Elsevier

NeuroImage

Volume 55, Issue 3, 1 April 2011, Pages 1159-1168
NeuroImage

Distinct oscillatory STN-cortical loops revealed by simultaneous MEG and local field potential recordings in patients with Parkinson's disease

https://doi.org/10.1016/j.neuroimage.2010.11.063Get rights and content

Abstract

Neuronal oscillations are assumed to play a pivotal role in the pathophysiology of Parkinson's disease (PD). Neurons in the subthalamic nucleus (STN) generate oscillations which are coupled to rhythmic population activity both in other basal ganglia nuclei and cortical areas.

In order to localize these cortical areas, we recorded local field potentials (LFPs) and magnetoencephalography (MEG) simultaneously in PD patients undergoing surgery for deep brain stimulation (DBS). Patients were withdrawn from antiparkinsonian medication and recorded at rest. We scanned the entire brain for oscillations coherent with LFPs recorded from the STN with a frequency domain beamformer.

Coherent activity in the low (12–20 Hz) and high (20–35 Hz) beta range was found in the ipsilateral sensorimotor and the premotor cortex. Coherence in the alpha range (7–12 Hz) was observed at various locations in the ipsilateral temporal lobe. In a subset of subjects, the superior temporal gyrus consistently showed coherent alpha oscillations.

Our findings provide new insights into patterns of frequency-specific functional connectivity between basal ganglia and cortex and suggest that simultaneous inter-regional interactions may be segregated in the frequency domain. Furthermore, they demonstrate that simultaneous MEG-LFP recordings are a powerful tool to study interactions between brain areas in PD patients undergoing surgery for DBS.

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

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