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Cortico-Striatal Oscillations Are Correlated to Motor Activity Levels in Both Physiological and Parkinsonian Conditions

Moënne-Loccoz, Cristóbal ; Astudillo-Valenzuela, Carolina ; Skovgård, Katrine LU ; Salazar-Reyes, Carolina A. ; Barrientos, Sebastian A. LU orcid ; García-Núñez, Ximena P. ; Cenci, M. Angela LU orcid ; Petersson, Per LU and Fuentes-Flores, Rómulo A. (2020) In Frontiers in Systems Neuroscience 14.
Abstract

Oscillatory neural activity in the cortico-basal ganglia-thalamocortical (CBGTC) loop is associated with the motor state of a subject, but also with the availability of modulatory neurotransmitters. For example, increased low-frequency oscillations in Parkinson’s disease (PD) are related to decreased levels of dopamine and have been proposed as biomarkers to adapt and optimize therapeutic interventions, such as deep brain stimulation. Using neural oscillations as biomarkers require differentiating between changes in oscillatory patterns associated with parkinsonism vs. those related to a subject’s motor state. To address this point, we studied the correlation between neural oscillatory activity in the motor cortex and striatum and... (More)

Oscillatory neural activity in the cortico-basal ganglia-thalamocortical (CBGTC) loop is associated with the motor state of a subject, but also with the availability of modulatory neurotransmitters. For example, increased low-frequency oscillations in Parkinson’s disease (PD) are related to decreased levels of dopamine and have been proposed as biomarkers to adapt and optimize therapeutic interventions, such as deep brain stimulation. Using neural oscillations as biomarkers require differentiating between changes in oscillatory patterns associated with parkinsonism vs. those related to a subject’s motor state. To address this point, we studied the correlation between neural oscillatory activity in the motor cortex and striatum and varying degrees of motor activity under normal and parkinsonian conditions. Using rats with bilateral or unilateral 6-hydroxydopamine lesions as PD models, we correlated the motion index (MI)—a measure based on the physical acceleration of the head of rats—to the local field potential (LFP) oscillatory power in the 1–80 Hz range. In motor cortices and striata, we observed a robust correlation between the motion index and the oscillatory power in two main broad frequency ranges: a low-frequency range [5.0–26.5 Hz] was negatively correlated to motor activity, whereas a high-frequency range [35.0–79.9 Hz] was positively correlated. We observed these correlations in both normal and parkinsonian conditions. In addition to these general changes in broad-band power, we observed a more restricted narrow-band oscillation [25–40 Hz] in dopamine-denervated hemispheres. This oscillation, which seems to be selective to the parkinsonian state, showed a linear frequency dependence on the concurrent motor activity level. We conclude that, independently of the parkinsonian condition, changes in broad-band oscillatory activities of cortico-basal ganglia networks (including changes in the relative power of low- and high-frequency bands) are closely correlated to ongoing motions, most likely reflecting he operations of these neural circuits to control motor activity. Hence, biomarkers based on neural oscillations should focus on specific features, such as narrow frequency bands, to allow differentiation between parkinsonian states and physiological movement-dependent circuit modulation.

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author
; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
acceleration, beta, cortex, local field potential, motor activity, oscillations, parkinsonian, striatum
in
Frontiers in Systems Neuroscience
volume
14
article number
56
publisher
Frontiers Media S. A.
external identifiers
  • scopus:85089920508
  • pmid:32903888
ISSN
1662-5137
DOI
10.3389/fnsys.2020.00056
project
Models and biomarkers of motor and neuropsychiatric complications in Parkinson’s disease
language
English
LU publication?
yes
id
b9fdbdbf-d518-468a-a806-a1c43172d487
date added to LUP
2020-09-08 11:59:28
date last changed
2024-05-29 19:32:11
@article{b9fdbdbf-d518-468a-a806-a1c43172d487,
  abstract     = {{<p>Oscillatory neural activity in the cortico-basal ganglia-thalamocortical (CBGTC) loop is associated with the motor state of a subject, but also with the availability of modulatory neurotransmitters. For example, increased low-frequency oscillations in Parkinson’s disease (PD) are related to decreased levels of dopamine and have been proposed as biomarkers to adapt and optimize therapeutic interventions, such as deep brain stimulation. Using neural oscillations as biomarkers require differentiating between changes in oscillatory patterns associated with parkinsonism vs. those related to a subject’s motor state. To address this point, we studied the correlation between neural oscillatory activity in the motor cortex and striatum and varying degrees of motor activity under normal and parkinsonian conditions. Using rats with bilateral or unilateral 6-hydroxydopamine lesions as PD models, we correlated the motion index (MI)—a measure based on the physical acceleration of the head of rats—to the local field potential (LFP) oscillatory power in the 1–80 Hz range. In motor cortices and striata, we observed a robust correlation between the motion index and the oscillatory power in two main broad frequency ranges: a low-frequency range [5.0–26.5 Hz] was negatively correlated to motor activity, whereas a high-frequency range [35.0–79.9 Hz] was positively correlated. We observed these correlations in both normal and parkinsonian conditions. In addition to these general changes in broad-band power, we observed a more restricted narrow-band oscillation [25–40 Hz] in dopamine-denervated hemispheres. This oscillation, which seems to be selective to the parkinsonian state, showed a linear frequency dependence on the concurrent motor activity level. We conclude that, independently of the parkinsonian condition, changes in broad-band oscillatory activities of cortico-basal ganglia networks (including changes in the relative power of low- and high-frequency bands) are closely correlated to ongoing motions, most likely reflecting he operations of these neural circuits to control motor activity. Hence, biomarkers based on neural oscillations should focus on specific features, such as narrow frequency bands, to allow differentiation between parkinsonian states and physiological movement-dependent circuit modulation.</p>}},
  author       = {{Moënne-Loccoz, Cristóbal and Astudillo-Valenzuela, Carolina and Skovgård, Katrine and Salazar-Reyes, Carolina A. and Barrientos, Sebastian A. and García-Núñez, Ximena P. and Cenci, M. Angela and Petersson, Per and Fuentes-Flores, Rómulo A.}},
  issn         = {{1662-5137}},
  keywords     = {{acceleration; beta; cortex; local field potential; motor activity; oscillations; parkinsonian; striatum}},
  language     = {{eng}},
  publisher    = {{Frontiers Media S. A.}},
  series       = {{Frontiers in Systems Neuroscience}},
  title        = {{Cortico-Striatal Oscillations Are Correlated to Motor Activity Levels in Both Physiological and Parkinsonian Conditions}},
  url          = {{http://dx.doi.org/10.3389/fnsys.2020.00056}},
  doi          = {{10.3389/fnsys.2020.00056}},
  volume       = {{14}},
  year         = {{2020}},
}