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

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.

[1]  J. Wickens,et al.  Computational models of the basal ganglia: from robots to membranes , 2004, Trends in Neurosciences.

[2]  J. Obeso,et al.  Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. , 2005, Brain : a journal of neurology.

[3]  Claire Calmels,et al.  Cortical Activity Prior to, and During, Observation and Execution of Sequential Finger Movements , 2006, Brain Topography.

[4]  M. Hallett,et al.  Electroencephalographic analysis of cortico-muscular coherence: reference effect, volume conduction and generator mechanism , 1999, Clinical Neurophysiology.

[5]  G. Rizzolatti,et al.  Resonance behaviors and mirror neurons. , 1999, Archives italiennes de biologie.

[6]  L. Craighero,et al.  Electrophysiology of Action Representation , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[7]  A. Oliviero,et al.  Dopamine Dependency of Oscillations between Subthalamic Nucleus and Pallidum in Parkinson's Disease , 2001, The Journal of Neuroscience.

[8]  A. Nambu.  A new dynamic model of the cortico-basal ganglia loop. , 2004, Progress in brain research.

[9]  Á. Pascual-Leone,et al.  Phase-specific modulation of cortical motor output during movement observation , 2001, Neuroreport.

[10]  W. Szurhaj,et al.  Predominance of the contralateral movement-related activity in the subthalamo-cortical loop , 2006, Clinical Neurophysiology.

[11]  A. Lozano,et al.  Targeting the basal ganglia for deep brain stimulation in Parkinson's disease. , 2000, Neurology.

[12]  F. Tremblay,et al.  Corticomotor facilitation associated with observation and imagery of hand actions is impaired in Parkinson’s disease , 2008, Experimental Brain Research.

[13]  M. Delong,et al.  Functional and pathophysiological models of the basal ganglia , 1996, Current Opinion in Neurobiology.

[14]  A. Priori,et al.  Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease , 2004, Experimental Neurology.

[15]  G. Baselli,et al.  Movement‐related frequency modulation of beta oscillatory activity in the human subthalamic nucleus , 2005, The Journal of physiology.

[16]  Tipu Aziz,et al.  Movement‐related synchronization of gamma activity is lateralized in patients with dystonia , 2008, The European journal of neuroscience.

[17]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[18]  J. Obeso,et al.  Efficacy of deep brain stimulation of the subthalamic nucleus in Parkinson’s disease 4 years after surgery: double blind and open label evaluation , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[19]  J A Obeso,et al.  Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. , 2006, Brain : a journal of neurology.

[20]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[21]  M. Fiorio,et al.  Modulation of beta oscillations in the subthalamic area during action observation in Parkinson's disease , 2009, Neuroscience.

[22]  A. Nambu.  Seven problems on the basal ganglia , 2008, Current Opinion in Neurobiology.

[23]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

[24]  Joseph P. McCleery,et al.  EEG evidence for mirror neuron dysfunction in autism spectrum disorders. , 2005, Brain research. Cognitive brain research.

[25]  K. Mewes,et al.  The subthalamic nucleus in Parkinson's disease: somatotopic organization and physiological characteristics. , 2001, Brain : a journal of neurology.

[26]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[27]  Peter Brown,et al.  Modulation of beta oscillations in the subthalamic area during motor imagery in Parkinson's disease. , 2006, Brain : a journal of neurology.

[28]  S. Cochin,et al.  Perception of motion and qEEG activity in human adults. , 1998, Electroencephalography and clinical neurophysiology.

[29]  Febo Cincotti,et al.  Human Cortical Electroencephalography (EEG) Rhythms during the Observation of Simple Aimless Movements: A High-Resolution EEG Study , 2002, NeuroImage.

[30]  B. Puri,et al.  The human mirror system: A motor resonance theory of mind-reading , 2007, Brain Research Reviews.

[31]  H. Bekkering,et al.  The mirror neuron system is more active during complementary compared with imitative action , 2007, Nature Neuroscience.

[32]  G. Rizzolatti,et al.  Motor facilitation during action observation: a magnetic stimulation study. , 1995, Journal of neurophysiology.

[33]  P. Brown,et al.  Levodopa‐induced modulation of subthalamic beta oscillations during self‐paced movements in patients with Parkinson's disease , 2005, The European journal of neuroscience.

[34]  Ellen Poliakoff,et al.  The effect of viewing graspable objects and actions in Parkinson's disease , 2007, Neuroreport.

[35]  Riitta Hari,et al.  Actor's and observer's primary motor cortices stabilize similarly after seen or heard motor actions , 2007, Proceedings of the National Academy of Sciences.

[36]  J. Mink.  THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[37]  J A Obeso,et al.  Movement‐related changes in oscillatory activity in the human subthalamic nucleus: ipsilateral vs. contralateral movements , 2005, The European journal of neuroscience.

[38]  A. Meltzoff,et al.  A PET Exploration of the Neural Mechanisms Involved in Reciprocal Imitation , 2002, NeuroImage.

[39]  M. Iacoboni,et al.  The mirror neuron system and the consequences of its dysfunction , 2006, Nature Reviews Neuroscience.

[40]  Andrew N. Meltzoff,et al.  Neural circuits involved in imitation and perspective-taking , 2006, NeuroImage.

[41]  P. Brown.  Oscillatory nature of human basal ganglia activity: Relationship to the pathophysiology of Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[42]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[43]  U. Castiello,et al.  Visuomotor priming effects in Parkinson's disease patients depend on the match between the observed and the executed action , 2009, Neuropsychologia.

[44]  G. Rizzolatti,et al.  Activation of human primary motor cortex during action observation: a neuromagnetic study. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[45]  G Pfurtscheller,et al.  Event-related coherence as a tool for studying dynamic interaction of brain regions. , 1996, Electroencephalography and clinical neurophysiology.

[46]  L. Cohen,et al.  Time-frequency distributions-a review , 1989, Proc. IEEE.

[47]  A. Oliviero,et al.  Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. , 2002, Brain : a journal of neurology.

[48]  C D Frith,et al.  A possible role for primary motor cortex during action observation , 2007, Proceedings of the National Academy of Sciences.

[49]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[50]  Alexander Münchau,et al.  Investigating the human mirror neuron system by means of cortical synchronization during the imitation of biological movements , 2006, NeuroImage.

[51]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[52]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[53]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[54]  C. Marsden,et al.  The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. , 1994, Brain : a journal of neurology.

[55]  J. Artieda,et al.  Movement-related changes in cortical oscillatory activity in ballistic, sustained and negative movements , 2002, Experimental Brain Research.

[56]  Peter Brown,et al.  Patterns of Bidirectional Communication between Cortex and Basal Ganglia during Movement in Patients with Parkinson Disease , 2008, The Journal of Neuroscience.