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Sensorimotor processing in the basal ganglia leads to transient beta oscillations during behavior

Amin Mirzaei, Arvind Kumar, Daniel Leventhal, Nicolas Mallet, Ad Aertsen, Joshua Berke, Robert Schmidt
doi: https://doi.org/10.1101/136879
Amin Mirzaei
1BrainLinks-BrainTools, University of Freiburg, Freiburg, Germany.
2Faculty of Biology, University of Freiburg, Freiburg, Germany.
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Arvind Kumar
3Computational Biology, School of Computer Science and Communication, KTH Royal Institute of Technology, Stockholm, Sweden.
4Bernstein Center Freiburg, University of Freiburg, Freiburg, Germany.
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Daniel Leventhal
5Department of Neurology, University of Michigan, Ann Arbor, MI 48109, United States.
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Nicolas Mallet
6Universite de Bordeaux, Institut des Maladies Neurodegeneratives, 33076 Bordeaux, France.
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Ad Aertsen
2Faculty of Biology, University of Freiburg, Freiburg, Germany.
4Bernstein Center Freiburg, University of Freiburg, Freiburg, Germany.
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Joshua Berke
7Department of Neurology and Kavli Institute for Fundamental Neuroscience, University of California San Francisco, USA.
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Robert Schmidt
8Department of Psychology, University of Sheffield, UK.
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Abstract

Brief epochs of beta oscillations have been implicated in sensorimotor control in the basal ganglia of task-performing healthy animals. However, which neural processes underlie their generation and how they are affected by sensorimotor processing remains unclear. To determine the mechanisms underlying transient beta oscillations in the local field potential (LFP), we combined computational modeling of the subthalamo-pallidal network for the generation of beta oscillations with realistic stimulation patterns derived from single unit data. The single unit data were recorded from different basal ganglia subregions in rats performing a cued choice task. In the recordings we found distinct firing patterns in the striatum, globus pallidus and subthalamic nucleus related to sensory and motor events during the behavioral task. Using these firing patterns to generate realistic inputs to our network model lead to transient beta oscillations with the same time course as the rat LFP data. In addition, our model can account for further non-intuitive aspects of beta modulation, including beta phase resets following sensory cues and correlations with reaction time. Overall, our model can explain how the combination of temporally regulated sensory responses of the subthalamic nucleus, ramping activity of the subthalamic nucleus, and movement-related activity of the globus pallidus, leads to transient beta oscillations during behavior.

Significance Statement Transient beta oscillations emerge in the normal functioning cortico-basal ganglia loop during behavior. In this work we employ a unique approach connecting a computational model closely with experimental data. In this way we achieve a simulation environment for our model that mimics natural input patterns in awake behaving animals. Using this approach we demonstrate that a computational model for beta oscillations in Parkinson’s disease can also account for complex patterns of transient beta oscillations in healthy animals. Therefore, we propose that transient beta oscillations in healthy animals share the same mechanism with pathological beta oscillations in Parkinson’s disease. This important result connects functional and pathological roles of beta oscillations in the basal ganglia.

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Posted September 21, 2017.
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Sensorimotor processing in the basal ganglia leads to transient beta oscillations during behavior
Amin Mirzaei, Arvind Kumar, Daniel Leventhal, Nicolas Mallet, Ad Aertsen, Joshua Berke, Robert Schmidt
bioRxiv 136879; doi: https://doi.org/10.1101/136879
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Sensorimotor processing in the basal ganglia leads to transient beta oscillations during behavior
Amin Mirzaei, Arvind Kumar, Daniel Leventhal, Nicolas Mallet, Ad Aertsen, Joshua Berke, Robert Schmidt
bioRxiv 136879; doi: https://doi.org/10.1101/136879

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