On the human sensorimotor-cortex beta rhythm: Sources and modeling
Introduction
Oscillatory activity of the human cerebral cortex, readily monitored by electroencephalographic (EEG) and magnetoencephalographic (MEG) recordings, comprises several prominent frequency bands. The best known is the ≈10 Hz parieto-occipital “alpha” rhythm that reacts strongly to opening/closing of the eyes. The rolandic mu-rhythm is observed as spontaneous activity in healthy subjects over sensorimotor areas and has a 10-Hz and 20-Hz components that have different sources in the primary somatosensory and the motor cortex, respectively, (see Hari and Salmelin, 1997 for a review). The 20-Hz rhythm is modulated during various motor and cognitive tasks (Farmer, 1998, Hari and Salmelin, 1997). Moreover, a part of the 20-Hz motor-cortex oscillations are coherent with simultaneously recorded surface electromyogram during isometric contraction (Conway et al., 1995, Salenius et al., 1997) and have been suggested to be related to re-calibration after movements (Kilner et al., 1999). Patients with progressive myoclonus epilepsy and chronic pain display abnormal reactivity of the motor-cortex beta-range activity (Juottonen et al., 2002, Silen et al., 2000), suggesting reduced intracortical inhibition.
In clinical EEG records, rhythmic beta oscillations are observed in frontal scalp electrodes in subjects who have taken benzodiazepine-type drugs (Wanquier, 1998). Interestingly, Baker and Baker (2003) reported that cortico-muscle coherence in the beta range decreased after the application of benzodiazepines. Our experimental aim was to investigate whether benzodiazepine would modify the motor-cortex 20-Hz oscillations measured by MEG in healthy subjects. Furthermore, we were interested in finding out whether we could identify the generation site(s) of the beta-range rhythms after benzodiazepine administration. Preliminary results on this subject (Jensen et al., 2002) prompted the current study.
The primary effect of benzodiazepines is an increase in the conductance of GABA-mediated currents. It is not intuitive how the resulting increase in inhibition could increase the power of a rhythm and why that increase would be in the beta band. We use suggestions from in vitro research and computational modeling to help to provide an answer. The human beta oscillations appear to have many features in common with gamma band oscillations (30–80 Hz) observed in various animal preparations. Gamma oscillations have been modeled in vitro in the hippocampus (Towers et al., 2002, Traub et al., 1996, Whittington et al., 1995, Whittington et al., 1997a). In those preparations, the fast-spiking interneurons are important for the gamma frequency oscillations. Bacci et al. (2003) and Faulkner et al. (1999) recently showed that these are the interneurons affected by benzodiazepine-like agonists. Interestingly, Shimono et al. (2000) showed that cholinergically induced beta oscillations in hippocampal rat slice increased in power and decreased in frequency by benzodiazepine.
The computational network model we offer hypothesizes that the human beta oscillations in the sensorimotor cortex are an analogue of the gamma oscillations studied in rats. Networks of inhibitory interneurons have shown to be crucially involved in generating the gamma rhythm (Towers et al., 2002, Traub et al., 1996, Whittington et al., 1995, Whittington et al., 1997a). The main motivation for hypothesizing this analogy is the sensitivity in frequency and power of these rhythms to GABAergic agonists, suggesting a strong role to be played by the interneuronal network. The frequencies of the rhythms are affected by the size and decay time of the GABA conductance and the drive to both excitatory and inhibitory neurons. We show a parameter range in which all the behavior of the power spectrum described in the experimental findings is replicated. Specifically, modeling the effects of benzodiazepine as an increase in the strength of the GABA conductance, we show that this can increase the power in the beta frequency range, lower the frequency and broaden the range in which there is large power. We show that the major effects come about from an increase in inhibitory current to the inhibitory interneurons; instead, increase in inhibitory currents to the excitatory pyramidal cells does not increase the beta power.
Section snippets
Subjects
Magnetoencephalographic (MEG) signals were recorded from eight healthy subjects (ages 26–35 years; 3 males; 5 females) with no history of neurological disorders. Informed consent was obtained from each subject after full explanation of the study. The work had a prior approval by the ethics committee of the Helsinki Uusimaa Hospital District.
Procedure
The subjects were seated in a relaxed position under the MEG helmet. They were instructed to keep their eyes closed and relax without falling asleep while 3
Experiments
Fig. 1 shows power spectra for subject S2 before (pre-BNZ) and after (post-BNZ) benzodiazepine administration, respectively. The spectra are arranged according to sensor locations on the helmet. Each spectrum is the average calculated from two orthogonal planar gradiometers at the same position. The enlarged graphs show the spectra from a set of gradiometers over the sensorimotor cortex. In the pre-BNZ condition, the rolandic mu rhythm consists of ≈10 Hz and ≈20 Hz main frequencies. In the
Discussion
Using magnetoencephalographic recordings in humans, we observed a strong increase with benzodiazepines in the power of beta oscillations in the primary sensorimotor regions of both hemispheres. The increase in power was associated with a small decrease in the beta frequency. The beta oscillations sensitive to benzodiazepine originated from the primary sensorimotor cortex, close to the hand area. Ours is the first study to demonstrate that the 20-Hz oscillations emerging after benzodiazepine
Acknowledgments
The experimental part of the study has been financially supported by the Academy of Finland, the NWO Innovative Research Incentive Schemes with financial aid from the Netherlands Organization for Scientific Research (NWO) and by the EU's Large-Scale Facility Neuro-BIRCH III hosted at the Brain Research Unit of the Low Temperature Laboratory, Helsinki University of Technology. The theoretical parts of the study have been supported by the National Institute of Heath, National Science Foundation
References (38)
- et al.
The interplay of lorazepam-induced brain oscillations: microstructural electromagnetic study
Clin. Neurophysiol.
(2004) - et al.
Human cortical oscillations: a neuromagnetic view through the skull
Trends Neurosci.
(1997) - et al.
New method to identify multiple sources of oscillatory activity from magnetoencephalographic data
NeuroImage
(2002) - et al.
Altered central sensorimotor processing in patients with complex regional pain syndrome
Pain
(2002) - et al.
Synchronous cortical oscillatory activity during motor action
Curr. Opin. Neurobiol.
(2003) - et al.
Abnormal reactivity of the approximately 20-Hz motor cortex rhythm in Unverricht Lundborg type progressive myoclonus epilepsy
NeuroImage
(2000) - et al.
Visualization of magnetoencephalographic data using minimum current estimates
NeuroImage
(1999) - et al.
Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses
J. Neurosci.
(2003) - et al.
The effect of diazepam on motor cortical oscillations and corticomuscular coherence studied in man
J. Physiol.
(2003) - et al.
Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation
J. Physiol.
(1997)
Synchronization in networks of excitatory and inhibitory neurons with sparse, random connectivity
Neural Comput.
Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man
J. Physiol.
Fine structure of neural spiking and synchronization in the presence of conduction delays
Proc. Natl. Acad. Sci. U. S. A.
Rhythmicity, synchronization and binding in human and primate motor systems
J. Physiol.
Anaesthetic/amnesic agents disrupt beta frequency oscillations associated with potentiation of excitatory synaptic potentials in the rat hippocampal slice
Br. J. Pharmacol.
Magnetoencephalography—theory, instrumentation, and applications to noninvasive studies of the working human brain
Rev. Mod. Phys.
Rhythmical corticomotor communication
NeuroReport
Rhythm generation in monkey motor cortex explored using pyramidal tract stimulation
J. Physiol.
On the physiological basis of the 15–30 Hz motor-cortex rhythm
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