Rhythm-specific modulation of the sensorimotor network in drug-naive patients with Parkinson's disease by levodopa

F. Esposito, A. Tessitore, A. Giordano, R. De Micco, A. Paccone, R. Conforti, G. Pignataro, L. Annunziato, G. Tedeschi

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Abstract

Brain activity during rest is characterized by slow (0.01-0.1 Hz) fluctuations of blood oxygenation level-dependent functional magnetic resonance imaging signals. These fluctuations are organized as functional connectivity networks called resting-state networks, anatomically corresponding to specific neuronal circuits. As Parkinson's disease is mainly characterized by a dysfunction of the sensorimotor pathways, which can be influenced by levodopa administration, the present study investigated the functional connectivity changes within the sensorimotor resting-state network in drug-naive patients with Parkinson's disease after acute levodopa administration. Using a double-blind placebo-controlled design, resting-state functional magnetic resonance imaging was carried out in 20 drug-naive patients with Parkinson's disease, immediately before and 60 min after, oral administration of either levodopa or placebo. Control resting-state functional magnetic resonance imaging data were recorded in 18 age- and sex-matched healthy volunteers. Independent component analysis was performed to extract resting-state network maps and associated time-course spectral features. At the anatomical level, levodopa enhanced the sensorimotor network functional connectivity in the supplementary motor area, a region where drug-naive patients with Parkinson's disease exhibited reduced signal fluctuations compared with untreated patients. At the spectral frequency level, levodopa stimulated these fluctuations in a selective frequency band of the sensorimotor network. The reported effects induced by levodopa on sensorimotor network topological and spectral features confirm that the sensorimotor system is a target of acute levodopa administration in drug-naive patients with Parkinson's disease. Moreover, while the regional changes in supplementary motor area reflect the functional improvement in motor function, the rhythm-specific modulation induced by the dopamine precursor discloses a novel aspect of pharmacological stimulation in Parkinson's disease, adding further insight to the comprehension of levodopa action.
Original languageEnglish
Pages (from-to)710-725
Number of pages16
JournalBrain
Volume136
Issue number3
DOIs
Publication statusPublished - Mar 2013

Keywords

  • resting-state functional magnetic resonance imaging
  • levodopa
  • motor function
  • sensorimotor network
  • Parkinson disease
  • INDEPENDENT COMPONENT ANALYSIS
  • RESTING-STATE NETWORKS
  • CEREBRAL-BLOOD-FLOW
  • EXTERNALLY TRIGGERED MOVEMENTS
  • POSITRON EMISSION TOMOGRAPHY
  • FUNCTIONAL CONNECTIVITY
  • HUMAN BRAIN
  • MOTOR CORTEX
  • IMAGE-ANALYSIS
  • FMRI

Cite this

Esposito, F., Tessitore, A., Giordano, A., De Micco, R., Paccone, A., Conforti, R., Pignataro, G., Annunziato, L., & Tedeschi, G. (2013). Rhythm-specific modulation of the sensorimotor network in drug-naive patients with Parkinson's disease by levodopa. Brain, 136(3), 710-725. https://doi.org/10.1093/brain/awt007