Pathological gambling in Parkinson's disease: Subthalamic oscillations during economics decisions

Pathological gambling develops in up to 8% of patients with Parkinson's disease. Although the pathophysiology of gambling remains unclear, several findings argue for a dysfunction in the basal ganglia circuits. To clarify the role of the subthalamic nucleus in pathological gambling, we studied its activity during economics decisions. We analyzed local field potentials recorded from deep brain stimulation electrodes in the subthalamic nucleus while parkinsonian patients with (n = 8) and without (n = 9) pathological gambling engaged in an economics decision‐making task comprising conflictual trials (involving possible risk‐taking) and non conflictual trials. In all parkinsonian patients, subthalamic low frequencies (2–12 Hz) increased during economics decisions. Whereas, in patients without gambling, low‐frequency oscillations exhibited a similar pattern during conflictual and non conflictual stimuli, in those with gambling, low‐frequency activity increased significantly more during conflictual than during non conflictual stimuli. The specific low‐frequency oscillatory pattern recorded in patients with Parkinson's disease who gamble could reflect a subthalamic dysfunction that makes their decisional threshold highly sensitive to risky options. When parkinsonian patients process stimuli related to an economics task, low‐frequency subthalamic activity increases. This task‐related change suggests that the cognitive‐affective system that drives economics decisional processes includes the subthalamic nucleus. The specific subthalamic neuronal activity during conflictual decisions in patients with pathological gambling supports the idea that the subthalamic nucleus is involved in behavioral strategies and in the pathophysiology of gambling. © 2013 International Parkinson and Movement Disorder Society

[1]  Sara Marceglia,et al.  The effects of levodopa and ongoing deep brain stimulation on subthalamic beta oscillations in Parkinson's disease , 2010, Experimental Neurology.

[2]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[3]  Dany Paleressompoulle,et al.  Reducing the desire for cocaine with subthalamic nucleus deep brain stimulation , 2009, Proceedings of the National Academy of Sciences.

[4]  Colin Camerer,et al.  Dopamine D1 Receptors and Nonlinear Probability Weighting in Risky Choice , 2010, The Journal of Neuroscience.

[5]  J. Menchón,et al.  Effect of executive functioning, decision-making and self-reported impulsivity on the treatment outcome of pathologic gambling. , 2011, Journal of psychiatry & neuroscience : JPN.

[6]  C. Baunez,et al.  Alcohol Preference Influences the Subthalamic Nucleus Control on Motivation for Alcohol in Rats , 2008, Neuropsychopharmacology.

[7]  S. Houle,et al.  Increased striatal dopamine release in Parkinsonian patients with pathological gambling: a [11C] raclopride PET study. , 2009, Brain : a journal of neurology.

[8]  M Tagliati,et al.  Subthalamic deep brain stimulation and impulse control in Parkinson’s disease , 2009, European journal of neurology.

[9]  E. Foncke,et al.  Pathological gambling after bilateral subthalamic nucleus stimulation in Parkinson disease , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[10]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[11]  P. Brown,et al.  The subthalamic region is activated during valence‐related emotional processing in patients with Parkinson's disease , 2007, The European journal of neuroscience.

[12]  H. Lesieur,et al.  The South Oaks Gambling Screen (SaGS): A New Instrument for the Identification of Pathological Gamblers , 2010 .

[13]  G. Band,et al.  Deep Brain Stimulation of the Subthalamic Nucleus Improves Reward-Based Decision-Learning in Parkinson's Disease , 2011, Front. Hum. Neurosci..

[14]  R. Dolan,et al.  Dopamine, Time, and Impulsivity in Humans , 2010, The Journal of Neuroscience.

[15]  T. Robbins,et al.  Enhanced Food-Related Motivation after Bilateral Lesions of the Subthalamic Nucleus , 2002, The Journal of Neuroscience.

[16]  Alberto Priori,et al.  Functional and clinical neuroanatomy of morality. , 2012, Brain : a journal of neurology.

[17]  S Cerutti,et al.  300-Hz subthalamic oscillations in Parkinson's disease. , 2003, Brain : a journal of neurology.

[18]  R. Snaith,et al.  The Hospital Anxiety And Depression Scale , 2003, Health and quality of life outcomes.

[19]  Andrea A. Kühn,et al.  High-Frequency Stimulation of the Subthalamic Nucleus Suppresses Oscillatory β Activity in Patients with Parkinson's Disease in Parallel with Improvement in Motor Performance , 2008, The Journal of Neuroscience.

[20]  M. Jahanshahi,et al.  STN Stimulation Alters Pallidal—Frontal Coupling during Response Selection under Competition , 2007, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[21]  P. Brown,et al.  Activation of the subthalamic region during emotional processing in Parkinson disease , 2005, Neurology.

[22]  C. Baunez,et al.  Beyond the reward pathway: coding reward magnitude and error in the rat subthalamic nucleus. , 2009, Journal of neurophysiology.

[23]  Y. Agid,et al.  Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior , 2007, Proceedings of the National Academy of Sciences.

[24]  Sara Marceglia,et al.  Neurophysiology of deep brain stimulation. , 2012, International review of neurobiology.

[25]  Thomas V. Wiecki,et al.  Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold , 2011, Nature Neuroscience.

[26]  Mark Hallett,et al.  Impulse control disorders in Parkinson's disease: recent advances. , 2011, Current opinion in neurology.

[27]  Y. Shimo,et al.  Acute effects of bilateral subthalamic stimulation on decision-making in Parkinson's disease. , 2011, Parkinsonism & related disorders.

[28]  R. Aitken Measurement of feelings using visual analogue scales. , 1969, Proceedings of the Royal Society of Medicine.

[29]  H. Groenewegen The Basal Ganglia and Motor Control , 2003, Neural plasticity.

[30]  Guglielmo Foffani,et al.  Time dependent subthalamic local field potential changes after DBS surgery in Parkinson's disease , 2010, Experimental Neurology.

[31]  Annamaria Bianchi,et al.  Basal ganglia local field potentials: applications in the development of new deep brain stimulation devices for movement disorders , 2007, Expert review of medical devices.

[32]  Matteo Pizzorno,et al.  Using STN DBS and medication reduction as a strategy to treat pathological gambling in Parkinson's disease. , 2007, Parkinsonism & related disorders.

[33]  Y. Agid,et al.  Pathological gambling in Parkinson's disease improves on chronic subthalamic nucleus stimulation , 2006, Movement disorders : official journal of the Movement Disorder Society.

[34]  M. Potenza,et al.  Neuroscience of Behavioral and Pharmacological Treatments for Addictions , 2011, Neuron.

[35]  David Garcia-Garcia,et al.  Involvement of the subthalamic nucleus in impulse control disorders associated with Parkinson's disease. , 2011, Brain : a journal of neurology.

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

[37]  Michael J. Frank,et al.  Hold your horses: A dynamic computational role for the subthalamic nucleus in decision making , 2006, Neural Networks.

[38]  A. Lawrence,et al.  Dopamine dysregulation syndrome, impulse control disorders and punding after deep brain stimulation surgery for Parkinson’s disease , 2009, Journal of Clinical Neuroscience.

[39]  Claudio Lucchiari,et al.  Conflict-dependent dynamic of subthalamic nucleus oscillations during moral decisions , 2011, Social neuroscience.

[40]  T. Robinson,et al.  Subthalamic Nucleus Lesions Enhance the Psychomotor-Activating, Incentive Motivational, and Neurobiological Effects of Cocaine , 2005, The Journal of Neuroscience.

[41]  B. Averbeck,et al.  Risk and learning in impulsive and nonimpulsive patients with Parkinson's disease , 2010, Movement disorders : official journal of the Movement Disorder Society.

[42]  L. Wojtecki,et al.  Deep brain stimulation of the subthalamic nucleus transiently enhances loss-chasing behaviour in patients with Parkinson's Disease , 2011, Experimental Neurology.

[43]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

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

[45]  A. Priori,et al.  The Effects of Levodopa and Deep Brain Stimulation on Subthalamic Local Field Low-Frequency Oscillations in Parkinson's Disease , 2012, Neurosignals.

[46]  V. Tronnier,et al.  Subthalamic nucleus stimulation affects striato-anterior cingulate cortex circuit in a response conflict task: a PET study. , 2002, Brain : a journal of neurology.

[47]  Michael J. Frank,et al.  Hold Your Horses: Impulsivity, Deep Brain Stimulation, and Medication in Parkinsonism , 2007, Science.

[48]  M. Amalric,et al.  The subthalamic nucleus exerts opposite control on cocaine and 'natural' rewards , 2005, Nature Neuroscience.

[49]  A. Priori,et al.  Adaptive deep brain stimulation (aDBS) controlled by local field potential oscillations , 2013, Experimental Neurology.

[50]  Sara Marceglia,et al.  What neurophysiological recordings tell us about cognitive and behavioral functions of the human subthalamic nucleus , 2011, Expert review of neurotherapeutics.

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

[52]  J. Deakin,et al.  Effect of quinolinic acid-induced lesions of the subthalamic nucleus on performance on a progressive-ratio schedule of reinforcement: A quantitative analysis , 2008, Behavioural Brain Research.

[53]  Terry E Robinson,et al.  The Influence of Subthalamic Nucleus Lesions on Sign-Tracking to Stimuli Paired with Food and Drug Rewards: Facilitation of Incentive Salience Attribution? , 2008, Neuropsychopharmacology.

[54]  Sara Marceglia,et al.  Subthalamic Local Field Beta Oscillations during Ongoing Deep Brain Stimulation in Parkinson’s Disease in Hyperacute and Chronic Phases , 2011, Neurosignals.