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
J. Neurosci.. 2017-10-16; 37(46): 11220-11232
DOI: 10.1523/JNEUROSCI.1289-17.2017

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1. J Neurosci. 2017 Nov 15;37(46):11220-11232. doi: 10.1523/JNEUROSCI.1289-17.2017.
Epub 2017 Oct 16.

Sensorimotor Processing in the Basal Ganglia Leads to Transient Beta Oscillations
during Behavior.

Mirzaei A(1)(2), Kumar A(3)(4), Leventhal D(5), Mallet N(6), Aertsen A(2)(4),
Berke J(7), Schmidt R(8).

Author information:
(1)BrainLinks-BrainTools, University of Freiburg, 79110, Freiburg, Germany,
(2)Faculty of Biology, University of Freiburg, 79104, Freiburg, Germany.
(3)Computational Biology, School of Computer Science and Communication, KTH Royal
Institute of Technology, 11428 Stockholm, Sweden.
(4)Bernstein Center Freiburg, University of Freiburg, 79104, Freiburg, Germany.
(5)Department of Neurology, University of Michigan, Ann Arbor, Michigan 48109.
(6)Institut des Maladies Neurodegeneratives, Universite de Bordeaux, 33076,
Bordeaux, France.
(7)Department of Neurology and Kavli Institute for Fundamental Sciences,
University of California, San Francisco, California 94158, and.
(8)Department of Psychology, University of Sheffield, Cathederal Court,
Sheffield, S1 1HD, United Kingdom.

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 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 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 led to transient beta oscillations with the same time course as the rat LFP
data. In addition, our model can account for further nonintuitive aspects of beta
modulation, including beta phase resets after 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. Here, we used a unique approach connecting a computational model
closely with experimental data. In this way, we achieved a simulation environment
for our model that mimics natural input patterns in awake, behaving animals. We
demonstrate that a computational model for beta oscillations in Parkinson’s
disease (PD) 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
PD. This important result connects functional and pathological roles of beta
oscillations in the basal ganglia.

Copyright © 2017 the authors 0270-6474/17/3711220-13$15.00/0.

DOI: 10.1523/JNEUROSCI.1289-17.2017
PMID: 29038241 [Indexed for MEDLINE]

Auteurs Bordeaux Neurocampus