Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks
Introduction
Cortical activation associated with behavioral activity has long been known to involve desynchronization of low-frequency components of the resting electroencephalogram (EEG). More sensitive recordings have revealed that such activation can also involve increases in high-frequency activity in the gamma range (30–80 Hz) (Pfurtscheller and Neuper, 1992). The possible function of such gamma activity has been debated vigorously (Gray, 1994, MacKay, 1997, Pantev et al., 1994, Singer, 1994). Clear gamma oscillations in the mammalian brain were first observed in the olfactory system (Adrian, 1942), leading to extensive studies of the underlying cellular and physiological mechanisms. The olfactory bulb has been found to exhibit spatially coherent gamma range oscillation of the local field potential (LFP) whose amplitude contains odor-specific information (Bressler and Freeman, 1980, Freeman, 1991, Freeman and Skarda, 1985, Laurent et al., 1996). Studies in the visual system of monkeys have suggested that the spatial pattern of the gamma oscillations may be involved in processing behaviorally relevant information (Freeman and van Dijk, 1987, Kreiter and Singer, 1992, Livingstone, 1996). In the visual system, neuronal responses in the gamma frequency range became synchronized for sites in area 17 with similar orientation preference (Eckhorn et al., 1988, Gray et al., 1989), and could become synchronized between hemispheres and between striate and extrastriate areas (Eckhorn et al., 1988, Engel et al., 1991a, Engel et al., 1991b, Roelfsema et al., 1997). The resultant temporal synchrony has been hypothesized to function as a binding mechanism for visual features and figure-ground separation (Engel et al., 1992). In the human visual system, gamma rhythms (25–50 Hz) induced by visual and auditory stimuli were recorded via depth electrodes in the calcarine cortex (Chatrian et al., 1960, Perez-Borja et al., 1961). However, these gamma waves were rather general and non-specific responses to various types of sensory stimulation.
Gamma-range oscillations also have been observed in the sensorimotor cortex of a variety of subjects in relation to motor behaviors. Murthy and Fetz, 1992, Murthy and Fetz, 1996a, Murthy and Fetz, 1996b) found episodes of widespread 25–35 Hz oscillations in monkeys performing exploratory limb movements; unit and field potential oscillations occurred synchronously in pre- and post-central cortex and bilaterally. Sanes and Donoghue (1993) observed field potential oscillations in monkeys performing an instructed delayed response; oscillations of 15–50 Hz occurred during the delay and decreased during the movement (Donoghue et al., 1998). MacKay and Mendonça (1995) observed broad-band increases in high-frequency power in parietal LFPs of monkeys during reaching. Baker et al. (1997) found evidence of oscillations in cortex and hand muscles of monkeys during a precision grip. Jasper and Penfield (1949) recorded 25 Hz electrocorticograms (ECoG) from the hand area of the precentral cortex in human subjects and observed that oscillations were blocked by movement of the contralateral finger. In cats, gamma oscillations in the sensorimotor cortex became very apparent when the animals were attentive and immobilized (Bouyer et al., 1981, Bouyer et al., 1987, Rougeul et al., 1979). Thus, most of these observations indicate that gamma oscillations in sensorimotor cortex may relate to attention or planning of movement, but have less reliable relation to execution of movement.
Using techniques developed to record human cortical activity simultaneously from multiple sites over a wide area, several investigators have studied the spatiotemporal patterns of activity. Coherent and distributed gamma oscillatory responses to auditory stimuli have been recorded via magnetoencephalography (Pantev et al., 1991, Ribary et al., 1991, Tesche and Hari, 1993). Scalp-recorded 40 Hz responses to auditory stimuli were highest when the subject paid attention to the stimuli (Tiitinen et al., 1993). The somatic sensorimotor system shows a decrease in 10 Hz power and an increase in 40 Hz power of the EEG during finger movement (Pfurtscheller and Neuper, 1992, Pfurtscheller et al., 1993). The spatial pattern of 40 Hz power could be differentiated between finger, toe and tongue movement by the topographical display of narrow-band power (Pfurtscheller et al., 1994). However, the spatial resolution of scalp-recorded EEG in humans is relatively limited compared with the resolution obtainable by direct cortical recording in animal studies; moreover, EEG signals are usually filtered with a narrow bandpass, risking the inclusion of harmonics of lower frequency (Jurgens et al., 1995).
Electrocorticography, which uses arrays of electrodes implanted subdurally, makes it possible to record potentials directly from the cortical surface at multiple sites simultaneously. This technique was used originally to localize the epileptic focus during surgical treatment of intractable epilepsy (Luders et al., 1987). The cortical sites can be functionally identified by electrical stimulation through the same electrodes (Ojemann, 1995). Recordings using the subdural electrodes with sufficiently wide band-pass filters can detect gamma-range activity with relatively high sensitivity. A previous study of the ECoG of two patients performing a sensory discrimination task produced little evidence for selective changes in power in particular frequency bands, and no evidence of globally correlated activity in the ECoG (Menon et al., 1996). In the present study, we used multichannel ECoG recording to investigate the presence and properties of gamma activity in the forearm and adjacent sensorimotor areas during performance of various visuomotor tasks.
Section snippets
Subjects
Subjects were 6 patients with intractable epilepsy, two males and 4 females aged 12–41 years (Table 1). One subject (R.A.) exhibited diplegia (right < left) but could use both hands and fingers for fine manipulation. None of the other 5 subjects showed any motor or sensory abnormality, including visual field deficits, on standard neurological examination. The subjects gave written informed consent to participate in the study.
The epileptic focus and functional sites were mapped with the use of
Gamma oscillations during task performance
In 3 subjects, the appearance of gamma oscillations during performance of the visual motor tasks was obvious upon visual inspection of the ECoG signal. Representative ECoG records of subject B.R. during rest and performance of the tracking task are illustrated in Fig. 1 (for the relative locations of the recording sites see Fig. 6). During rest, the subject's ECoG exhibited activity in the range of 10–30 Hz, as seen at sites 1h and 2h. During performance of the target tracking task, this
Gamma activity related to visuomotor task performance
This report is the first to show increased gamma activity in broadly filtered ECoG recorded in human sensorimotor cortex, during performance of specific visuomotor tasks. Previous work has documented decreases in low-frequency power with movements. Jasper and Penfield (1949) first reported 25 Hz oscillations in the ECoG in human precentral cortex, which disappeared during contralateral finger movements. The alpha-beta rhythm in human sensorimotor areas has been studied with the use of
Acknowledgements
We thank Dr. Nancy Temkin and Mr. Heracles Panagiotides for help with statistical analysis, Mr. Jonathan Garlid for help with instrumentation, and Ms. Kate Elias for editorial help. This work was supported in part by the Human Frontiers Science Program, the Japan Foundation for Aging and Health, and grants NS12542 and RR00166 from the National Institutes of Health.
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Present address: Division of Neurophysiology, Department of Neuroscience, Karolinska Institute, 171 77 Stockholm, Sweden.