Local field potential activity dynamics in response to deep brain stimulation of the subthalamic nucleus in Parkinson's disease
Local field potentials (LFPs) may afford insight into the mechanisms of action of deep brain stimulation (DBS) and potential feedback signals for adaptive DBS. In Parkinson's disease (PD) DBS of the subthalamic nucleus (STN) suppresses spontaneous activity in the beta band and drives evoked res...
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Published in: | Neurobiology of disease Vol. 143; p. 105019 |
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Abstract | Local field potentials (LFPs) may afford insight into the mechanisms of action of deep brain stimulation (DBS) and potential feedback signals for adaptive DBS. In Parkinson's disease (PD) DBS of the subthalamic nucleus (STN) suppresses spontaneous activity in the beta band and drives evoked resonant neural activity (ERNA). Here, we investigate how STN LFP activities change over time following the onset and offset of DBS. To this end we recorded LFPs from the STN in 14 PD patients during long (mean: 181.2 s) and short (14.2 s) blocks of continuous stimulation at 130 Hz. LFP activities were evaluated in the temporal and spectral domains. During long stimulation blocks, the frequency and amplitude of the ERNA decreased before reaching a steady state after ~70 s. Maximal ERNA amplitudes diminished over repeated stimulation blocks. Upon DBS cessation, the ERNA was revealed as an under-damped oscillation, and was more marked and lasted longer after short duration stimulation blocks. In contrast, activity in the beta band suppressed within 0.5 s of continuous DBS onset and drifted less over time. Spontaneous activity was also suppressed in the low gamma band, suggesting that the effects of high frequency stimulation on spontaneous oscillations may not be selective for pathological beta activity. High frequency oscillations were present in only six STN recordings before stimulation onset and their frequency was depressed by stimulation. The different dynamics of the ERNA and beta activity with stimulation imply different DBS mechanisms and may impact how these activities may be used in adaptive feedback.
•ERNA frequency and amplitude reach a steady state after ~70 s stimulation.•Beta activity is suppressed within 0.5 s by stimulation and then remains stable.•Different response dynamics provide different insights into stimulation effects.•Different response dynamics may impact how signals may be used in adaptive DBS. |
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AbstractList | Local field potentials (LFPs) may afford insight into the mechanisms of action of deep brain stimulation (DBS) and potential feedback signals for adaptive DBS. In Parkinson's disease (PD) DBS of the subthalamic nucleus (STN) suppresses spontaneous activity in the beta band and drives evoked resonant neural activity (ERNA). Here, we investigate how STN LFP activities change over time following the onset and offset of DBS. To this end we recorded LFPs from the STN in 14 PD patients during long (mean: 181.2 s) and short (14.2 s) blocks of continuous stimulation at 130 Hz. LFP activities were evaluated in the temporal and spectral domains. During long stimulation blocks, the frequency and amplitude of the ERNA decreased before reaching a steady state after ~70 s. Maximal ERNA amplitudes diminished over repeated stimulation blocks. Upon DBS cessation, the ERNA was revealed as an under-damped oscillation, and was more marked and lasted longer after short duration stimulation blocks. In contrast, activity in the beta band suppressed within 0.5 s of continuous DBS onset and drifted less over time. Spontaneous activity was also suppressed in the low gamma band, suggesting that the effects of high frequency stimulation on spontaneous oscillations may not be selective for pathological beta activity. High frequency oscillations were present in only six STN recordings before stimulation onset and their frequency was depressed by stimulation. The different dynamics of the ERNA and beta activity with stimulation imply different DBS mechanisms and may impact how these activities may be used in adaptive feedback.
•ERNA frequency and amplitude reach a steady state after ~70 s stimulation.•Beta activity is suppressed within 0.5 s by stimulation and then remains stable.•Different response dynamics provide different insights into stimulation effects.•Different response dynamics may impact how signals may be used in adaptive DBS. Local field potentials (LFPs) may afford insight into the mechanisms of action of deep brain stimulation (DBS) and potential feedback signals for adaptive DBS. In Parkinson's disease (PD) DBS of the subthalamic nucleus (STN) suppresses spontaneous activity in the beta band and drives evoked resonant neural activity (ERNA). Here, we investigate how STN LFP activities change over time following the onset and offset of DBS. To this end we recorded LFPs from the STN in 14 PD patients during long (mean: 181.2 s) and short (14.2 s) blocks of continuous stimulation at 130 Hz. LFP activities were evaluated in the temporal and spectral domains. During long stimulation blocks, the frequency and amplitude of the ERNA decreased before reaching a steady state after ~70 s. Maximal ERNA amplitudes diminished over repeated stimulation blocks. Upon DBS cessation, the ERNA was revealed as an under-damped oscillation, and was more marked and lasted longer after short duration stimulation blocks. In contrast, activity in the beta band suppressed within 0.5 s of continuous DBS onset and drifted less over time. Spontaneous activity was also suppressed in the low gamma band, suggesting that the effects of high frequency stimulation on spontaneous oscillations may not be selective for pathological beta activity. High frequency oscillations were present in only six STN recordings before stimulation onset and their frequency was depressed by stimulation. The different dynamics of the ERNA and beta activity with stimulation imply different DBS mechanisms and may impact how these activities may be used in adaptive feedback. • ERNA frequency and amplitude reach a steady state after ~70 s stimulation. • Beta activity is suppressed within 0.5 s by stimulation and then remains stable. • Different response dynamics provide different insights into stimulation effects. • Different response dynamics may impact how signals may be used in adaptive DBS. Local field potentials (LFPs) may afford insight into the mechanisms of action of deep brain stimulation (DBS) and potential feedback signals for adaptive DBS. In Parkinson's disease (PD) DBS of the subthalamic nucleus (STN) suppresses spontaneous activity in the beta band and drives evoked resonant neural activity (ERNA). Here, we investigate how STN LFP activities change over time following the onset and offset of DBS. To this end we recorded LFPs from the STN in 14 PD patients during long (mean: 181.2 s) and short (14.2 s) blocks of continuous stimulation at 130 Hz. LFP activities were evaluated in the temporal and spectral domains. During long stimulation blocks, the frequency and amplitude of the ERNA decreased before reaching a steady state after ~70 s. Maximal ERNA amplitudes diminished over repeated stimulation blocks. Upon DBS cessation, the ERNA was revealed as an under-damped oscillation, and was more marked and lasted longer after short duration stimulation blocks. In contrast, activity in the beta band suppressed within 0.5 s of continuous DBS onset and drifted less over time. Spontaneous activity was also suppressed in the low gamma band, suggesting that the effects of high frequency stimulation on spontaneous oscillations may not be selective for pathological beta activity. High frequency oscillations were present in only six STN recordings before stimulation onset and their frequency was depressed by stimulation. The different dynamics of the ERNA and beta activity with stimulation imply different DBS mechanisms and may impact how these activities may be used in adaptive feedback. |
ArticleNumber | 105019 |
Author | Groppa, S. Torrecillos, F. Wiest, C. Mostofi, A. Bange, M. Brown, P. Pogosyan, A. Muthuraman, M. Tinkhauser, G. Baig, F. Pereira, E.A. Tan, H. |
Author_xml | – sequence: 1 givenname: C. surname: Wiest fullname: Wiest, C. organization: Medical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, UK – sequence: 2 givenname: G. surname: Tinkhauser fullname: Tinkhauser, G. organization: Department of Neurology, Bern University Hospital, Bern, Switzerland – sequence: 3 givenname: A. surname: Pogosyan fullname: Pogosyan, A. organization: Medical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, UK – sequence: 4 givenname: M. surname: Bange fullname: Bange, M. organization: Movement Disorders and Neurostimulation, Biomedical Statistics and Multimodal Signal Processing Unit, Department of Neurology, Mainz University Hospital, Mainz, Germany – sequence: 5 givenname: M. surname: Muthuraman fullname: Muthuraman, M. organization: Movement Disorders and Neurostimulation, Biomedical Statistics and Multimodal Signal Processing Unit, Department of Neurology, Mainz University Hospital, Mainz, Germany – sequence: 6 givenname: S. surname: Groppa fullname: Groppa, S. organization: Movement Disorders and Neurostimulation, Biomedical Statistics and Multimodal Signal Processing Unit, Department of Neurology, Mainz University Hospital, Mainz, Germany – sequence: 7 givenname: F. surname: Baig fullname: Baig, F. organization: Medical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, UK – sequence: 8 givenname: A. surname: Mostofi fullname: Mostofi, A. organization: Neurosciences Research Centre, Molecular and Clinical Sciences Institute, St. George's, University of London, London, UK – sequence: 9 givenname: E.A. surname: Pereira fullname: Pereira, E.A. organization: Neurosciences Research Centre, Molecular and Clinical Sciences Institute, St. George's, University of London, London, UK – sequence: 10 givenname: H. surname: Tan fullname: Tan, H. organization: Medical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, UK – sequence: 11 givenname: P. surname: Brown fullname: Brown, P. organization: Medical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, UK – sequence: 12 givenname: F. surname: Torrecillos fullname: Torrecillos, F. email: flavie.torrecillos@ndcn.ox.ac.uk organization: Medical Research Council Brain Network Dynamics Unit, University of Oxford, Oxford, UK |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32681881$$D View this record in MEDLINE/PubMed |
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Keywords | High frequency oscillations Gamma activity Parkinson's disease Local field potentials Evoked resonant neural activity Feedback markers Beta oscillations Adaptive deep brain stimulation |
Language | English |
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