Biomarkers for closed-loop deep brain stimulation in Parkinson disease and beyond (original) (raw)

• Limousin, P. et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N. Engl. J. Med. 339, 1105–1111 (1998).
  Article CAS PubMed Google Scholar
• Dayal, V., Limousin, P. & Foltynie, T. Subthalamic nucleus deep brain stimulation in Parkinson’s disease: the effect of varying stimulation parameters. J. Parkinsons Dis. 7, 235–245 (2017).
  Article PubMed PubMed Central Google Scholar
• Castrioto, A., Lhommée, E., Moro, E. & Krack, P. Mood and behavioural effects of subthalamic stimulation in Parkinson’s disease. Lancet Neurol. 13, 287–305 (2014).
  Article PubMed Google Scholar
• Hatsopoulos, N. G. & Donoghue, J. P. The science of neural interface systems. Annu. Rev. Neurosci. 32, 249–266 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Arlotti, M. et al. Eight-hours adaptive deep brain stimulation in patients with Parkinson disease. Neurology 90, e971–e976 (2018).
  Article PubMed PubMed Central Google Scholar
• Vansteensel, M. J. et al. Fully implanted brain–computer interface in a locked-in patient with ALS. N. Engl. J. Med. 375, 2060–2066 (2016).
  Article PubMed PubMed Central Google Scholar
• Hoang, K. B., Cassar, I. R., Grill, W. M. & Turner, D. A. Biomarkers and stimulation algorithms for adaptive brain stimulation. Front. Neurosci. 11, 117–115 (2017).
  Article Google Scholar
• Hebb, A. O. et al. Creating the feedback loop: closed-loop neurostimulation. Neurosurg. Clin. North Am. 25, 187–204 (2014).
  Article Google Scholar
• Chaudhary, U., Birbaumer, N. & Ramos-Murguialday, A. Brain–computer interfaces for communication and rehabilitation. Nat. Rev. Neurol. 12, 513–525 (2016).
  Article PubMed Google Scholar
• Ajiboye, A. B. et al. Restoration of reaching and grasping movements through brain-controlled muscle stimulation in a person with tetraplegia: a proof-of-concept demonstration. Lancet 389, 1821–1830 (2017).
  Article PubMed PubMed Central Google Scholar
• Slutzky, M. W. & Flint, R. D. Physiological properties of brain–machine interface input signals. J. Neurophysiol. 118, 1329–1343 (2017).
  Article PubMed PubMed Central Google Scholar
• Hariz, M. Twenty-five years of deep brain stimulation: celebrations and apprehensions. Mov. Disord. 27, 930–933 (2012).
  Article PubMed Google Scholar
• Clausen, J. et al. Help, hope, and hype: ethical dimensions of neuroprosthetics. Science 356, 1338–1339 (2017).
  Article CAS PubMed Google Scholar
• Hariz, M., Blomstedt, P. & Zrinzo, L. Future of brain stimulation: new targets, new indications, new technology. Mov. Disord. 28, 1784–1792 (2013).
  Article PubMed Google Scholar
• Yuste, R. et al. Four ethical priorities for neurotechnologies and AI. Nature 551, 159–163 (2017).
  Article CAS PubMed PubMed Central Google Scholar
• Lipsman, N., Mendelsohn, D., Taira, T. & Bernstein, M. The contemporary practice of psychiatric surgery: results from a survey of North American functional neurosurgeons. Stereotact. Funct. Neurosurg. 89, 103–110 (2011).
  Article PubMed Google Scholar
• Baumeister, A. The Tulane electrical brain stimulation program: a historical case study in medical ethics. J. Hist. Neurosci. 9, 262–278 (2000).
  Article CAS PubMed Google Scholar
• Hariz, M. I., Blomstedt, P. & Zrinzo, L. Deep brain stimulation between 1947 and 1987: the untold story. Neurosurg. Focus 29, E1 (2010).
  Article PubMed Google Scholar
• Lüscher, C. Dark past of deep-brain stimulation. Nature 555, 306–307 (2018).
  Article CAS PubMed Google Scholar
• Hochberg, L. R. et al. Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 485, 372–375 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Oswal, A., Brown, P. & Litvak, V. Synchronized neural oscillations and the pathophysiology of Parkinson’s disease. Curr. Opin. Neurol. 26, 662–670 (2013).
  Article PubMed Google Scholar
• Birbaumer, N., Elbert, T., Canavan, A. G. M. & Rockstroh, B. Slow potentials of the cerebral cortex and behavior. Physiol. Rev. 70, 1–41 (1990).
  Article CAS PubMed Google Scholar
• Pfurtscheller, G. & da Silva, F. L. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin. Neurophysiol. 110, 1842–1857 (1999).
  Article CAS PubMed Google Scholar
• Cheyne, D. O. MEG studies of sensorimotor rhythms: a review. Exp. Neurol. 245, 27–39 (2013).
  Article PubMed Google Scholar
• Hammond, C., Bergman, H. & Brown, P. Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci. 30, 357–364 (2007).
  Article CAS PubMed Google Scholar
• Bergman, H. et al. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. 21, 32–38 (1998).
  Article CAS PubMed Google Scholar
• Neumann, W.-J. et al. Long term correlation of subthalamic beta band activity with motor impairment in patients with Parkinson’s disease. Clin. Neurophysiol. 128, 2286–2291 (2017).
  Article PubMed PubMed Central Google Scholar
• Whitmer, D. et al. High frequency deep brain stimulation attenuates subthalamic and cortical rhythms in Parkinson’s disease. Front. Hum. Neurosci. 6, 155 (2012).
  Article PubMed PubMed Central Google Scholar
• Blumenfeld, Z. et al. Sixty-Hertz stimulation improves bradykinesia and amplifies subthalamic low-frequency oscillations. Mov. Disord. 32, 80–88 (2016).
  Article PubMed Google Scholar
• Tinkhauser, G. et al. Directional local field potentials: a tool to optimize deep brain stimulation. Mov. Disord. 33, 159–164 (2017).
  Article PubMed PubMed Central Google Scholar
• Brittain, J.-S. & Brown, P. Oscillations and the basal ganglia: motor control and beyond. Neuroimage 85, 637–647 (2014).
  Article PubMed Google Scholar
• Miller, K. J. et al. Human motor cortical activity is selectively phase-entrained on underlying rhythms. PLOS Comput. Biol. 8, e1002655 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Rosin, B. et al. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron 72, 370–384 (2011).
  Article CAS PubMed Google Scholar
• Little, S. et al. Adaptive deep brain stimulation in advanced Parkinson disease. Ann. Neurol. 74, 449–457 (2013).
  Article PubMed PubMed Central Google Scholar
• Little, S. et al. Bilateral adaptive deep brain stimulation is effective in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 87, 717–721 (2015).
  Article PubMed Google Scholar
• Little, S. et al. Adaptive deep brain stimulation for Parkinson’s disease demonstrates reduced speech side effects compared to conventional stimulation in the acute setting. J. Neurol. Neurosurg. Psychiatry 87, 1388–1389 (2016).
  Article PubMed Google Scholar
• Rosa, M. et al. Adaptive deep brain stimulation in a freely moving parkinsonian patient. Mov. Disord. 30, 1003–1005 (2015).
  Article PubMed PubMed Central Google Scholar
• Rosa, M. et al. Adaptive deep brain stimulation controls levodopa-induced side effects in parkinsonian patients. Mov. Disord. 32, 628–629 (2017).
  Article PubMed PubMed Central Google Scholar
• Daneshzand, M., Faezipour, M. & Barkana, B. D. Robust desynchronization of Parkinson’s disease pathological oscillations by frequency modulation of delayed feedback deep brain stimulation. PLOS ONE 13, e0207761 (2018).
  Article PubMed PubMed Central CAS Google Scholar
• Rappel, P. et al. Subthalamic theta activity: a novel human subcortical biomarker for obsessive compulsive disorder. Transl Psychiatry 8, 252 (2018).
  Article Google Scholar
• Feingold, J., Gibson, D. J., DePasquale, B. & Graybiel, A. M. Bursts of beta oscillation differentiate postperformance activity in the striatum and motor cortex of monkeys performing movement tasks. Proc. Natl Acad. Sci. USA 112, 13687–13692 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Tinkhauser, G. et al. Beta burst dynamics in Parkinson’s disease OFF and ON dopaminergic medication. Brain 140, 2968–2981 (2017).
  Article PubMed Google Scholar
• Tinkhauser, G. et al. The modulatory effect of adaptive deep brain stimulation on beta bursts in Parkinson’s disease. Brain 140, 1053–1067 (2017).
  Article PubMed PubMed Central Google Scholar
• Torrecillos, F. et al. Modulation of beta bursts in the subthalamic nucleus predicts motor performance. J. Neurosci. 38, 8905–8917 (2018).
  Article CAS PubMed PubMed Central Google Scholar
• de Hemptinne, C. et al. Exaggerated phase–amplitude coupling in the primary motor cortex in Parkinson disease. Proc. Natl Acad. Sci. USA 10, 4780–4785 (2013).
  Article Google Scholar
• Swann, N. C. et al. Elevated synchrony in Parkinson disease detected with electroencephalography. Ann. Neurol. 78, 742–750 (2015).
  Article PubMed PubMed Central Google Scholar
• de Hemptinne, C. et al. Therapeutic deep brain stimulation reduces cortical phase-amplitude coupling in Parkinson’s disease. Nat. Neurosci. 18, 779–786 (2015).
  Article PubMed PubMed Central CAS Google Scholar
• Swann, N. C. et al. Gamma oscillations in the hyperkinetic state detected with chronic human brain recordings in Parkinson’s disease. J. Neurosci. 36, 6445–6458 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Swann, N. C. et al. Adaptive deep brain stimulation for Parkinson’s disease using motor cortex sensing. J. Neural Eng. 15, 046006 (2018).
  Article PubMed PubMed Central Google Scholar
• Cagnan, H., Kühn, A. A. & Brown, P. Co-modulation of finely tuned high-gamma band activity across hemispheres in Parkinson’s disease. Clin. Neurophysiol. 125, 777–785 (2014).
  Article PubMed PubMed Central Google Scholar
• Cagnan, H. et al. Stimulating at the right time: phase-specific deep brain stimulation. Brain 140, 132–145 (2017).
  Article PubMed Google Scholar
• Malekmohammadi, M. et al. Kinematic adaptive deep brain stimulation for resting tremor in Parkinson’s disease. Mov. Disord. 31, 426–428 (2016).
  Article PubMed Google Scholar
• Houston, B. C., Thompson, M. C., Ojemann, J. G., Ko, A. L. & Chizeck, H. J. in 8th Int. IEEE/EMBS Conf. on Neural Engineering 316–320 (IEEE, 2017).
• Shah, S. A., Tinkhauser, G., Chen, C. C., Little, S. & Brown, P. Parkinsonian tremor detection from subthalamic nucleus local field potentials for closed-loop deep brain stimulation. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2018, 2320–2324 (2018).
  PubMed Central Google Scholar
• Krack, P. et al. Mirthful laughter induced by subthalamic nucleus stimulation. Mov. Disord. 16, 867–875 (2001).
  Article CAS PubMed Google Scholar
• Eusebio, A. et al. Subthalamic nucleus stimulation and compulsive use of dopaminergic medication in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 84, 868–874 (2013).
  Article PubMed Google Scholar
• Lhommee, E. et al. Subthalamic stimulation in Parkinson’s disease: restoring the balance of motivated behaviours. Brain 135, 1463–1477 (2012).
  Article PubMed Google Scholar
• Lhommée, E. et al. Behavioural outcomes of subthalamic stimulation and medical therapy versus medical therapy alone for Parkinson’s disease with early motor complications (EARLYSTIM trial): secondary analysis of an open-label randomised trial. Lancet Neurol. 17, 223–231 (2018).
  Article PubMed Google Scholar
• Jahanshahi, M., Obeso, I., Baunez, C., Alegre, M. & Krack, P. Parkinson’s disease, the subthalamic nucleus, inhibition, and impulsivity. Mov. Disord. 30, 128–140 (2014).
  Article PubMed Google Scholar
• Polosan, M. et al. Affective modulation of the associative-limbic subthalamic nucleus: deep brain stimulation in obsessive–compulsive disorder. Transl Psychiatry 9, 896 (2019).
  Article Google Scholar
• Pagonabarraga, J., Kulisevsky, J., Strafella, A. & Krack, P. Apathy in Parkinson’s disease: clinical features, neural substrates, diagnosis, and treatment. Lancet Neurol. 14, 518–531 (2015).
  Article PubMed Google Scholar
• Weintraub, D. & Burn, D. J. Parkinson’s disease: the quintessential neuropsychiatric disorder. Mov. Disord. 26, 1022–1031 (2011).
  Article PubMed PubMed Central Google Scholar
• Martinez-Fernandez, R., Schmitt, E., Martinez-Martin, P. & Krack, P. The hidden sister of motor fluctuations in Parkinson’s disease: a review on nonmotor fluctuations. Mov. Disord. 31, 1080–1094 (2016).
  Article CAS PubMed Google Scholar
• Béreau, M. et al. Hyperdopaminergic behavioral spectrum in Parkinson’s disease: a review. Rev. Neurol. (Paris) 174, 653–663 (2018).
  Article Google Scholar
• Eitan, R. et al. Asymmetric right/left encoding of emotions in the human subthalamic nucleus. Front. Syst. Neurosci. 7, 69 (2013).
  Article PubMed PubMed Central Google Scholar
• Kuhn, A. A. et al. Activation of the subthalamic region during emotional processing in Parkinson disease. Neurology 65, 707–713 (2005).
  Article CAS PubMed Google Scholar
• Huebl, J. et al. Oscillatory subthalamic nucleus activity is modulated by dopamine during emotional processing in Parkinson’s disease. Cortex 60, 69–81 (2014).
  Article PubMed Google Scholar
• Schmitt, E. et al. The neuropsychiatric fluctuations scale for Parkinson’s disease: a pilot study. Mov. Disord. Clin. Pract. 5, 265–272 (2018).
  Article PubMed PubMed Central Google Scholar
• Rodriguez-Oroz, M. C. et al. Involvement of the subthalamic nucleus in impulse control disorders associated with Parkinson’s disease. Brain 134, 36–49 (2011).
  Article PubMed Google Scholar
• Pelloux, Y. et al. Subthalamic nucleus high frequency stimulation prevents and reverses escalated cocaine use. Mol. Psychiatry 21, 1033 (2018).
  Google Scholar
• Delpont, B. et al. Psychostimulant effect of dopaminergic treatment and addictions in Parkinson’s disease. Mov. Disord. 8, 464–468 (2017).
  Google Scholar
• Canali, P. et al. Shared reduction of oscillatory natural frequencies in bipolar disorder, major depressive disorder and schizophrenia. J. Affect. Disord. 184, 111–115 (2015).
  Article PubMed Google Scholar
• Avanzino, L., Pelosin, E., Martino, D. & Abbruzzese, G. Motor timing deficits in sequential movements in Parkinson disease are related to action planning: a motor imagery study. PLOS ONE 8, e75454 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Aron, A. R., Herz, D. M., Brown, P., Forstmann, B. U. & Zaghloul, K. Frontosubthalamic circuits for control of action and cognition. J. Neurosci. 36, 11489–11495 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Bour, L. J. et al. Directional recording of subthalamic spectral power densities in Parkinson’s disease and the effect of steering deep brain stimulation. Brain Stimul. 8, 730–741 (2015).
  Article CAS PubMed Google Scholar
• Trager, M. H. et al. Subthalamic beta oscillations are attenuated after withdrawal of chronic high frequency neurostimulation in Parkinson’s disease. Neurobiol. Dis. 96, 22–30 (2016).
  Article PubMed Google Scholar
• Swann, N. C. et al. Chronic multisite brain recordings from a totally implantable bidirectional neural interface: experience in 5 patients with Parkinson’s disease. J. Neurosurg. 128, 605–616 (2018).
  Article PubMed Google Scholar
• Meidahl, A. C. et al. Adaptive deep brain stimulation for movement disorders: the long road to clinical therapy. Mov. Disord. 32, 810–819 (2017).
  Article PubMed PubMed Central Google Scholar
• Sani, O. G. et al. Mood variations decoded from multi-site intracranial human brain activity. Nat. Biotechnol. 156, 675 (2018).
  Google Scholar
• Mallet, L. et al. Subthalamic nucleus stimulation in severe obsessive–compulsive disorder. N. Engl. J. Med. 359, 2121–2134 (2008).
  Article CAS PubMed Google Scholar
• Mallet, L. et al. Compulsions, Parkinson’s disease, and stimulation. Lancet 360, 1302–1304 (2002).
  Article PubMed Google Scholar
• Schlaepfer, T. E. Deep brain stimulation for major depression — steps on a long and winding road. Biol. Psychiatry 78, 218–219 (2015).
  Article PubMed Google Scholar
• Menzies, L. et al. Integrating evidence from neuroimaging and neuropsychological studies of obsessive–compulsive disorder: the orbitofronto-striatal model revisited. Neurosci. Biobehav. Rev. 32, 525–549 (2008).
  Article PubMed Google Scholar
• Houeto, J. L. Tourette’s syndrome and deep brain stimulation. J. Neurol. Neurosurg. Psychiatry 76, 992–995 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Robertson, M. M. et al. Gilles de la Tourette syndrome. Nat. Rev. Dis. Primers 3, 16097 (2017).
  Article PubMed Google Scholar
• Shahed, J., Poysky, J., Kenney, C., Simpson, R. & Jankovic, J. GPi deep brain stimulation for Tourette syndrome improves tics and psychiatric comorbidities. Neurology 68, 159–160 (2007).
  Article CAS PubMed Google Scholar
• Welter, M.-L. et al. Internal pallidal and thalamic stimulation in patients with Tourette syndrome. Arch. Neurol. 65, 952–957 (2008).
  Article PubMed Google Scholar
• Zhang, C. et al. Pallidal deep brain stimulation combined with capsulotomy for Tourette’s syndrome with psychiatric comorbidity. J. Neurosurg. 4, 1–9 (2019).
  CAS Google Scholar
• Martinez-Ramirez, D. et al. Efficacy and safety of deep brain stimulation in Tourette syndrome. JAMA Neurol. 75, 353 (2018).
  Article PubMed PubMed Central Google Scholar
• Neumann, W.-J. et al. Pallidal and thalamic neural oscillatory patterns in Tourette’s syndrome. Ann. Neurol. 84, 505–514 (2018).
  Article PubMed Google Scholar
• Neumann, W.-J. et al. Toward electrophysiology-based intelligent adaptive deep brain stimulation for movement disorders. Neurotherapeutics 16, 105–118 (2019).
  Article PubMed PubMed Central Google Scholar
• Molina, R. et al. Report of a patient undergoing chronic responsive deep brain stimulation for Tourette syndrome: proof of concept. J. Neurosurg. 129, 308–314 (2018).
  Article PubMed Google Scholar
• Mayberg, H. S. et al. Deep brain stimulation for treatment-resistant depression. Neuron 45, 651–660 (2005).
  Article CAS PubMed Google Scholar
• Lozano, A. M. et al. Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol. Psychiatry 64, 461–467 (2008).
  Article PubMed Google Scholar
• Puigdemont, D. et al. A randomized double-blind crossover trial of deep brain stimulation of the subcallosal cingulate gyrus in patients with treatment-resistant depression: a pilot study of relapse prevention. J. Psychiatry Neurosci. 40, 224–231 (2015).
  Article PubMed PubMed Central Google Scholar
• Holtzheimer, P. E. et al. Subcallosal cingulate deep brain stimulation for treatment-resistant depression: a multisite, randomised, sham-controlled trial. Lancet Psychiatry 4, 839–849 (2017).
  Article PubMed Google Scholar
• Neumann, W.-J. et al. Different patterns of local field potentials from limbic DBS targets in patients with major depressive and obsessive compulsive disorder. Mol. Psychiatry 19, 1186–1192 (2014).
  Article PubMed PubMed Central Google Scholar
• Widge, A. S., Malone, D. A. Jr & Dougherty, D. D. Closing the loop on deep brain stimulation for treatment-resistant depression. Front. Neurosci. 12, 640 (2018).
  Article Google Scholar
• Smart, O. et al. Initial unilateral exposure to deep brain stimulation in treatment-resistant depression patients alters spectral power in the subcallosal cingulate. Front. Comput. Neurosci. 12, 1764–1713 (2018).
  Article Google Scholar
• Schlaepfer, T. E., Bewernick, B. H., Kayser, S., Hurlemann, R. & Coenen, V. A. Deep brain stimulation of the human reward system for major depression — rationale, outcomes and outlook. Neuropsychopharmacology 39, 1303–1314 (2014).
  Article PubMed PubMed Central Google Scholar
• Coenen, V. A. et al. The medial forebrain bundle as a target for deep brain stimulation for obsessive-compulsive disorder. CNS Spectr. 22, 282–289 (2016).
  Article PubMed Google Scholar
• Coenen, V. A. et al. Medial forebrain bundle stimulation as a pathophysiological mechanism for hypomania in subthalamic nucleus deep brain stimulation for Parkinson’s disease. Neurosurgery 64, 1106–1115 (2009).
  Article PubMed Google Scholar
• Kulisevsky, J. et al. Mania following deep brain stimulation for Parkinson’s disease. Neurology 59, 1421–1424 (2002).
  Article CAS PubMed Google Scholar
• Romito, L. M. et al. Transient mania with hypersexuality after surgery for high frequency stimulation of the subthalamic nucleus in Parkinson’s disease. Mov. Disord. 17, 1371–1374 (2002).
  Article PubMed Google Scholar
• Herzog, J. et al. Manic episode with psychotic symptoms induced by subthalamic nucleus stimulation in a patient with Parkinson’s disease. Mov. Disord. 18, 1382–1384 (2003).
  Article PubMed Google Scholar
• Schlaepfer, T. E., Bewernick, B. H., Kayser, S., Mädler, B. & Coenen, V. A. Rapid effects of deep brain stimulation for treatment-resistant major depression. Biol. Psychiatry 73, 1204–1212 (2013).
  Article PubMed Google Scholar
• Torres-Sanchez, S., Perez-Caballero, L. & Berrocoso, E. Cellular and molecular mechanisms triggered by deep brain stimulation in depression: a preclinical and clinical approach. Prog. Neuropsychopharmacol. Biol. Psychiatry 73, 1–10 (2017).
  Article CAS PubMed Google Scholar
• Schlaepfer, T. E. et al. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 33, 368–377 (2007).
  Article PubMed Google Scholar
• Coenen, V. A. et al. Tractography-assisted deep brain stimulation of the superolateral branch of the medial forebrain bundle (slMFB DBS) in major depression. Neuroimage Clin. 20, 580–593 (2018).
  Article PubMed PubMed Central Google Scholar
• Mallet, L. et al. Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior. Proc. Natl Acad. Sci. USA 104, 10661–10666 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Bewernick, B. H. et al. Deep brain stimulation to the medial forebrain bundle for depression- long-term outcomes and a novel data analysis strategy. Brain Stimul. 10, 664–671 (2017).
  Article PubMed Google Scholar
• Hamani, C. et al. Memory enhancement induced by hypothalamic/fornix deep brain stimulation. Ann. Neurol. 63, 119–123 (2008).
  Article PubMed Google Scholar
• Mirzadeh, Z., Bari, A. & Lozano, A. M. The rationale for deep brain stimulation in Alzheimer’s disease. J. Neural Transm. 123, 775–783 (2015).
  Article PubMed CAS Google Scholar
• Leoutsakos, J.-M. S. et al. Deep brain stimulation targeting the fornix for mild Alzheimer dementia (the ADvance trial): a two year follow-up including results of delayed activation. J. Alzheimers Dis. 64, 597–606 (2018).
  Article PubMed PubMed Central Google Scholar
• Kandel, E. R. The biology of memory: a forty-year perspective. J. Neurosci. 29, 12748–12756 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Rowland, N. C. et al. Task-related activity in sensorimotor cortex in Parkinson’s disease and essential tremor: changes in beta and gamma bands. Front. Hum. Neurosci. 9, 512 (2015).
  Article PubMed PubMed Central Google Scholar
• Nelson, A. B. et al. Beta oscillatory changes and retention of motor skills during practice in healthy subjects and in patients with Parkinson’s disease. Front. Hum. Neurosci. 11, 104 (2017).
  Article PubMed PubMed Central Google Scholar
• Heinrichs-Graham, E. et al. Neuromagnetic evidence of abnormal movement-related beta desynchronization in Parkinson’s disease. Cereb. Cortex 24, 2669–2678 (2013).
  Article PubMed PubMed Central Google Scholar
• Beck, M. H. et al. Short- and long-term dopamine depletion causes enhanced beta oscillations in the cortico-basal ganglia loop of parkinsonian rats. Exp. Neurol. 286, 124–136 (2016).
  Article CAS PubMed Google Scholar
• Wichmann, T., Bergman, H. & DeLong, M. R. Basal ganglia, movement disorders and deep brain stimulation: advances made through non-human primate research. J. Neural Transm. 125, 419–430 (2018).
  Article PubMed Google Scholar
• MacQueen, D. A., Young, J. W. & Cope, Z. A. in Biomarkers in Psychiatry (Current Topics in Behavioral Neurosciences) Vol. 40 (eds Pratt, J. & Hall, J.) 111–166 (Springer, 2018).
• Ahmari, S. E. Using mice to model obsessive compulsive disorder: from genes to circuits. Neuroscience 321, 121–137 (2016).
  Article CAS PubMed Google Scholar
• Lüscher, C. The emergence of a circuit model for addiction. Annu. Rev. Neurosci. 39, 257–276 (2016).
  Article PubMed CAS Google Scholar
• Pascoli, V. et al. Stochastic synaptic plasticity underlying compulsion in a model of addiction. Nature 564, 366–371 (2018).
  Article CAS PubMed Google Scholar
• Kato, T., Kasahara, T., Kubota-Sakashita, M., Kato, T. M. & Nakajima, K. Animal models of recurrent or bipolar depression. Neuroscience 321, 189–196 (2016).
  Article CAS PubMed Google Scholar
• Ménard, C., Hodes, G. E. & Russo, S. J. Pathogenesis of depression: insights from human and rodent studies. Neuroscience 321, 138–162 (2016).
  Article PubMed CAS Google Scholar
• Engel, A. K., Moll, C. K. E., Fried, I. & Ojemann, G. A. Invasive recordings from the human brain: clinical insights and beyond. Nat. Rev. Neurosci. 6, 35–47 (2005).
  Article CAS PubMed Google Scholar
• Pandarinath, C. et al. High performance communication by people with paralysis using an intracortical brain-computer interface. eLife 6, e18554 (2017).
  Article PubMed PubMed Central Google Scholar
• Winestone, J. S., Zaidel, A., Bergman, H. & Israel, Z. The use of macroelectrodes in recording cellular spiking activity. J. Neurosci. Methods 206, 34–39 (2012).
  Article PubMed Google Scholar
• Benis, D. et al. Response inhibition rapidly increases single-neuron responses in the subthalamic nucleus of patients with Parkinson’s disease. Cortex 84, 111–123 (2016).
  Article PubMed Google Scholar
• Pötter-Nerger, M. et al. Movement-related activity of human subthalamic neurons during a reach-to-grasp task. Front. Hum. Neurosci. 11, 436 (2017).
  Article PubMed PubMed Central Google Scholar
• Burbaud, P. et al. Neuronal activity correlated with checking behaviour in the subthalamic nucleus of patients with obsessive–compulsive disorder. Brain 136, 304–317 (2013).
  Article PubMed Google Scholar
• Creed, M., Pascoli, V. & Lüscher, C. Refining deep brain stimulation to emulate optogenetic treatment of synaptic pathology. Science 347, 659–664 (2015).
  Article CAS PubMed Google Scholar
• Wu, X. H., Song, J. J., Faull, R. L. M. & Waldvogel, H. J. GABAA and GABAB receptor subunit localization on neurochemically identified neurons of the human subthalamic nucleus. J. Comp. Neurol. 526, 803–823 (2018).
  Article CAS PubMed Google Scholar
• Arber, S. & Costa, R. M. Connecting neuronal circuits for movement. Science 360, 1403–1404 (2018).
  Article CAS PubMed Google Scholar
• Daneshzand, M., Faezipour, M. & Barkana, B. D. Computational stimulation of the basal ganglia neurons with cost effective delayed gaussian waveforms. Front. Comput. Neurosci. 11, 73 (2017).
  Article PubMed PubMed Central Google Scholar
• Lüscher, C., Pascoli, V. & Creed, M. Optogenetic dissection of neural circuitry: from synaptic causalities to blue prints for novel treatments of behavioral diseases. Curr. Opin. Neurobiol. 35, 95–100 (2015).
  Article PubMed CAS Google Scholar
• Lo, M.-C. & Widge, A. S. Closed-loop neuromodulation systems: next-generation treatments for psychiatric illness. Int. Rev. Psychiatry 29, 191–204 (2017).
  Article PubMed PubMed Central Google Scholar
• Buot, A. et al. Processing of emotional information in the human subthalamic nucleus. J. Neurol. Neurosurg. Psychiatry 84, 1331–1338 (2013).
  Article PubMed Google Scholar
• Péron, J. et al. Vocal emotion decoding in the subthalamic nucleus: an intracranial ERP study in Parkinson’s disease. Brain Lang. 168, 1–11 (2017).
  Article PubMed Google Scholar
• Bastin, J. et al. Changes of oscillatory activity in the subthalamic nucleus during obsessive-compulsive disorder symptoms: two case reports. Cortex 60, 145–150 (2014).
  Article PubMed Google Scholar
• Smith, G. S. et al. Increased cerebral metabolism after 1 year of deep brain stimulation in Alzheimer disease. Arch. Neurol. 69, 1141–1148 (2012).
  Article PubMed Google Scholar