Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band

Abstract

It has been shown in animals that neuronal activity in the 'gamma band' (>30 Hz) is associated with cortical activation and may play a role in multi-regional and multi-modal integration of cortical processing. Studies of gamma activity in human scalp EEG have typically focused on event-related synchronization (ERS) in the 40 Hz band. To assess further the gamma band ERS further, as an index of cortical activation and as a tool for human functional brain mapping, we recorded subdural electrocorticographic (ECoG) signals in five clinical subjects while they performed visual-motor decision tasks designed to activate the representations of different body parts in sensorimotor cortex. ECoG spectral analysis utilized a mixed-effects analysis of variance model in which within-trial temporal dependencies were accounted for. Taking an exploratory approach, we studied gamma ERS in 10-Hz-wide bands (overlapping by 5 Hz) ranging from 30 to 100 Hz, and compared these findings with changes in the alpha (8-13 Hz) and beta (15-25 Hz) bands. Gamma ERS (observed in three out of subjects) occurred in two broad bands-'low gamma' included the 35-45 and 40-50 Hz bands, and 'high gamma' the 75-85, 80-90, 85-95 and 90-100 Hz bands. The temporal and spatial characteristics of low and high gamma ERS were distinct, suggesting relatively independent neurophysiological mechanisms. Low gamma ERS often began after onset of the motor response and was sustained through much of it, in parallel with event-related desynchronization (ERD) in the alpha band. High gamma ERS often began during, or slightly before, the motor response and was transient, ending well before completion of the motor response. These temporal differences in low and high gamma suggest different functional associations with motor performance. Compared with alpha and beta ERD, the topographical patterns of low and high gamma ERS were more discrete and somatotopically specific and only occurred over contralateral sensorimotor cortex during unilateral limb movements (alpha and beta ERD were also observed ipsilaterally). Maps of sensorimotor function inferred from gamma ERS were consistent with maps generated by cortical electrical stimulation for clinical purposes. In addition, different task conditions in one subject produced consistent differences in both motor response latencies and onset latency of gamma ERS, particularly high gamma ERS. Compared with alpha and beta ERD, the topography of gamma ERS is more consistent with traditional maps of sensorimotor functional anatomy. In addition, gamma ERS may provide complementary information about cortical neurophysiology that is useful for mapping brain function in humans.

Neurophysiologic correlates of fMRI in human motor cortex

“…Increases in HFB change were focused on primary sensorimotor electrodes during movement (Figs. 1, 2, and 5), consistent with previous studies [Crone et al, 1998a;Leuthardt et al, 2007;Miller et al, 2007;Miller et al, 2009b]. This high frequency spectral power change has been shown to correlate directly with firing rate [Manning et al, 2009;Miller et al, 2009a;Whittingstall and Logothetis, 2009], and has been demonstrated to reflect broadspectral change across all frequencies Miller et al, 2009b].…”

“…They have shown that broadband power increases, revealed at high frequencies, are typically local, on areas primarily involved in the task [Crone et al, 1998a;Miller et al, 2009b], and these high frequency changes correspond well to sites found with electrocortical stimulation of language and motor regions Sinai et al, 2005]. Power decreases in low frequency sensorimotor rhythms are distributed over larger areas of cortex [Crone et al, 1998b;Miller et al, 2007].…”

Young patients with focal seizures may have the primary motor area for the hand in the postcentral gyrus

“…The observations in the present study using electrical stimulation are consistent with those reported in previous studies using fMRI (Yousry et al, 1997), MEG (Kristeva et al, 1991) and intracranial EEG (Crone et al, 1998). Previous neuroimaging studies using fMRI and [15O]-water PET demonstrated that motor tasks such as finger tapping or hand grasping consistently activated the contralateral post-central gyrus defined by anatomical landmarks, in addition to the precentral, premotor and supplementary motor areas (Yousry et al, 1997).…”

“…Similarly, previous studies using MEG coregistered to MRI demonstrated that a large-amplitude motor task-evoked magnetic field was localized to the contralateral postcentral gyrus in healthy volunteers (Kristeva et al, 1991). A previous study of adults with focal epilepsy using intracranial EEG recording and each individual's brain surface image demonstrated that gamma-band EEG power was increased in both pre-and postcentral gyri about 200−500 ms after the onset of contralateral fist-clenching (Crone et al, 1998).…”

High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex

“…In humans, high gamma power ECoG responses following movements of different body parts were found to occur in a more discrete topographical pattern than the beta ERD phenomena. Furthermore, somatotopically defined regions on the basis of high gamma oscillations in the sensorimotor cortex were consistent with maps generated by cortical electrical stimulation (Crone et al, 1998b). Furthermore, another study on 4 epileptic patients performing a face detection task showed a good spatial colocalization between the increase of high gamma band SEEG activity and the results from the fMRI literature using different but comparable tasks (Lachaux et al, in press).…”