Distinct oscillatory STN-cortical loops revealed by simultaneous MEG and local field potential recordings in patients with Parkinson's disease
Research highlights
► Beta oscillations in the STN are coherent with beta oscillations in the ipsilateral sensorimotor and premotor cortex (precentral gyrus, postcentral gyrus, medial frontal gyrus). ► Alpha oscillations in the STN are coherent with oscillations in the ipsilateral temporal cortex. ► The distribution of motor cortex–STN coherence across DBS electrode contacts is focal. ► The distribution of superior temporal gyrus–STN coherence across DBS electrode contacts is homogenous.
Introduction
Recordings from the basal ganglia of patients with Parkinson's disease (PD) undergoing surgery for deep brain stimulation (DBS) revealed strong oscillatory power in the alpha (7–12 Hz) and beta (12–35 Hz) band (Brown et al., 2001, Kühn et al., 2004, Levy et al., 2002, Priori et al., 2004). Furthermore, basal ganglia oscillations were found to be coupled to oscillations in distant brain regions. By simultaneously recording electroencephalography (EEG) and local field potentials (LFPs) it was shown that oscillations recorded from the STN are coherent with oscillations in cortical areas (Cassidy et al., 2002, Fogelson et al., 2006, Lalo et al., 2008, Marsden et al., 2001, Williams et al., 2002). Much like beta power in the STN, coherence in the range from 10 to 30 Hz was found to be attenuated by movement (Cassidy et al., 2002, Lalo et al., 2008), the administration of levodopa (Lalo et al., 2008, Williams et al., 2002) and DBS (Kühn et al., 2008).
Although these findings suggest that abnormal coupling between STN and cortical oscillations may be pathophysiologically relevant, the cortical areas engaged in this coupling have not been identified so far. Simultaneous EEG-LFP recordings provided first evidence that the distribution of coherence across cortical areas is heterogeneous and frequency-dependent (Fogelson et al., 2006, Williams et al., 2002). However, the exact topography of STN-cortical coherence remains to be determined.
In this study we utilized simultaneous magnetoencephalography (MEG)-LFP recordings to map STN-cortical coherence. In contrast to EEG, MEG allows for whole-head, post-surgical measurements and thus for source localization with high spatial resolution. Using a frequency domain beamformer (Gross et al., 2001), we localized STN-cortical coherence in eight PD patients. While the feasibility of this approach has recently been demonstrated with data from a single subject (Litvak et al., 2010), it has not been realized in a group of patients so far.
Section snippets
Patients
Nine patients (three females) with idiopathic, akinetic-rigid PD (mean age: 64 ± 7.6 years, range: 47–75), who were clinically selected for DBS of the STN, participated in the study. One patient was excluded due to severe head movement artifacts. All patients gave written informed consent. Table 1 summarizes the clinical details.
The study was approved by the local ethics committee (study no. 3209) and is in accordance with the Declaration of Helsinki. High resolution T1-weighted magnetic resonance
Sensor level analysis
We observed significant coherence between LFPs and MEG sensors in the alpha, low beta and high beta band in all subjects (see Fig. S2 in the supplementary material). Coherence lateralized to the ipsilateral side with respect to the STN. On average, sensors ipsilateral to the STN showed higher coherence than contralateral sensors (Fig. 3). As in the example shown in Fig. 4, coherence was usually strongest in sensors located above the paramedian central sulcus region.
Except for a single patient
Discussion
This study shows that the ipsilateral sensorimotor and adjacent premotor cortex is the main source of cortical activity coherent with beta oscillations in the STN of PD patients. Moreover, it identified ipsilateral temporal areas as a source of coherent alpha activity.
Conclusions
By recording MEG and LFPs simultaneously we were able to precisely map frequency-dependent interactions between STN and cortex for the first time. Our study showed that STN-cortical coherence is focal in the spatial and in the frequency domain and revealed two distinct couplings between STN and cortex: One with the motor cortex in the beta frequency band and one with temporal areas in the alpha frequency band. Moreover, it further established simultaneous MEG and intracranial electrode
Acknowledgments
The authors would like to express their sincere gratefulness to the patients who participated in this study. Furthermore, we are very thankful to the people of Medtronic Neuromodulation (Dr. Ali Sarem-Aslani, Mr. Paul van Venrooij, and Mr. Andreas Rolf) for technical support. In addition, we thank Mrs. E. Rädisch for assistance with MRI scans, Prof. Joachim Gross (CCNi Glasgow) for help in analysis issues and the people behind the fieldtrip project for excellent support. This study was
References (59)
- et al.
Functional architecture of basal ganglia circuits: neural substrates of parallel processing
Trends Neurosci.
(1990) - et al.
An extended difference of coherence test for comparing and combining several independent coherence estimates: theory and application to the study of motor units and physiological tremor
J. Neurosci. Meth.
(1997) - et al.
Sensory and cognitive functions of the basal ganglia
Curr. Opin. Neurobiol.
(1997) - et al.
Role of left posterior superior temporal gyrus in phonological processing for speech perception and production
Cogn. Sci.
(2001) - et al.
The mystery of motor asymmetry in Parkinson's disease
Lancet Neurol.
(2006) - et al.
Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging
Neuroimage
(2002) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence
Trends Cogn. Sci. (Regul. Ed.)
(2005)- et al.
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.
(1995) - et al.
A direct demonstration of functional specialization within motion-related visual and auditory cortex of the human brain
Curr. Biol.
(1996) - et al.
The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson's disease
Exp. Neurol.
(2005)
Optimized beamforming for simultaneous MEG and intracranial local field potential recordings in deep brain stimulation patients
Neuroimage
Nonparametric statistical testing of coherence differences
J. Neurosci. Meth.
Somatotopically arranged inputs from putamen and subthalamic nucleus to primary motor cortex
Neurosci. Res.
Total information extracted from MEG measurements
Int. Congr. Ser.
Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease
Exp. Neurol.
Time dependent subthalamic local field potential changes after DBS surgery in Parkinson's disease
Exp. Neurol.
Imaging the human motor system's beta-band synchronization during isometric contraction
Neuroimage
EEG and MEG coherence: measures of functional connectivity at distinct spatial scales of neocortical dynamics
J. Neurosci. Meth.
Frequency-dependent distribution of local field potential activity within the subthalamic nucleus in Parkinson's disease
Exp. Neurol.
Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections
Brain Res.
Sampling theory for neuromagnetic detector arrays
Biomed. Eng. IEEE Trans.
Effects of DBS on auditory and somatosensory processing in Parkinson's disease
Hum. Brain Mapp.
Parallel organization of functionally segregated circuits linking basal ganglia and cortex
Annu. Rev. Neurosci.
Time series: data analysis and theory (SIAM)
Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease
J. Neurosci
Movement-related changes in synchronization in the human basal ganglia
Brain
Different functional loops between cerebral cortex and the subthalmic area in Parkinson's disease
Cereb. Cortex
Focal increase of blood flow in the cerebral cortex of man during vestibular stimulation
Brain
Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results
Mov. Disord.
Cited by (182)
Cortical brain signals improve decoding of movement and tremor for clinical brain computer interfaces
2024, Clinical NeurophysiologyAdverse and compensatory neurophysiological slowing in Parkinson's disease
2023, Progress in NeurobiologyNeuronal oscillations predict deep brain stimulation outcome in Parkinson's disease
2022, Brain Stimulation