Changes in subthalamic activity during movement observation in Parkinson’s disease: Is the mirror system mirrored in the basal ganglia?

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Abstract

Objective

The observation of a voluntary movement executed by another person is associated with an alpha and beta EEG desynchronization over the motor cortex, thought to reflect activity from the human “mirror neuron” system. The aim of our work was to study the changes in local field potentials (LFP) recorded from the subthalamic nucleus (STN) and their relationship with cortical activity, during movement observation.

Methods

Bilateral EEG and STN LFP recordings were acquired in 18 patients with Parkinson’s disease, through surgically implanted electrodes for deep brain stimulation. Oscillatory changes during movement execution and movement observation were compared with two different control conditions (simple stimulus and rotating stimulus observation), in “off” and “on” motor states. Time–frequency transforms and event-related coherence were used for the analysis.

Results

Movement observation was accompanied by bilateral beta reduction in subthalamic power and cortico-STN coherence, which was smaller than the decrease observed during movement execution, but significant when compared with the two control conditions.

Conclusions

Movement observation is accompanied by changes in the beta oscillatory activity of the STN, similar to those observed in the EEG.

Significance

These changes suggest that the basal ganglia might be engaged by the activity of the human mirror system.

Introduction

The term “mirror neurons” was initially given to a group of neurons located in the monkey frontal cortex that discharge both when a purposeful movement is executed and when that movement is observed (Rizzolatti et al., 1996). Neurons with similar properties have been found in other regions beyond the frontal lobe, like the inferior parietal lobe (Fogassi et al., 2005). There is increasing evidence that a similar system exists in humans, encompassing a complex visuo–motor network (Iacoboni et al., 1999, Buccino et al., 2001). A recent study using magnetoencephalography (MEG) suggests that the basal ganglia might be also involved in that circuit (Kessler et al., 2006). Otherwise, no definite evidence from direct recording of basal ganglia activity has so far been reported.

Deep brain stimulation (DBS) of the internal part of the globus pallidus (GPi) and subthalamic nucleus (STN) to treat Parkinson’s disease (PD) and other movement disorders has become nowadays a routine surgical procedure. The macroelectrodes used for DBS allow the recording of local field potentials (LFP) and provide an opportunity to study the basal ganglia in humans. In the “off medication” state of PD, the STN and GPi show a predominant activity in the high alpha-low beta range (11–30 Hz) which is attenuated when parkinsonian signs abate during the “on” medication state. The latter is also characterized by a peak around 60–80 Hz in the power spectrum (Brown et al., 2001). More recently, an increase in the theta band in the STN has been described in the “on” state related to the presence of levodopa-induced dyskinesia (Alonso-Frech et al., 2006).

Execution of a voluntary movement is associated with changes in the oscillatory activity recorded from the STN in PD patients (Doyle et al., 2005). Thus, in the “off” state, the alpha–beta activity decreases in power from at least 1 s before movement initiation until the end of the action. In the “on” state, a decrease in the beta range can also be observed with a similar temporal pattern and relative amplitude (despite the lower absolute values) together with a marked increase in gamma activity (Alegre et al., 2005). Similar findings (beta decrease and gamma increase during movement) have been described in the GPi of patients with dystonia (Brucke et al., 2008).

In normal subjects, movement-related changes in oscillatory activity in the motor cortex are similar to those found in the STN in PD patients (decrease in alpha and beta activity, increase in the gamma range) (Crone et al., 1998, Alegre et al., 2003). A peri-movement decrease in cortico-STN beta coherence has also been described in PD patients (Kuhn et al., 2006).

Observation of movement execution by another person is associated with a decrease in alpha and beta EEG bands recorded over the motor cortex (Babiloni et al., 2002, Calmels et al., 2006). Such changes are thought to reflect activity from the human mirror neuron system. In a recent study, Marceglia et al. (2009) described in a small group of patients the presence of beta changes in subthalamic activity during the observation of a motor action in a movie clip.

We report here the presence of changes in LFP recorded from the STN in patients with PD related to the observation of a movement performed by another subject, which are not present during the observation of a static or moving visual stimulus. These changes are present in both “on” and “off” motor states, and share some properties with those observed during movement execution.

Section snippets

Methods

A total of 18 highly collaborative PD patients treated with bilateral DBS of the STN were studied. All patients were right-handed according to the Oldfield inventory. The study, conformed to the standards set by the latest revision of the Declaration of Helsinki, was approved by the institutional ethical committee (Comité de ética de investigación clínica de la Universidad de Navarra) and each patient gave written informed consent.

All patients were assessed pre-operatively in the “off”

Results

Results will be presented separately for each of the studies, and separately for the beta and gamma bands.

Discussion

We found that movement observation is associated with significant changes in the beta oscillatory activity in the STN of PD patients. Globally, our results showed the presence of a movement observation-related decrease in beta activity in the STN. This decrease, although smaller than the movement-related decrease, had similar characteristics: it had the same relative amplitude in “on” and “off”, was bilateral, and coherent with cortical activity. The movement-related gamma increase, on the

Conclusions

In summary, our results show that movement observation generates a decrease both in the abnormal beta activity observed in the STN in PD patients and in the cortico-STN coherence, with no change in gamma activity. These findings indicate that the STN is influenced by the activity of the human mirror system but such input by itself is probably insufficient to generate feedback output to the cortex. Further studies are needed to clarify the potential pathophysiological implications of these

Disclosure

The authors have no financial disclosures/conflicts of interest related to the present work.

Acknowledgements

This study has been funded by “UTE project FIMA” and Departamento de Salud, Gobierno de Navarra.

References (55)

  • S. Marceglia et al.

    Modulation of beta oscillations in the subthalamic area during action observation in Parkinson’s disease

    Neuroscience

    (2009)
  • T. Mima et al.

    Electroencephalographic analysis of cortico-muscular coherence: reference effect, volume conduction and generator mechanism

    Clin Neurophysiol

    (1999)
  • J.W. Mink

    The basal ganglia: focused selection and inhibition of competing motor programs

    Prog Neurobiol

    (1996)
  • A. Nambu

    A new dynamic model of the cortico-basal ganglia loop

    Prog Brain Res

    (2004)
  • A. Nambu

    Seven problems on the basal ganglia

    Curr Opin Neurobiol

    (2008)
  • L.M. Oberman et al.

    EEG evidence for mirror neuron dysfunction in autism spectrum disorders

    Brain Res Cogn Brain Res

    (2005)
  • A. Priori et al.

    Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson’s disease

    Exp Neurol

    (2004)
  • G. Rizzolatti et al.

    Premotor cortex and the recognition of motor actions

    Brain Res Cogn Brain Res

    (1996)
  • T. Wichmann et al.

    Functional and pathophysiological models of the basal ganglia

    Curr Opin Neurobiol

    (1996)
  • M. Alegre et al.

    Movement-related changes in oscillatory activity in the human subthalamic nucleus: ipsilateral vs. contralateral movements

    Eur J Neurosci

    (2005)
  • M. Alegre et al.

    Movement-related changes in cortical oscillatory activity in ballistic, sustained and negative movements

    Exp Brain Res

    (2003)
  • F. Alonso-Frech et al.

    Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson’s disease

    Brain

    (2006)
  • P. Brown

    Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson’s disease

    Mov Disord

    (2003)
  • P. Brown et al.

    Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease

    J Neurosci

    (2001)
  • C. Brucke et al.

    Movement-related synchronization of gamma activity is lateralized in patients with dystonia

    Eur J Neurosci

    (2008)
  • G. Buccino et al.

    Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study

    Eur J Neurosci

    (2001)
  • G. Caetano et al.

    Actor’s and observer’s primary motor cortices stabilize similarly after seen or heard motor actions

    Proc Natl Acad Sci USA

    (2007)
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