlman, 1978).
One of the most relevant activities overlapping the occipital alpha band rhythm is the so-called mu rhythm which is restricted over the hand area of the primary sensorimotor cortex (SM1) and is suppressed not by eye opening but by active hand movements. The sensorimotor mu rhythm could also be considered as an idling rhythm of sensorimotor areas (Kuhlman, 1978, Pfurtscheller, 1992). Although the role of the thalamocortical circuitry in the generation of sleep spindles has been emphasized (Steriade et al., 1990), the neurophysiological mechanisms by which the regional alpha band rhythm such as the occipital alpha or the sensorimotor mu rhythm are to be generated or suppressed are still unclear.
Higher frequency EEG waves such as the beta band rhythm (13–30 Hz) are associated with the cortical activation most pronounced during the awake state and rapid eye movement sleep (Nofzinger et al., 2000). During various motor tasks, EEG studies showed a transient decrease of EEG power in the beta band (Pfurtscheller, 1989), which is called event-related desynchronization (ERD) (Pfurtscheller, 1977, Pfurtscheller and Aranibar, 1977) or task-related power decrease (Gerloff et al., 1998). This decrease starts 1–2 s prior to the movement onset and is followed by a rebound-like increase just after termination of the movement (event-related synchronization: ERS) (Pfurtscheller, 1992). It is speculated that the motor cortex shifts from an activated state during preparation and execution of movement (working cortex) to a resting state after termination of movement or, in other words, from a processing mode to an ‘idling’ mode (Pfurtscheller et al., 1996). This hypothesis is also supported by a transcranial magnetic stimulation study showing decreased corticospinal excitability at the time of the 20-Hz event-related synchronization (Chen et al., 1998). However, the generator mechanism of regional beta band rhythm is still unknown.
Brain electrical activity represents the single greatest demand on cerebral metabolism (Erecinska and Silver, 1989), suggesting that measurement of electrical energy also should be coupled to cerebral metabolism and perfusion. In normal subjects, cerebral glucose uptake and blood flow are generally accepted as tightly coupled measures of cerebral energy utilization (Sokoloff, 1977, Sokoloff, 1981). The association between EEG power and cerebral glucose metabolism has been occasionally studied using the 18-fluoro-deoxyglucose positron emission tomography (PET) technique (Larson et al., 1998, Oakes et al., 2004, Schreckenberger et al., 2004). However, a limitation of the 18-fluoro-deoxyglucose tracer is that over the span of 30 min it is difficult to ensure that the subject remains in the same functional state (Oakes et al., 2004). Regional cerebral blood flow (rCBF) has been used as an indirect measure of functional neural activity (Raichle, 1987) and the PET technique is considered to be the ‘gold standard’ in CBF measurements in humans (Feng et al., 2004). Measurement of rCBF using H215O PET has been well established based on the single-tissue compartment model for diffusible tracers in at least physiologically normal brain tissue (Sadato et al., 1998). The H215O tracer has shorter time frame (10–30 s) than the 18-fluoro-deoxyglucose tracer (20–30 min) and the results of H215O PET examinations directly depend on the acute cerebral state of activation during tracer injection (Schreckenberger et al., 2004). In normal subjects, cerebral blood flow is generally accepted as tightly coupled measures of cerebral energy utilization (Sokoloff, 1977, Sokoloff, 1981). It was reported that EEG power showed strong associations with rCBF in most frequency bands including the alpha and beta range (Leuchter et al., 1999). Therefore, taken together with the EEG power change described above, it is predicted that rCBF associated with the neuronal activation might covary with the EEG power in at least normal subjects. Although previous reports (Ingvar et al., 1976, Paulson and Sharbrough, 1974) mentioned the relationship between EEG and rCBF in humans, the record of EEG and rCBF could not be done simultaneously due to limitations in the EEG and rCBF technique. Recently, the association between EEG power and rCBF recorded simultaneously has been occasionally studied using the H215O technique (Leuchter et al., 1999, Nakamura et al., 1999, Sadato et al., 1998). However, the previous reports investigated a correlation between rCBF and the EEG rhythm averaged across the whole scalp. The averaged EEG rhythm might be inappropriate to investigate regional EEG power change such as sensorimotor mu rhythm because the occipital alpha band rhythm may diminish an effect of sensorimotor mu rhythm in the averaged alpha power. Therefore, it would be preferable to investigate the relationship between rCBF change induced by several tasks and the regional EEG rhythm to clarify neurophysiological mechanisms in the generation or suppression of the regional EEG power. To achieve this goal, we employed rather simple tasks that are commonly used in clinical EEG recording.
The purpose of the present study is to quantitatively evaluate the correlation between rCBF changes using H215O PET and EEG power changes induced by several motor tasks and clarify what brain regions are involved in the generation and suppression of the regional EEG rhythms.
Section snippets
Subjects
Eight right-handed healthy volunteers (5 males and 3 females; mean age ± SD, 42 ± 10 years) participated in the experiment. The protocol was approved by the NINDS Institutional Review Board and the NIH Radiation Safety Committee. All subjects gave their written informed consent for the study and had no medical history of neurological or psychiatric disorders.
Tasks
The subjects lay in a supine position and the following tasks were performed twice for each (total 10 times):
- 1.
rest condition with eyes closed
Results
The mean movement frequencies during the tasks (task 3, 4 and 5) were 1.3 ± 0.3 Hz in RH, 1.2 ± 0.2 Hz in LH and 1.3 ± 0.3 Hz in RF (no significant differences). The mean EEG alpha frequencies were 9.8 ± 0.9 Hz in the occipital area, 10.8 ± 2.1 Hz in the left sensorimotor area and 11.0 ± 1.5 Hz in the right sensorimotor area (no significant differences). The logarithmic regional EEG band power is shown in Fig. 2.
Discussion
This is the first report of quantitative evaluation of the correlation between rCBF changes and regional EEG powers. Significant negative correlations between the occipital EEG power within the alpha and lower beta bands and the occipital rCBF were observed. There were also significant negative correlations between the left and right sensorimotor EEG power within the alpha and beta ranges and the ipsilateral sensorimotor rCBF, respectively. These findings suggest that decrease in the regional
Acknowledgments
This study is partly supported by the Grants-in-Aid for Scientific Research on Priority Areas (Integrative Brain Research) for T.M. (18019020) and (System study on higher-order brain functions) for H.F. (18020014) from the MEXT of Japan, Grant-in-Aid for Scientific Research (C) 18500239 for T.M. from Japan Society for the Promotion of Science.
We would like to thank Dr. Hiroshi Shibasaki for useful comments.
References (96)
- et al.
Human anterior and frontal midline theta and lower alpha reflect emotionally positive state and internalized attention: high-resolution EEG investigation of meditation
Neurosci. Lett.
(2001) - et al.
Functional significance of the mu rhythm of human cortex: an electrophysiologic study with subdural electrodes
Electroencephalogr. Clin. Neurophysiol.
(1993) - et al.
Brain perfusion in Alzheimer's disease with and without apathy: a SPECT study with statistical parametric mapping analysis
Psychiatry Res.
(2002) - et al.
Fast fronto-parietal rhythms during combined focused attentive behaviour and immobility in cat: cortical and thalamic localizations
Electroencephalogr. Clin. Neurophysiol.
(1981) - et al.
Alpha EEG coherence in different brain states: an electrophysiological index of the arousal level in human subjects
Neurosci. Lett.
(1999) - et al.
State-modulation of cortico-cortical connections underlying normal EEG alpha variants
Physiol. Behav.
(2000) - et al.
Human alpha oscillations in wakefulness, drowsiness period, and REM sleep: different electroencephalographic phenomena within the alpha band
Neurophysiol. Clin.
(2002) - et al.
Comparison of subcortical, cortical and scalp activity using chronically indwelling electrodes in man
Electroencephalogr. Clin. Neurophysiol.
(1965) - et al.
Motor areas in the frontal lobe of the primate
Physiol. Behav.
(2002) - et al.
CBF changes during brain activation: fMRI vs. PET
NeuroImage
(2004)
A framework for the analysis of mixed time series/point process data—theory and application to the study of physiological tremor, single motor unit discharges and electromyograms
Prog. Biophys. Mol. Biol.
Human cortical oscillations: a neuromagnetic view through the skull
Trends Neurosci.
Correlation between dominant EEG frequency, cerebral oxygen uptake and blood flow
Electroencephalogr. Clin. Neurophysiol.
Memory processes, brain oscillations and EEG synchronization
Int. J. Psychophysiol.
EEG-alpha rhythms and memory processes
Int. J. Psychophysiol.
EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis
Brain Res. Brain Res. Rev.
Rhythmic electrical activity from isolated cerebral cortex
Electroencephalogr. Clin. Neurophysiol.
Functional topography of the human mu rhythm
Electroencephalogr. Clin. Neurophysiol.
Relationship between brain electrical activity and cortical perfusion in normal subjects
Psychiatry Res.
Neural mechanisms underlying brain waves: from neural membranes to networks
Electroencephalogr. Clin. Neurophysiol.
Relative contributions of intracortical and thalamo-cortical processes in the generation of alpha rhythms, revealed by partial coherence analysis
Electroencephalogr. Clin. Neurophysiol.
Electroencephalographic analysis of cortico-muscular coherence: reference effect, volume conduction and generator mechanism
Clin. Neurophysiol.
Functional coupling of human right and left cortical motor areas demonstrated with partial coherence analysis
Neurosci. Lett.
Movement-related slow cortical magnetic fields and changes of spontaneous MEG- and EEG-brain rhythms
Electroencephalogr. Clin. Neurophysiol.
Analysis of music–brain interaction with simultaneous measurement of regional cerebral blood flow and electroencephalogram beta rhythm in human subjects
Neurosci. Lett.
Event-related dynamics of cortical rhythms: frequency-specific features and functional correlates
Int. J. Psychophysiol.
Towards a neurobiology of dysfunctional arousal in depression: the relationship between beta EEG power and regional cerebral glucose metabolism during NREM sleep
Psychiatry Res.
EEG coherency. I: statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales
Electroencephalogr. Clin. Neurophysiol.
Electrocorticogram–electromyogram coherence during isometric contraction of hand muscle in human
Clin. Neurophysiol.
Graphical display and statistical evaluation of event-related desynchronization (ERD)
Electroencephalogr. Clin. Neurophysiol.
Central beta rhythm during sensorimotor activities in man
Electroencephalogr. Clin. Neurophysiol.
Event-related synchronization (ERS): an electrophysiological correlate of cortical areas at rest
Electroencephalogr. Clin. Neurophysiol.
Event-related cortical desynchronization detected by power measurements of scalp EEG
Electroencephalogr. Clin. Neurophysiol.
Patterns of cortical activation during planning of voluntary movement
Electroencephalogr. Clin. Neurophysiol.
Event-related EEG/MEG synchronization and desynchronization: basic principles
Clin. Neurophysiol.
Post-movement beta synchronization. A correlate of an idling motor area?
Electroencephalogr. Clin. Neurophysiol.
Functional dissociation of lower and upper frequency mu rhythms in relation to voluntary limb movement
Clin. Neurophysiol.
The functional significance of mu rhythms: translating “seeing” and “hearing” into “doing”
Brain Res. Brain Res. Rev.
The functions of the orbitofrontal cortex
Brain Cogn.
Fast somato-parietal rhythms during combined focal attention and immobility in baboon and squirrel monkey
Electroencephalogr. Clin. Neurophysiol.
Rhythms in the alpha band in cats and their behavioural correlates
Int. J. Psychophysiol.
Human cortical 40 Hz rhythm is closely related to EMG rhythmicity
Neurosci. Lett.
Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement
Neuroscience
Functional segregation of movement-related rhythmic activity in the human brain
NeuroImage
Studies on integrative functions of the human frontal association cortex with MEG
Brain Res. Cogn. Brain Res.
The thalamus as the generator and modulator of EEG alpha rhythm: a combined PET/EEG study with lorazepam challenge in humans
NeuroImage
Spatial structure of the human alpha rhythm: global correlation in adults and local correlation in children
Clin. Neurophysiol.
Craniocerebral topography within the international 10–20 system
Electroencephalogr. Clin. Neurophysiol.
Cited by (31)
Pathophysiology of unilateral asterixis due to thalamic lesion
2012, Clinical NeurophysiologyCitation Excerpt :These findings suggest that the thalamic asterixis in the present cases is mediated by the corresponding part of the sensorimotor cortex, but its underlying pathophysiology is different from that of epileptic negative myoclonus. The power increase in alpha or beta bands time-locked to an event, event-related synchronisation (ERS), is considered to be associated with decreased activation of the corresponding cortical area or return to the resting state from the activated condition while the power decrease, event-related desynchronisation (ERD), represents increased activation of the cortical area (Pfurtscheller and Aranibar, 1977; Pfurtscheller et al., 2003; Pfurtscheller, 2006; Oishi et al., 2007). Therefore, the present findings suggest that the sensorimotor cortex is in an excessive inhibition associated with each lapse of sustained hand posture.
Region and frequency specific changes of spectral power in Alzheimer's disease and mild cognitive impairment
2011, Clinical NeurophysiologyCitation Excerpt :Spectral power differences in the delta band were less prominent. Slowing of rhythms has been replicated in previous studies on AD patients (Babiloni et al., 2006a,b,c,e, 2004, 2007; Brunovsky et al., 2003; Jelic et al., 2000, 1997; Jeong, 2004; Oishi et al., 2007; Pucci et al., 1998; Rossini et al., 2006; van der Hiele et al., 2007b). The earliest changes in patients with AD are an increase in theta power and a decrease in beta power, followed by a decrease in alpha power.
Differences in quantitative EEG between frontotemporal dementia and Alzheimer's disease as revealed by LORETA
2011, Clinical NeurophysiologyCitation Excerpt :Other studies that also show decreased function in parietal regions for AD patients compared to FTD are reported (Varrone et al., 2002; Foster et al., 2007). In particular, with respect to the observed increase in beta generators for the FTD patients in sensorimotor areas, this result corresponds to a concomitant decrease in regional cerebral blood flow that has been observed by Oishi et al. (2007) in the sensorimotor areas. They found significant negative correlation between sensorimotor EEG rhythm in the 10–20 Hz range with sensorimotor rCBF.
Neural mirroring systems: Exploring the EEG mu rhythm in human infancy
2011, Developmental Cognitive NeuroscienceCitation Excerpt :It is relevant that historical accounts of the mu rhythm have long noted its relation with somatosensory activation (Chatrian et al., 1959; Kuhlman, 1978). Links between the mu rhythm and the somatosensory system have been further strengthened by recent studies from adults which have used concurrent EEG/fMRI recording or MEG localization methods to show that the EEG mu rhythm reflects activity in (and likely originates in) primary somatosensory cortex (Formaggio et al., 2008; Hari and Salmelin, 1997; Oishi et al., 2007; Ritter et al., 2009; Yuan et al., 2010). Future work should be directed towards exploring the connections between the mu rhythm, motor system activity, and somatosensory processing.
The effect of pre- vs. post-reward attainment on EEG asymmetry in melancholic depression
2011, International Journal of Psychophysiology