209 Movement-Related Dynamics of Beta Band Causal Interactions Between Subthalamic Nucleus and Sensorimotor Cortex Revealed Through Intraoperative Recordings in Parkinson's Disease

Ahmad Alhourani, Anna Korzeniewska, Thomas A. Wozny, Efstathios Kondylis, Witold J. Lipski, Donald Crammond, R. Mark Richardson

Research output: Contribution to journalArticle

Abstract

INTRODUCTION: Beta oscillations play an important role in gating movement. Because pathological oscillatory changes in the beta band represent a hallmark of Parkinson disease (PD), tracking oscillatory changes in this band has been proposed as a marker for closed-loop stimulation. However, the dynamics of casual influences across the motor circuit during movement remain unknown. Using intracranial local field potential (LFP) recordings, we used both standard functional connectivity and event-related causality (ERC) techniques to explore these interactions.

METHODS: LFPs were recorded simultaneously from subthalamic nucleus (STN) and sensorimotor cortex, while PD subjects (n = 8) undergoing the implantation of DBS leads performed an incentivized, bimanual handgrip task. Using the beta frequency band between 13 and 30 Hz, functional connectivity was estimated using wavelet-based phase locking values (PLV), and ERC was calculated by constructing a multivariate autoregressive model based on the signal of interest from M1, S1, and STN channels. A false discovery rate correction of 5% was applied.

RESULTS: All the patients showed significant causal interactions between STN and sensorimotor cortex that coincided with movement epochs showing significant PLV on the individual level. In the 200 ms before movement, precentral beta activity modulated beta activity in the STN, implying that cortical beta activity drives the STN beta activity in that epoch. Reciprocal modulations between the cortex and STN were apparent at the termination of movement. Causal influences from the precentral cortex to the STN in the beta band around 0.5 ms after movement onset correlated significantly with the time to peak force (rho = 0.86, corrected P < .0028).

CONCLUSION: The directionality of causal interactions across the basal ganglia-cortical motor loop are specific to the directionality of causal interactions across the basal ganglia-cortical motor loop are specific to different phases of motor planning and execution. These novel data highlight the value of intraoperative recordings for furthering our understanding of cortical-basal ganglia models.

Original languageEnglish (US)
Number of pages1
JournalNeurosurgery
Volume63
DOIs
StatePublished - Aug 1 2016

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Subthalamic Nucleus
Parkinson Disease
Basal Ganglia
Causality
Sensorimotor Cortex

ASJC Scopus subject areas

  • Surgery
  • Clinical Neurology

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209 Movement-Related Dynamics of Beta Band Causal Interactions Between Subthalamic Nucleus and Sensorimotor Cortex Revealed Through Intraoperative Recordings in Parkinson's Disease. / Alhourani, Ahmad; Korzeniewska, Anna; Wozny, Thomas A.; Kondylis, Efstathios; Lipski, Witold J.; Crammond, Donald; Richardson, R. Mark.

In: Neurosurgery, Vol. 63, 01.08.2016.

Research output: Contribution to journalArticle

Alhourani, Ahmad ; Korzeniewska, Anna ; Wozny, Thomas A. ; Kondylis, Efstathios ; Lipski, Witold J. ; Crammond, Donald ; Richardson, R. Mark. / 209 Movement-Related Dynamics of Beta Band Causal Interactions Between Subthalamic Nucleus and Sensorimotor Cortex Revealed Through Intraoperative Recordings in Parkinson's Disease. In: Neurosurgery. 2016 ; Vol. 63.
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abstract = "INTRODUCTION: Beta oscillations play an important role in gating movement. Because pathological oscillatory changes in the beta band represent a hallmark of Parkinson disease (PD), tracking oscillatory changes in this band has been proposed as a marker for closed-loop stimulation. However, the dynamics of casual influences across the motor circuit during movement remain unknown. Using intracranial local field potential (LFP) recordings, we used both standard functional connectivity and event-related causality (ERC) techniques to explore these interactions.METHODS: LFPs were recorded simultaneously from subthalamic nucleus (STN) and sensorimotor cortex, while PD subjects (n = 8) undergoing the implantation of DBS leads performed an incentivized, bimanual handgrip task. Using the beta frequency band between 13 and 30 Hz, functional connectivity was estimated using wavelet-based phase locking values (PLV), and ERC was calculated by constructing a multivariate autoregressive model based on the signal of interest from M1, S1, and STN channels. A false discovery rate correction of 5{\%} was applied.RESULTS: All the patients showed significant causal interactions between STN and sensorimotor cortex that coincided with movement epochs showing significant PLV on the individual level. In the 200 ms before movement, precentral beta activity modulated beta activity in the STN, implying that cortical beta activity drives the STN beta activity in that epoch. Reciprocal modulations between the cortex and STN were apparent at the termination of movement. Causal influences from the precentral cortex to the STN in the beta band around 0.5 ms after movement onset correlated significantly with the time to peak force (rho = 0.86, corrected P < .0028).CONCLUSION: The directionality of causal interactions across the basal ganglia-cortical motor loop are specific to the directionality of causal interactions across the basal ganglia-cortical motor loop are specific to different phases of motor planning and execution. These novel data highlight the value of intraoperative recordings for furthering our understanding of cortical-basal ganglia models.",
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AU - Alhourani, Ahmad

AU - Korzeniewska, Anna

AU - Wozny, Thomas A.

AU - Kondylis, Efstathios

AU - Lipski, Witold J.

AU - Crammond, Donald

AU - Richardson, R. Mark

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AB - INTRODUCTION: Beta oscillations play an important role in gating movement. Because pathological oscillatory changes in the beta band represent a hallmark of Parkinson disease (PD), tracking oscillatory changes in this band has been proposed as a marker for closed-loop stimulation. However, the dynamics of casual influences across the motor circuit during movement remain unknown. Using intracranial local field potential (LFP) recordings, we used both standard functional connectivity and event-related causality (ERC) techniques to explore these interactions.METHODS: LFPs were recorded simultaneously from subthalamic nucleus (STN) and sensorimotor cortex, while PD subjects (n = 8) undergoing the implantation of DBS leads performed an incentivized, bimanual handgrip task. Using the beta frequency band between 13 and 30 Hz, functional connectivity was estimated using wavelet-based phase locking values (PLV), and ERC was calculated by constructing a multivariate autoregressive model based on the signal of interest from M1, S1, and STN channels. A false discovery rate correction of 5% was applied.RESULTS: All the patients showed significant causal interactions between STN and sensorimotor cortex that coincided with movement epochs showing significant PLV on the individual level. In the 200 ms before movement, precentral beta activity modulated beta activity in the STN, implying that cortical beta activity drives the STN beta activity in that epoch. Reciprocal modulations between the cortex and STN were apparent at the termination of movement. Causal influences from the precentral cortex to the STN in the beta band around 0.5 ms after movement onset correlated significantly with the time to peak force (rho = 0.86, corrected P < .0028).CONCLUSION: The directionality of causal interactions across the basal ganglia-cortical motor loop are specific to the directionality of causal interactions across the basal ganglia-cortical motor loop are specific to different phases of motor planning and execution. These novel data highlight the value of intraoperative recordings for furthering our understanding of cortical-basal ganglia models.

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