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The Subthalamic Nucleus, Limbic Function, and Impulse Control

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Abstract

It has been well documented that deep brain stimulation (DBS) of the subthalamic nucleus (STN) to address some of the disabling motor symptoms of Parkinson’s disease (PD) can evoke unintended effects, especially on non-motor behavior. This observation has catalyzed more than a decade of research concentrated on establishing trends and identifying potential mechanisms for these non-motor effects. While many issues remain unresolved, the collective result of many research studies and clinical observations has been a general recognition of the role of the STN in mediating limbic function. In particular, the STN has been implicated in impulse control and the related construct of valence processing. A better understanding of STN involvement in these phenomena could have important implications for treating impulse control disorders (ICDs). ICDs affect up to 40% of PD patients on dopamine agonist therapy and approximately 15% of PD patients overall. ICDs have been reported to be associated with STN DBS. In this paper we will focus on impulse control and review pre-clinical, clinical, behavioral, imaging, and electrophysiological studies pertaining to the limbic function of the STN.

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References

  • Accolla, E. A., Dukart, J., Helms, G., Weiskopf, N., Kherif, F., Lutti, A., et al. (2014). Brain tissue properties differentiate between motor and limbic basal ganglia circuits. Human Brain Mapping, 35, 5083–5092.

    Article  PubMed Central  PubMed  Google Scholar 

  • Aleksandrova, L. R., Creed, M. C., Fletcher, P. J., Lobo, D. S. S., Hamani, C., & Nobrega, J. N. (2013). Deep brain stimulation of the subthalamic nucleus increases premature responding in a rat gambling task. Behavioural Brain Research, 245, 76–82.

    Article  PubMed  Google Scholar 

  • Alkemade, A., & Forstmann, B. U. (2014). Do we need to revise the tripartite subdivision hypothesis of the human subthalamic nucleus (STN)? NeuroImage, 95, 326–329.

    Article  PubMed  Google Scholar 

  • Alkemade A., Schnitzler A., Forstmann B. U. (2015). Topographic organization of the human and non-human primate subthalamic nucleus. Brain Struct. Funct.

  • Ardouin, C., Voon, V., Worbe, Y., Abouazar, N., Czernecki, V., Hosseini, H., et al. (2006). Pathological gambling in Parkinson’s disease improves on chronic subthalamic nucleus stimulation. Movement Disorders, 21, 1941–1946.

    Article  PubMed  Google Scholar 

  • Aron, A. R., Behrens, T. E., Smith, S., Frank, M. J., & Poldrack, R. A. (2007). Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 27, 3743–3752.

    Article  CAS  Google Scholar 

  • Balarajah, S., & Cavanna, A. E. (2013). The pathophysiology of impulse control disorders in Parkinson disease. Behavioural Neurology, 26, 237–244.

    Article  PubMed  Google Scholar 

  • Balasubramani, P. P., Chakravarthy, V. S., Ali, M., Ravindran, B., Moustafa, A. A. (2015). Identifying the Basal Ganglia Network Model Markers for Medication-Induced Impulsivity in Parkinson’s Disease Patients [Internet]. PLoS ONE 10[cited 2015 Aug 4] Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4456385/

  • Baláž, M., Bočková, M., Rektorová, I., & Rektor, I. (2011). Involvement of the subthalamic nucleus in cognitive functions -- a concept. Journal of Neurological Sciences, 310, 96–99.

    Article  Google Scholar 

  • Ballanger, B., van Eimeren, T., Moro, E., Lozano, A. M., Hamani, C., Boulinguez, P., et al. (2009). Stimulation of the subthalamic nucleus and impulsivity: release your horses. Annals of Neurology, 66, 817–824.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bari, A., & Robbins, T. W. (2013). Inhibition and impulsivity: behavioral and neural basis of response control. Progress in Neurobiology, 108, 44–79.

    Article  PubMed  Google Scholar 

  • Baunez, C., & Lardeux, S. (2011). Frontal cortex-like functions of the subthalamic nucleus. Frontiers in Systems Neuroscience, 5, 83.

    Article  PubMed Central  PubMed  Google Scholar 

  • Baunez, C., Nieoullon, A., & Amalric, M. (1995). In a rat model of parkinsonism, lesions of the subthalamic nucleus reverse increases of reaction time but induce a dramatic premature responding deficit. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 15, 6531–6541.

    CAS  Google Scholar 

  • Baunez, C., Amalric, M., & Robbins, T. W. (2002). Enhanced food-related motivation after bilateral lesions of the subthalamic nucleus. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 22, 562–568.

    CAS  Google Scholar 

  • Baunez, C., Dias, C., Cador, M., & Amalric, M. (2005). The subthalamic nucleus exerts opposite control on cocaine and ‘natural’ rewards. Nature Neuroscience, 8, 484–489.

    CAS  PubMed  Google Scholar 

  • Baunez, C., Christakou, A., Chudasama, Y., Forni, C., & Robbins, T. W. (2007). Bilateral high-frequency stimulation of the subthalamic nucleus on attentional performance: transient deleterious effects and enhanced motivation in both intact and parkinsonian rats. European Journal of Neuroscience, 25, 1187–1194.

    Article  PubMed Central  PubMed  Google Scholar 

  • Benedetti, F., Colloca, L., Lanotte, M., Bergamasco, B., Torre, E., & Lopiano, L. (2004). Autonomic and emotional responses to open and hidden stimulations of the human subthalamic region. Brain Research Bulletin, 63, 203–211.

    Article  PubMed  Google Scholar 

  • Bickel, S., Alvarez, L., Macias, R., Pavon, N., Leon, M., Fernandez, C., et al. (2010). Cognitive and neuropsychiatric effects of subthalamotomy for Parkinson’s disease. Parkinsonism & Related Disorders, 16, 535–539.

    Article  Google Scholar 

  • Boller, J. K., Barbe, M. T., Pauls, K. A. M., Reck, C., Brand, M., Maier, F., et al. (2014). Decision-making under risk is improved by both dopaminergic medication and subthalamic stimulation in Parkinson’s disease. Experimental Neurology, 254, 70–77.

    Article  PubMed  Google Scholar 

  • Borden, A., Wallon, D., Lefaucheur, R., Derrey, S., Fetter, D., Verin, M., et al. (2014). Does early verbal fluency decline after STN implantation predict long-term cognitive outcome after STN-DBS in Parkinson’s disease? Journal of Neurological Sciences, 346, 299–302.

    Article  Google Scholar 

  • Brandt, J., Rogerson, M., Al-Joudi, H., Reckess, G., Shpritz, B., Umeh, C. C., et al. (2015). Betting on DBS: Effects of subthalamic nucleus deep brain stimulation on risk taking and decision making in patients with Parkinson’s disease. Neuropsychology, 29, 622–631.

    Article  PubMed  Google Scholar 

  • Breysse, E., Pelloux, Y., Baunez, C. (2015). The Good and Bad Differentially Encoded within the Subthalamic Nucleus in Rats,, [Internet]. eNeuro; 2[cited 2015 Oct 26] Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4607759/

  • Brücke, C., Kupsch, A., Schneider, G.-H., Hariz, M. I., Nuttin, B., Kopp, U., et al. (2007). The subthalamic region is activated during valence-related emotional processing in patients with Parkinson’s disease. European Journal of Neuroscience, 26, 767–774.

    Article  PubMed  Google Scholar 

  • Brunenberg, E. J. L., Moeskops, P., Backes, W. H., Pollo, C., Cammoun, L., Vilanova, A., et al. (2012). Structural and resting state functional connectivity of the subthalamic nucleus: identification of motor STN parts and the hyperdirect pathway. PloS One, 7, e39061.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Buot, A., Welter, M.-L., Karachi, C., Pochon, J.-B., Bardinet, E., Yelnik, J., et al. (2013). Processing of emotional information in the human subthalamic nucleus. Journal of Neurology, Neurosurgery, and Psychiatry, 84, 1331–1338.

    Article  PubMed  Google Scholar 

  • Burbaud, P., Clair, A.-H., Langbour, N., Fernandez-Vidal, S., Goillandeau, M., Michelet, T., et al. (2013). Neuronal activity correlated with checking behaviour in the subthalamic nucleus of patients with obsessive-compulsive disorder. Brain: A Journal of Neurology, 136, 304–317.

    Article  Google Scholar 

  • Burrows, A. M., Ravin, P. D., Novak, P., Peters, M. L. B., Dessureau, B., Swearer, J., et al. (2012). Limbic and motor function comparison of deep brain stimulation of the zona incerta and subthalamic nucleus. Neurosurgery, 70, 125–130.

    Article  PubMed  Google Scholar 

  • Camacho-Abrego, I., Tellez-Merlo, G., Melo, A. I., Rodríguez-Moreno, A., Garcés, L., De La Cruz, F., et al. (2014). Rearrangement of the dendritic morphology of the neurons from prefrontal cortex and hippocampus after subthalamic lesion in Sprague–Dawley rats. Synapse (New York), 68, 114–126.

    Article  CAS  Google Scholar 

  • Cera, N., Bifolchetti, S., Martinotti, G., Gambi, F., Sepede, G., Onofrj, M., et al. (2014). Amantadine and cognitive flexibility: decision making in Parkinson’s patients with severe pathological gambling and other impulse control disorders. Neuropsychiatric Disease and Treatment, 10, 1093–1101.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chowdhury, R., Guitart-Masip, M., Lambert, C., Dolan, R. J., & Düzel, E. (2013). Structural integrity of the substantia nigra and subthalamic nucleus predicts flexibility of instrumental learning in older-age individuals. Neurobiology of Aging, 34, 2261–2270.

    Article  PubMed Central  PubMed  Google Scholar 

  • Coenen, V. A., Honey, C. R., Hurwitz, T., Rahman, A. A., McMaster, J., Bürgel, U., et al. (2009). Medial forebrain bundle stimulation as a pathophysiological mechanism for hypomania in subthalamic nucleus deep brain stimulation for Parkinson’s disease. Neurosurgery, 64, 1106–1114.

    Article  PubMed  Google Scholar 

  • Cools, R., Altamirano, L., & D’Esposito, M. (2006). Reversal learning in Parkinson’s disease depends on medication status and outcome valence. Neuropsychologia, 44, 1663–1673.

    Article  PubMed  Google Scholar 

  • Couto, M. I., Monteiro, A., Oliveira, A., Lunet, N., & Massano, J. (2014). Depression and anxiety following deep brain stimulation in Parkinson’s disease: systematic review and meta-analysis. Acta Médica Portuguesa, 27, 372–382.

    PubMed  Google Scholar 

  • Coxon, J. P., Impe, A. V., Wenderoth, N., & Swinnen, S. P. (2012). Aging and inhibitory control of action: cortico-subthalamic connection strength predicts stopping performance. Journal of Neuroscience, 32, 8401–8412.

    Article  CAS  PubMed  Google Scholar 

  • Darbaky, Y., Baunez, C., Arecchi, P., Legallet, E., & Apicella, P. (2005). Reward-related neuronal activity in the subthalamic nucleus of the monkey. Neuroreport, 16, 1241–1244.

    Article  PubMed  Google Scholar 

  • Demetriades, P., Rickards, H., Cavanna, A. E. (2011). Impulse Control Disorders Following Deep Brain Stimulation of the Subthalamic Nucleus in Parkinson’s Disease: Clinical Aspects [Internet]. Park. Dis. 2011; [cited 2015 Aug 4] Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3043299/

  • Desbonnet, L., Temel, Y., Visser-Vandewalle, V., Blokland, A., Hornikx, V., & Steinbusch, H. W. M. (2004). Premature responding following bilateral stimulation of the rat subthalamic nucleus is amplitude and frequency dependent. Brain Research, 1008, 198–204.

    Article  CAS  PubMed  Google Scholar 

  • Dick, D. M., Smith, G., Olausson, P., Mitchell, S. H., Leeman, R. F., O’Malley, S. S., et al. (2010). Understanding the construct of impulsivity and its relationship to alcohol use disorders. Addiction Biology, 15, 217–226.

    Article  PubMed Central  PubMed  Google Scholar 

  • Diergaarde, L., Pattij, T., Nawijn, L., Schoffelmeer, A. N. M., & De Vries, T. J. (2009). Trait impulsivity predicts escalation of sucrose seeking and hypersensitivity to sucrose-associated stimuli. Behavioral Neuroscience, 123, 794–803.

    Article  CAS  PubMed  Google Scholar 

  • Drapier, D., Drapier, S., Sauleau, P., Haegelen, C., Raoul, S., Biseul, I., et al. (2006). Does subthalamic nucleus stimulation induce apathy in Parkinson’s disease? Journal of Neurology, 253, 1083–1091.

    Article  CAS  PubMed  Google Scholar 

  • Eisenstein, S. A., Koller, J. M., Black, K. D., Campbell, M. C., Lugar, H. M., Ushe, M., et al. (2014). Functional anatomy of subthalamic nucleus stimulation in Parkinson disease. Annals of Neurology, 76, 279–295.

    Article  PubMed Central  PubMed  Google Scholar 

  • Eitan, R., Shamir, R. R., Linetsky, E., Rosenbluh, O., Moshel, S., Ben-Hur, T., et al. (2013). Asymmetric right/left encoding of emotions in the human subthalamic nucleus. Frontiers in Systems Neuroscience, 7, 69.

    Article  PubMed Central  PubMed  Google Scholar 

  • Espinosa-Parrilla, J.-F., Baunez, C., & Apicella, P. (2013). Linking reward processing to behavioral output: motor and motivational integration in the primate subthalamic nucleus. Frontiers in Computational Neuroscience, 7, 175.

    Article  PubMed Central  PubMed  Google Scholar 

  • Espinosa-Parrilla, J. F., Baunez, C., & Apicella, P. (2015). Modulation of neuronal activity by reward identity in the monkey subthalamic nucleus. European Journal of Neuroscience, 42, 1705–1717.

    Article  PubMed  Google Scholar 

  • Evens, R., Stankevich, Y., Dshemuchadse, M., Storch, A., Wolz, M., Reichmann, H., et al. (2015). The impact of Parkinson’s disease and subthalamic deep brain stimulation on reward processing. Neuropsychologia, 75, 11–19.

    Article  PubMed  Google Scholar 

  • Forstmann, B. U., Keuken, M. C., Jahfari, S., Bazin, P.-L., Neumann, J., Schäfer, A., et al. (2012). Cortico-subthalamic white matter tract strength predicts interindividual efficacy in stopping a motor response. NeuroImage, 60, 370–375.

    Article  PubMed  Google Scholar 

  • Frank, M. J. (2005). Dynamic dopamine modulation in the basal ganglia: a neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. Journal Cognitive Neuroscience, 17, 51–72.

    Article  Google Scholar 

  • Frank, M. J. (2006). Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Network Official Journal International Neural Networks Society, 19, 1120–1136.

    Article  Google Scholar 

  • Frank, M. J., & O’Reilly, R. C. (2006). A mechanistic account of striatal dopamine function in human cognition: psychopharmacological studies with cabergoline and haloperidol. Behavioral Neuroscience, 120, 497–517.

    Article  CAS  PubMed  Google Scholar 

  • Fukaya, C., & Yamamoto, T. (2015). Deep brain stimulation for Parkinson’s disease: recent trends and future direction. Neurologia Medico-Chirurgica (Tokyo), 55, 422–431.

    Article  Google Scholar 

  • Funkiewiez, A., Ardouin, C., Caputo, E., Krack, P., Fraix, V., Klinger, H., et al. (2004). Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 75, 834–839.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia-Ruiz, P. J., Martinez Castrillo, J. C., Alonso-Canovas, A., Herranz Barcenas, A., Vela, L., Sanchez Alonso, P., et al. (2014). Impulse control disorder in patients with Parkinson’s disease under dopamine agonist therapy: a multicentre study. Journal of Neurology, Neurosurgery, and Psychiatry, 85, 840–844.

    Article  PubMed  Google Scholar 

  • Gee, L., Smith, H., De La Cruz, P., Campbell, J., Fama, C., Haller, J., et al. (2015). The influence of bilateral subthalamic nucleus deep brain stimulation on impulsivity and prepulse inhibition in Parkinson’s disease patients. Stereotactic and Functional Neurosurgery, 93, 265–270.

    Article  PubMed  Google Scholar 

  • Greenhouse, I., Swann, N. C., Aron, A. R. (2011). Fronto-basal-ganglia circuits for stopping action [Internet]. Neural Basis Motiv. Cogn. Control; 189[cited 2015 Aug 5] Available from: http://books.google.com/books?hl=en&lr=&id=A_eoYgtLmFMC&oi=fnd&pg=PA189&dq=info:tSbAIu32TzcJ:scholar.google.com&ots=YdmRHP-rLW&sig=3BZtsfOcSmRKyoFxZ5PrkzpxD1c

  • Guitart-Masip, M., Duzel, E., Dolan, R., & Dayan, P. (2014). Action versus valence in decision making. Trends in Cognitive Sciences, 18, 194–202.

    Article  PubMed Central  PubMed  Google Scholar 

  • Gunduz, A., Morita, H., Rossi, P. J., Allen, W. L., Alterman, R. L., Bronte-Stewart, H., et al. Proceedings of the Second Annual Deep Brain Stimulation Think Tank: What’s in the Pipeline. Int. J. Neurosci. 2015: 1–11.

  • Hachem-Delaunay, S., Fournier, M.-L., Cohen, C., Bonneau, N., Cador, M., Baunez, C., et al. (2015). Subthalamic nucleus high-frequency stimulation modulates neuronal reactivity to cocaine within the reward circuit. Neurobiology of Disease, 80, 54–62.

    Article  CAS  PubMed  Google Scholar 

  • Haegelen, C., Verin, M., Broche, B. A., Prigent, F., Jannin, P., Gibaud, B., et al. (2005). Does subthalamic nucleus stimulation affect the frontal limbic areas? a single-photon emission computed tomography study using a manual anatomical segmentation method. Surgical and Radiologic Anatomy, 27, 389–394.

    Article  CAS  PubMed  Google Scholar 

  • Haegelen, C., Rouaud, T., Darnault, P., & Morandi, X. (2009). The subthalamic nucleus is a key-structure of limbic basal ganglia functions. Medical Hypotheses, 72, 421–426.

    Article  PubMed  Google Scholar 

  • Haynes, W. I. A., & Haber, S. N. (2013). The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for basal ganglia models and deep brain stimulation. Journal of Neuroscience, 33, 4804–4814.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hewig, J., Kretschmer, N., Trippe, R. H., Hecht, H., Coles, M. G. H., Holroyd, C. B., et al. (2010). Hypersensitivity to reward in problem gamblers. Biological Psychiatry, 67, 781–783.

    Article  PubMed  Google Scholar 

  • Hilker, R., Voges, J., Weisenbach, S., Kalbe, E., Burghaus, L., Ghaemi, M., et al. (2004). Subthalamic nucleus stimulation restores glucose metabolism in associative and limbic cortices and in cerebellum: evidence from a FDG-PET study in advanced Parkinson’s disease. Journal of Cerebral Blood Flow and Metabolism Official journal of the International Society for Cerebral Blood Flow and Metabolism, 24, 7–16.

    Article  CAS  Google Scholar 

  • Jahanshahi, M. (2013). Effects of deep brain stimulation of the subthalamic nucleus on inhibitory and executive control over prepotent responses in Parkinson’s disease. Frontiers in Systems Neuroscience, 7, 118.

    Article  PubMed Central  PubMed  Google Scholar 

  • Joel, D., & Weiner, I. (1997). The connections of the primate subthalamic nucleus: indirect pathways and the open-interconnected scheme of basal ganglia-thalamocortical circuitry. Brain Research. Brain Research Reviews, 23, 62–78.

    Article  CAS  PubMed  Google Scholar 

  • Kantak, K. M., Yager, L. M., & Brisotti, M. F. (2013). Impact of medial orbital cortex and medial subthalamic nucleus inactivation, individually and together, on the maintenance of cocaine self-administration behavior in rats. Behavioural Brain Research, 238, 1–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karachi, C., Yelnik, J., Tandé, D., Tremblay, L., Hirsch, E. C., & François, C. (2005). The pallidosubthalamic projection: an anatomical substrate for nonmotor functions of the subthalamic nucleus in primates. Movement Disorders Official Journal Movement Disorder Society, 20, 172–180.

    Article  Google Scholar 

  • Karachi, C., Grabli, D., Baup, N., Mounayar, S., Tandé, D., François, C., et al. (2009). Dysfunction of the subthalamic nucleus induces behavioral and movement disorders in monkeys. Movement Disorders Official Journal Movement Disorder Society, 24, 1183–1192.

    Article  Google Scholar 

  • Keuken, M. C., Bazin, P.-L., Schäfer, A., Neumann, J., Turner, R., & Forstmann, B. U. (2013). Ultra-high 7T MRI of structural age-related changes of the subthalamic nucleus. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 33, 4896–4900.

    Article  CAS  Google Scholar 

  • Kim, H.-J., Jeon, B. S., & Paek, S. H. (2015). Nonmotor symptoms and subthalamic deep brain stimulation in Parkinson’s disease. Journal Movement Disorders, 8, 83–91.

    Article  Google Scholar 

  • Klein, J., Winter, C., Coquery, N., Heinz, A., Morgenstern, R., Kupsch, A., et al. (2010). Lesion of the medial prefrontal cortex and the subthalamic nucleus selectively affect depression-like behavior in rats. Behavioural Brain Research, 213, 73–81.

    Article  PubMed  Google Scholar 

  • Knight, E. J., Testini, P., Min, H.-K., Gibson, W. S., Gorny, K. R., Favazza, C. P., et al. (2015). Motor and nonmotor circuitry activation induced by subthalamic nucleus deep brain stimulation in patients with Parkinson disease: intraoperative functional magnetic resonance imaging for deep brain stimulation. Mayo Clinic Proceedings, 90, 773–785.

    Article  PubMed  Google Scholar 

  • Kocka, A., & Gagnon, J. (2014). Definition of impulsivity and related terms following traumatic brain injury: a review of the different concepts and measures used to assess impulsivity, disinhibition and other related concepts. Behavioral Sciences (Basel Switzerland), 4, 352–370.

    Google Scholar 

  • Krack, P., Kumar, R., Ardouin, C., Dowsey, P. L., McVicker, J. M., Benabid, A. L., et al. (2001). Mirthful laughter induced by subthalamic nucleus stimulation. Movement Disorders Official Journal Movement Disorder Society, 16, 867–875.

    Article  CAS  Google Scholar 

  • Krack, P., Hariz, M. I., Baunez, C., Guridi, J., & Obeso, J. A. (2010). Deep brain stimulation: from neurology to psychiatry? Trends in Neurosciences, 33, 474–484.

    Article  CAS  PubMed  Google Scholar 

  • Kühn, A. A., Hariz, M. I., Silberstein, P., Tisch, S., Kupsch, A., Schneider, G.-H., et al. (2005). Activation of the subthalamic region during emotional processing in Parkinson disease. Neurology, 65, 707–713.

    Article  PubMed  Google Scholar 

  • Lambert, C., Zrinzo, L., Nagy, Z., Lutti, A., Hariz, M., Foltynie, T., et al. (2012). Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging. NeuroImage, 60, 83–94.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lanotte, M., Lopiano, L., Torre, E., Bergamasco, B., Colloca, L., & Benedetti, F. (2005). Expectation enhances autonomic responses to stimulation of the human subthalamic limbic region. Brain, Behavior, and Immunity, 19, 500–509.

    Article  PubMed  Google Scholar 

  • Lardeux, S., & Baunez, C. (2007). Alcohol preference influences the subthalamic nucleus control on motivation for alcohol in rats. Neuropsychopharmacology, 33, 634–642.

    Article  PubMed  Google Scholar 

  • Lardeux, S., Pernaud, R., Paleressompoulle, D., & Baunez, C. (2009). Beyond the reward pathway: coding reward magnitude and error in the rat subthalamic nucleus. Journal of Neurophysiology, 102, 2526–2537.

    Article  PubMed  Google Scholar 

  • Lardeux, S., Paleressompoulle, D., Pernaud, R., Cador, M., & Baunez, C. (2013). Different populations of subthalamic neurons encode cocaine vs. sucrose reward and predict future error. Journal of Neurophysiology, 110, 1497–1510.

    Article  CAS  PubMed  Google Scholar 

  • Le Jeune, F., Péron, J., Biseul, I., Fournier, S., Sauleau, P., Drapier, S., et al. (2008). Subthalamic nucleus stimulation affects orbitofrontal cortex in facial emotion recognition: a PET study. Brain: A Journal of Neurology, 131, 1599–1608.

    Article  Google Scholar 

  • Le Jeune, F., Péron, J., Grandjean, D., Drapier, S., Haegelen, C., Garin, E., et al. (2010). Subthalamic nucleus stimulation affects limbic and associative circuits: a PET study. European Journal of Nuclear Medicine and Molecular Imaging, 37, 1512–1520.

    Article  PubMed  Google Scholar 

  • Leicht, G., Troschütz, S., Andreou, C., Karamatskos, E., Ertl, M., Naber, D., et al. (2013). Relationship between oscillatory neuronal activity during reward processing and trait impulsivity and sensation seeking. PloS One, 8, e83414.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Łęski, S., Lindén, H., Tetzlaff, T., Pettersen, K. H., Einevoll, G. T. (2013). Frequency Dependence of Signal Power and Spatial Reach of the Local Field Potential [Internet]. PLoS Comput. Biol.; 9[cited 2015 Nov 5] Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3715549/

  • Lévesque, J.-C., & Parent, A. (2005). GABAergic interneurons in human subthalamic nucleus. Movement Disorders Official Journal Movement Disorder Society, 20, 574–584.

    Article  Google Scholar 

  • Mallet, L., Mesnage, V., Houeto, J.-L., Pelissolo, A., Yelnik, J., Behar, C., et al. (2002). Compulsions, Parkinson’s disease, and stimulation. Lancet (London, England), 360, 1302–1304.

    Article  Google Scholar 

  • Mallet, L., Schüpbach, M., N’Diaye, K., Remy, P., Bardinet, E., Czernecki, V., et al. (2007). Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior. Proceedings of the National Academy of Sciences of the United States of America, 104, 10661–10666.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marceglia, S., Fumagalli, M., & Priori, A. (2011). What neurophysiological recordings tell us about cognitive and behavioral functions of the human subthalamic nucleus. Expert Review of Neurotherapeutics, 11, 139–149.

    Article  PubMed  Google Scholar 

  • Morris, L. S., Kundu, P., Baek, K., Irvine, M. A., Mechelmans, D. J., Wood, J., et al. (2015) Jumping the Gun: Mapping Neural Correlates of Waiting Impulsivity and Relevance Across Alcohol Misuse. Biol. Psychiatry.

  • Mosley, P. E., & Marsh, R. (2015). The psychiatric and neuropsychiatric symptoms after subthalamic stimulation for Parkinson’s disease. Journal of Neuropsychiatry and Clinical Neurosciences, 27, 19–26.

    Article  PubMed  Google Scholar 

  • Moum, S. J., Price, C. C., Limotai, N., Oyama, G., Ward, H., Jacobson, C., et al. (2012). Effects of STN and GPi deep brain stimulation on impulse control disorders and dopamine dysregulation syndrome. PloS One, 7, e29768.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mulder, M. J., Boekel, W., Ratcliff, R., & Forstmann, B. U. (2014). Cortico-subthalamic connection predicts individual differences in value-driven choice bias. Brain Structure and Function, 219, 1239–1249.

    Article  PubMed Central  PubMed  Google Scholar 

  • Oberg, S. A. K., Christie, G. J., & Tata, M. S. (2011). Problem gamblers exhibit reward hypersensitivity in medial frontal cortex during gambling. Neuropsychologia, 49, 3768–3775.

    Article  PubMed  Google Scholar 

  • Okai, D., Samuel, M., Askey-Jones, S., David, A. S., & Brown, R. G. (2011). Impulse control disorders and dopamine dysregulation in Parkinson’s disease: a broader conceptual framework. European Journal of Neurology Official Journal European Federation Neurology Society, 18, 1379–1383.

    CAS  Google Scholar 

  • Park, H. K., Kim, H.-J., Kim, S. J., Kim, J. S., Shin, H.-W., & Kim, J. S. (2011). From Jekyll to Hyde after limbic subthalamic nucleus infarction. Neurology, 77, 82–84.

    Article  CAS  PubMed  Google Scholar 

  • Péron, J., Grandjean, D., Le Jeune, F., Sauleau, P., Haegelen, C., Drapier, D., et al. (2010). Recognition of emotional prosody is altered after subthalamic nucleus deep brain stimulation in Parkinson’s disease. Neuropsychologia, 48, 1053–1062.

    Article  PubMed  Google Scholar 

  • Piray, P., Zeighami, Y., Bahrami, F., Eissa, A. M., Hewedi, D. H., & Moustafa, A. A. (2014). Impulse control disorders in Parkinson’s disease are associated with dysfunction in stimulus valuation but not action valuation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 34, 7814–7824.

    Article  CAS  Google Scholar 

  • Plessow, F., Fischer, R., Volkmann, J., & Schubert, T. (2014). Subthalamic deep brain stimulation restores automatic response activation and increases susceptibility to impulsive behavior in patients with Parkinson’s disease. Brain and Cognition, 87, 16–21.

    Article  PubMed  Google Scholar 

  • Rektor, I., Bočková, M., Chrastina, J., Rektorová, I., Baláž, M. (2014). The modulatory role of subthalamic nucleus in cognitive functions - A viewpoint. Clin. Neurophysiol. Off. J. Int. Fed. Clin. Neurophysiol.

  • Rodriguez-Oroz, M. C., López-Azcárate, J., Garcia-Garcia, D., Alegre, M., Toledo, J., Valencia, M., et al. (2011). Involvement of the subthalamic nucleus in impulse control disorders associated with Parkinson’s disease. Brain: A Journal of Neurology, 134, 36–49.

    Article  Google Scholar 

  • Rodriguez-Oroz, M. C., Moro, E., & Krack, P. (2012). Long-term outcomes of surgical therapies for Parkinson’s disease. Movement Disorders, 27, 1718–1728.

    Article  PubMed  Google Scholar 

  • Rouaud, T., Lardeux, S., Panayotis, N., Paleressompoulle, D., Cador, M., & Baunez, C. (2010). Reducing the desire for cocaine with subthalamic nucleus deep brain stimulation. Proceedings of the National Academy of Sciences of the United States of America, 107, 1196–1200.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Santangelo, G., Barone, P., Trojano, L., & Vitale, C. (2013). Pathological gambling in Parkinson’s disease. A comprehensive review. Parkinsonism & Related Disorders, 19, 645–653.

    Article  Google Scholar 

  • Sauleau, P., Raoul, S., Lallement, F., Rivier, I., Drapier, S., Lajat, Y., et al. (2005). Motor and non motor effects during intraoperative subthalamic stimulation for Parkinson’s disease. Journal of Neurology, 252, 457–464.

    Article  PubMed  Google Scholar 

  • Sensi, M., Eleopra, R., Cavallo, M. A., Sette, E., Milani, P., Quatrale, R., et al. (2004). Explosive-aggressive behavior related to bilateral subthalamic stimulation. Parkinsonism & Related Disorders, 10, 247–251.

    Article  CAS  Google Scholar 

  • Sestini, S., di Scotto Luzio, A., Ammannati, F., De Cristofaro, M. T. R., Passeri, A., Martini, S., et al. (2002). Changes in regional cerebral blood flow caused by deep-brain stimulation of the subthalamic nucleus in Parkinson’s disease. Journal of Nuclear Medicine Official Publisher Society of Nuclear Medicine, 43, 725–732.

    Google Scholar 

  • Shapiro, M. B., Vaillancourt, D. E., Sturman, M. M., Metman, L. V., Bakay, R. A. E., & Corcos, D. M. (2007). Effects of STN DBS on rigidity in Parkinson’s disease. IEEE Transactions on Neural Systems and Rehabilitation Engineering Publisher: IEEE Engineering in Medicine and Biology Society, 15, 173–181.

    Article  Google Scholar 

  • Tan, S. K. H., Temel, Y., Blokland, A., Steinbusch, H. W. M., & Visser-Vandewalle, V. (2006). The subthalamic nucleus: from response selection to execution. Journal of Chemical Neuroanatomy, 31, 155–161.

    Article  PubMed  Google Scholar 

  • Tandé, D., Féger, J., Hirsch, E. C., & François, C. (2006). Parafascicular nucleus projection to the extrastriatal basal ganglia in monkeys. Neuroreport, 17, 277–280.

    Article  PubMed  Google Scholar 

  • Teagarden, M. A., & Rebec, G. V. (2007). Subthalamic and striatal neurons concurrently process motor, limbic, and associative information in rats performing an operant task. Journal of Neurophysiology, 97, 2042–2058.

    Article  PubMed  Google Scholar 

  • Temel, Y., Blokland, A., Steinbusch, H. W. M., & Visser-Vandewalle, V. (2005). The functional role of the subthalamic nucleus in cognitive and limbic circuits. Progress in Neurobiology, 76, 393–413.

    Article  CAS  PubMed  Google Scholar 

  • Temel, Y., Kessels, A., Tan, S., Topdag, A., Boon, P., & Visser-Vandewalle, V. (2006). Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. Parkinsonism & Related Disorders, 12, 265–272.

    Article  Google Scholar 

  • Trottenberg, T., Kupsch, A., Schneider, G.-H., Brown, P., & Kühn, A. A. (2007). Frequency-dependent distribution of local field potential activity within the subthalamic nucleus in Parkinson’s disease. Experimental Neurology, 205, 287–291.

    Article  PubMed  Google Scholar 

  • Tsai, S. T., Lin, S. H., Lin. S. Z., Chen, J. Y., Lee, C. W., Chen. S. Y. (2007) Neuropsychological effects after chronic subthalamic stimulation and the topography of the nucleus in Parkinson’s disease. Neurosurgery 61, E1024–1029; discussion E1029–1030.

  • Turner, M. S., Lavin, A., Grace, A. A., & Napier, T. C. (2001). Regulation of limbic information outflow by the subthalamic nucleus: excitatory amino acid projections to the ventral pallidum. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 21, 2820–2832.

    CAS  Google Scholar 

  • Vesper, J., Klostermann, F., Stockhammer, F., Funk, T., & Brock, M. (2002). Results of chronic subthalamic nucleus stimulation for Parkinson’s disease: a 1-year follow-up study. Surgical Neurology, 57, 306–311. discussion 311–313.

    Article  CAS  PubMed  Google Scholar 

  • Volkmann, J., Daniels, C., & Witt, K. (2010). Neuropsychiatric effects of subthalamic neurostimulation in Parkinson disease. Nature Reviews Neurology, 6, 487–498.

    CAS  PubMed  Google Scholar 

  • Wagenbreth, C., Zaehle, T., Galazky, I., Voges, J., Guitart-Masip, M., Heinze, H.-J., et al. (2015). Deep brain stimulation of the subthalamic nucleus modulates reward processing and action selection in Parkinson patients. Journal of Neurology, 262, 1541–1547.

    Article  PubMed  Google Scholar 

  • Welter, M.-L., Burbaud, P., Fernandez-Vidal, S., Bardinet, E., Coste, J., Piallat, B., et al. (2011). Basal ganglia dysfunction in OCD: subthalamic neuronal activity correlates with symptoms severity and predicts high-frequency stimulation efficacy. Transcultural Psychiatry, 1, e5.

    Article  CAS  Google Scholar 

  • Williams, N. R., Foote, K. D., & Okun, M. S. (2014). STN vs. GPi deep brain stimulation: translating the rematch into clinical practice. Movement Disorders-Clinical Practice, 1, 24–35.

    Article  PubMed Central  PubMed  Google Scholar 

  • Winstanley, C. A., Baunez, C., Theobald, D. E. H., & Robbins, T. W. (2005). Lesions to the subthalamic nucleus decrease impulsive choice but impair autoshaping in rats: the importance of the basal ganglia in Pavlovian conditioning and impulse control. European Journal of Neuroscience, 21, 3107–3116.

    Article  PubMed  Google Scholar 

  • Winter, C., Lemke, C., Sohr, R., Meissner, W., Harnack, D., Juckel, G., et al. (2008). High frequency stimulation of the subthalamic nucleus modulates neurotransmission in limbic brain regions of the rat. Experimental Brain Research, 185, 497–507.

    Article  PubMed  Google Scholar 

  • Wylie, S. A., Ridderinkhof, K. R., Elias, W. J., Frysinger, R. C., Bashore, T. R., Downs, K. E., et al. (2010). Subthalamic nucleus stimulation influences expression and suppression of impulsive behaviour in Parkinson’s disease. Brain, 133, 3611–3624.

    Article  PubMed Central  PubMed  Google Scholar 

  • York, M. K., Wilde, E. A., Simpson, R., & Jankovic, J. (2009). Relationship between neuropsychological outcome and DBS surgical trajectory and electrode location. Journal of Neurological Sciences, 287, 159–171.

    Article  Google Scholar 

  • Zavala, B., Zaghloul, K., & Brown, P. (2015). The subthalamic nucleus, oscillations, and conflict. Movement Disorders-Clinical Practice, 30, 328–338.

    Article  Google Scholar 

  • Zhang, G., Zhang, Z., Liu, L., Yang, J., Huang, J., Xiong, N., et al. (2014). Impulsive and compulsive behaviors in Parkinson’s disease. Frontiers in Aging Neuroscience, 6, 318.

    PubMed Central  PubMed  Google Scholar 

  • Zijlstra, F., Veltman, D. J., Booij, J., van den Brink, W., & Franken, I. H. A. (2009). Neurobiological substrates of cue-elicited craving and anhedonia in recently abstinent opioid-dependent males. Drug and Alcohol Dependence, 99, 183–192.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Center for Movement Disorders and Neurorestoration, University of Florida, Gainesville, FL, USA

    P. Justin Rossi & Michael S. Okun

  2. Department of Neurology, University of Florida College of Medicine, HSC Box 100236, Gainesville, FL, 32610-0236, USA

    P. Justin Rossi

  3. J. Crayton Pruitt Family Department of Biomedical Engineering, University of Florida, Gainesville, FL, USA

    Aysegul Gunduz

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Rossi, P.J., Gunduz, A. & Okun, M.S. The Subthalamic Nucleus, Limbic Function, and Impulse Control. Neuropsychol Rev 25, 398–410 (2015). https://doi.org/10.1007/s11065-015-9306-9

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