Functional neurosurgery for movement disorders: a historical perspective.

Since the 1960s, deep brain stimulation and spinal cord stimulation at low frequency (30 Hz) have been used to treat intractable pain of various origins. For this purpose, specific hardware have been designed, including deep brain electrodes, extensions, and implantable programmable generators (IPGs). In the meantime, movement disorders, and particularly parkinsonian and essential tremors, were treated by electrolytic or mechanic lesions in various targets of the basal ganglia, particularly in the thalamus and in the internal pallidum. The advent in the 1960s of levodopa, as well as the side effects and complications of ablative surgery (e.g., thalamotomy and pallidotomy), has sent functional neurosurgery of movement disorders to oblivion. In 1987, the serendipitous discovery of the effect of high-frequency stimulation (HFS), mimicking lesions, allowed the revival of the surgery of movement disorders by stimulation of the thalamus, which treated tremors with limited morbidity, and adaptable and reversible results. The stability along time of these effects allowed extending it to new targets suggested by basic research in monkeys. The HFS of the subthalamic nucleus (STN) has profoundly challenged the practice of functional surgery as the effect on the triad of dopaminergic symptoms was very significant, allowing to decrease the drug dosage and therefore a decrease of their complications, the levodopa-induced dyskinesias. In the meantime, based on the results of previous basic research in various fields, HFS has been progressively extended to potentially treat epilepsy and, more recently, psychiatric disorders, such as obsessive-compulsive disorders, Gilles de la Tourette tics, and severe depression. Similarly, suggested by the observation of changes in PET scan, applications have been extended to cluster headaches by stimulation of the posterior hypothalamus and even more recently, to obesity and drug addiction. In the field of movement disorders, it has become clear that STN stimulation is not efficient on the nondopaminergic symptoms such as freezing of gait. Based on experimental data obtained in MPTP-treated parkinsonian monkeys, the pedunculopontine nucleus has been used as a new target, and as suggested by the animal research results, its use indeed improves walking and stability when stimulation is performed at low frequency (25 Hz). The concept of simultaneous stimulation of multiple targets eventually at low or high frequency, and that of several electrodes in one target, is being accepted to increase the efficiency. This leads to and is being facilitated by the development of new hardware (multiple-channel IPGs, specific electrodes, rechargeable batteries). Still additional efforts are needed at the level of the stimulation paradigm and in the waveform. The recent development of nanotechnologies allows the design of totally new systems expanding the field of deep brain stimulation. These new techniques will make it possible to not only inhibit or excite deep brain structures to alleviate abnormal symptoms but also open the field for the use of recording cortical activities to drive neuroprostheses through brain-computer interfaces. The new field of compensation of deficits will then become part of the field of functional neurosurgery.

[1]  Antonio Daniele,et al.  Transient mania with hypersexuality after surgery for high frequency stimulation of the subthalamic nucleus in Parkinson's disease , 2002, Movement disorders : official journal of the Movement Disorder Society.

[2]  D. Hansel,et al.  Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. , 2005, Brain : a journal of neurology.

[3]  S. Gill,et al.  Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson's disease , 2005, Neuroreport.

[4]  D. Brooks,et al.  Direct brain infusion of glial cell line–derived neurotrophic factor in Parkinson disease , 2003, Nature Medicine.

[5]  P. Stanzione,et al.  Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. , 2007, Brain : a journal of neurology.

[6]  G. Deuschl,et al.  Subthalamic nucleus deep brain stimulation: Summary and meta‐analysis of outcomes , 2006, Movement disorders : official journal of the Movement Disorder Society.

[7]  A. Benabid,et al.  Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[8]  Haruhiko Kishima,et al.  Functional Recovery in a Primate Model of Parkinson's Disease following Motor Cortex Stimulation , 2004, Neuron.

[9]  A. Benabid,et al.  Survival of midbrain dopaminergic cells after lesion or deep brain stimulation of the subthalamic nucleus in MPTP-treated monkeys. , 2007, Brain : a journal of neurology.

[10]  A. Benabid,et al.  Effect of subthalamic nucleus stimulation on levodopa-induced dyskinesia in Parkinson’s disease , 2000, Neurology.

[11]  Brigitte Piallat,et al.  A putative generalized model of the effects and mechanism of action of high frequency electrical stimulation of the central nervous system. , 2005, Acta neurologica Belgica.

[12]  P. Stanzione,et al.  Implantation of human pedunculopontine nucleus: a safe and clinically relevant target in Parkinson's disease , 2005, Neuroreport.

[13]  Y. Kajita,et al.  Long-term stimulation of the subthalamic nucleus in hemiparkinsonian rats: neuroprotection of dopaminergic neurons. , 2004, Journal of neurosurgery.

[14]  A. Benabid,et al.  Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. , 1996, Journal of neurosurgery.

[15]  J. Dostrovsky,et al.  Stimulation-induced inhibition of neuronal firing in human subthalamic nucleus , 2004, Experimental Brain Research.

[16]  Bettina Schrader,et al.  Manic episode with psychotic symptoms induced by subthalamic nucleus stimulation in a patient with Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[17]  C. Hammond,et al.  Latest view on the mechanism of action of deep brain stimulation , 2008, Movement disorders : official journal of the Movement Disorder Society.

[18]  H. Steinbusch,et al.  Protection of nigral cell death by bilateral subthalamic nucleus stimulation , 2006, Brain Research.

[19]  A. Benabid,et al.  Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. , 1987, Applied neurophysiology.

[20]  A. Benabid,et al.  Improvement of levodopa induced dyskinesias by thalamic deep brain stimulation is related to slight variation in electrode placement: possible involvement of the centre median and parafascicularis complex , 1999, Journal of neurology, neurosurgery, and psychiatry.

[21]  A. Benabid,et al.  Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus , 1991, The Lancet.

[22]  R. Bakay,et al.  Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2–neurturin) to patients with idiopathic Parkinson's disease: an open-label, phase I trial , 2008, The Lancet Neurology.

[23]  P. Brundin,et al.  From bench to bed: the potential of stem cells for the treatment of Parkinson’s disease , 2007, Cell and Tissue Research.

[24]  G. Deuschl,et al.  A randomized trial of deep-brain stimulation for Parkinson's disease. , 2006, The New England journal of medicine.

[25]  M. Hariz,et al.  Leksell's posteroventral pallidotomy in the treatment of Parkinson's disease. , 1992, Journal of neurosurgery.

[26]  Clement Hamani,et al.  Bilateral Subthalamic Nucleus Stimulation for Parkinson's Disease: A Systematic Review of the Clinical Literature , 2005, Neurosurgery.

[27]  A. Benabid,et al.  Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. , 2003, The New England journal of medicine.

[28]  Christian Hauptmann,et al.  Therapeutic modulation of synaptic connectivity with desynchronizing brain stimulation. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[29]  Rajesh Pahwa,et al.  Efficacy of unilateral deep brain stimulation of the vim nucleus of the thalamus for essential head tremor , 1999, Movement disorders : official journal of the Movement Disorder Society.

[30]  Y Agid,et al.  Transient acute depression induced by high-frequency deep-brain stimulation. , 1999, The New England journal of medicine.

[31]  A. Benabid,et al.  Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease , 2009, The Lancet Neurology.

[32]  L. Schiffer,et al.  Aromatic amino acids and modification of parkinsonism. , 1967, The New England journal of medicine.

[33]  Paul Krack,et al.  Mirthful laughter induced by subthalamic nucleus stimulation , 2001, Movement disorders : official journal of the Movement Disorder Society.

[34]  Clement Hamani,et al.  Hardware-Related Complications of Deep Brain Stimulation: A Review of the Published Literature , 2006, Stereotactic and Functional Neurosurgery.

[35]  T. Itakura,et al.  Ablation of the subthalamic nucleus supports the survival of nigral dopaminergic neurons after nigrostriatal lesions induced by the mitochondrial toxin 3‐nitropropionic acid , 1999, Annals of neurology.

[36]  A. Carlsson,et al.  3,4-Dihydroxyphenylalanine and 5-Hydroxytryptophan as Reserpine Antagonists , 1957, Nature.

[37]  I. S. Cooper Ligation of the anterior choroidal artery for involuntary movements-parkinsonism , 1953, The Psychiatric quarterly.

[38]  M. Álvarez-Vega,et al.  Complications in subthalamic nucleus stimulation surgery for treatment of Parkinson’s disease. Review of 272 procedures , 2007, Acta Neurochirurgica.

[39]  L. Metman,et al.  Deep brain stimulation for Parkinson's disease: Prevalence of adverse events and need for standardized reporting , 2008, Movement disorders : official journal of the Movement Disorder Society.

[40]  David Eidelberg,et al.  Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial , 2007, The Lancet.

[41]  O. Hornykiewicz,et al.  Distribution of noradrenaline and dopamine (3-hydroxytyramine) in the human brain and their behavior in diseases of the extrapyramidal system. , 1960, Parkinsonism & related disorders.

[42]  J. Stein,et al.  The role of the pedunculopontine region in basal-ganglia mechanisms of akinesia , 1999, Experimental Brain Research.

[43]  A. Benabid,et al.  Chronic stimulation of subthalamic nucleus improves levodopa-induced dyskinesias in Parkinson's disease , 1997, The Lancet.

[44]  M. Hariz,et al.  Hardware-related complications of deep brain stimulation: a ten year experience , 2005, Acta Neurochirurgica.

[45]  Y. Agid,et al.  Effects of high-frequency stimulation on subthalamic neuronal activity in parkinsonian patients. , 2004, Archives of neurology.

[46]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[47]  R HASSLER,et al.  Physiological observations in stereotaxic operations in extrapyramidal motor disturbances. , 1960, Brain : a journal of neurology.

[48]  S. Canavero,et al.  Extradural cortical stimulation for movement disorders. , 2007, Acta neurochirurgica. Supplement.

[49]  A. Benabid,et al.  Subthalamic Nucleus Lesion in Rats Prevents Dopaminergic Nigral Neuron Degeneration After Striatal 6‐OHDA Injection: Behavioural and Immunohistochemical Studies , 1996, The European journal of neuroscience.

[50]  I. S. Cooper An investigation of neurosurgical alleviation of parkinsonism, chorea, athetosis and dystonia. , 1956, Annals of internal medicine.

[51]  G. Deuschl,et al.  Pallidal deep-brain stimulation in primary generalized or segmental dystonia. , 2006, The New England journal of medicine.

[52]  A. Benabid,et al.  Alteration of hormone and neurotransmitter production in cultured cells by high and low frequency electrical stimulation , 2006, Acta Neurochirurgica.

[53]  E. Bézard,et al.  Electrophysiological and metabolic evidence that high‐frequency stimulation of the subthalamic nucleus bridles neuronal activity in the subthalamic nucleus and the substantia nigra reticulata , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[54]  A. Bentivoglio,et al.  Results by motor cortex stimulation in treatment of focal dystonia, Parkinson's disease and post-ictal spasticity. The experience of the Italian Study Group of the Italian Neurosurgical Society. , 2008, Acta neurochirurgica. Supplement.