The autonomic effects of deep brain stimulation-a therapeutic opportunity

Nature Reviews Neurology

Volumn 8, Issue 7, 2012, Pages 391-400

  Hyam, Jonathan A ^a   Kringelbach, Morten L ^a   Silburn, Peter A ^b   Aziz, Tipu Z ^a   Green, Alexander L ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ASTHMA; AUTONOMIC NERVOUS SYSTEM; BLOOD PRESSURE REGULATION; BLOOD PRESSURE VARIABILITY; BRAIN DEPTH STIMULATION; CARDIOVASCULAR FUNCTION; CHRONIC PAIN; DYSAUTONOMIA; DYSTONIA; EFFERENT NERVE; ELECTRODE; ESSENTIAL TREMOR; HEART RATE; HEART RATE VARIABILITY; HUMAN; LUNG FUNCTION; MICTURITION; MOTOR DYSFUNCTION; NEUROMODULATION; NONHUMAN; ORTHOSTATIC HYPOTENSION; PARKINSON DISEASE; PERIAQUEDUCTAL GRAY MATTER; POSTERIOR HYPOTHALAMUS; PRESSORECEPTOR; PRIORITY JOURNAL; RESPIRATION CONTROL; REVIEW; SENSORY NERVE; SUBTHALAMIC NUCLEUS; THERAPY EFFECT;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; AUTONOMIC NERVOUS SYSTEM DISEASES; BRAIN DISEASES; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; DEEP BRAIN STIMULATION; HUMANS; NEURAL PATHWAYS; RESPIRATION;

EID: 84863716511     PISSN: 17594758     EISSN: 17594766     Source Type: Journal    
DOI: 10.1038/nrneurol.2012.100     Document Type: Review

References (107)

1. Gildenberg, P. L. Stereotactic functional neurosurgery. Evolution of neuromodulation. Neuromodulation 83, 71-79 (2005).
2. Benabid, A. L. et al. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337, 403-406 (1991).
3. Benabid, A. L. et al. Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J. Neurosurg. 84, 203-214 (1996).
4. Bittar, R. G. et al. Deep brain stimulation for movement disorders and pain. J. Clin. Neurosci. 12, 457-463 (2005).
5. Koller, W. C., Lyons, K. E., Wilkinson, S. B. & Pahwa, R. Efficacy of unilateral deep brain stimulation of the VIM nucleus of the thalamus for essential head tremor. Mov. Disord. 14, 847-850 (1999).
6. Krack, P. et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N. Engl. J. Med. 349, 1925-1934 (2003).
7. Marchand, S., Kupers, R. C., Bushnell, M. C. & Duncan, G. H. Analgesic and placebo effects of thalamic stimulation. Pain 105, 481-488 (2003).
8. Owen, S. L., Green, A. L., Stein, J. F. & Aziz, T. Z. Deep brain stimulation for the alleviation of post-stroke neuropathic pain. Pain 120, 202-206 (2006).
9. Lozano, A. M. et al. Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol. Psychiatry 64, 461-467 (2008).
10. Pereira, E. A., Green, A. L, Nandi, D. & Aziz, T. Z. Deep brain stimulation: indications and evidence. Expert Rev. Med. Devices 5, 591-603 (2007).
11. Goldstein, D., Eisenhofer, G., Robertson, D., Straus, R. & Esler, M. Dysautonomias: clinical disorders of the autonomic nervous system. Ann. Intern. Med. 137, 753-763 (2002).
12. Goldstein, D. S. Dysautonomia in Parkinson's disease: neurocardiological abnormalities. Lancet Neurol. 2, 669-676 (2003).
13. Barnes, P. J. Is asthma a nervous disease? Chest 3, 119S-125S (1995).
14. Hammond, C., Amir, R., Bioulac, B., & Garcia, L. Latest view on the mechanism of action of deep brain stimulation. Mov. Disord. 23, 2111-2121 (2008).
15. Gradinaru, V., Mogri, M., Thompson, K. R., Henderson, J. M. & Deisseroth, K. Optical deconstruction of parkinsonian neural circuitry. Science 17, 354-359 (2009).
16. McIntyre, C. C. & Hahn, P. J. Network perspectives on the mechanisms of deep brain stimulation. Neurobiol. Dis. 38, 329-337 (2010).
17. Kringelbach, M. L., Green, A. L. & Aziz, T. Z. Balancing the brain: resting state networks and deep brain stimulation. Front. Integr. Neurosci. 5, 1-5 (2011).
18. Hamani, C., Saint-Cyr, J. A., Fraser, J., Kaplitt, M. & Lozano, A. M. The subthalamic nucleus in the context of movement disorders. Brain 127, 4-20 (2004).
19. Hashimoto, T., Elder, C. M., Okun, M. S., Patrick, S. K. & Vitek, J. L. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J. Neurosci. 23, 1916-1923 (2003).
20. Carter, H. H. et al. Deep brain stimulation of the periaqueductal grey induces vasodilation in humans. Hypertension 57, e24-e25 (2011).
21. Cortelli, P. et al. Effect of deep brain stimulation of the posterior hypothalamic area on the cardiovascular system in chronic cluster headache patients. Eur. J. Neurol. 14, 1008-1015 (2007).
22. Green, A. L. et al. Deep brain stimulation can regulate arterial blood pressure in awake humans. Neuroreport 16, 1741-1745 (2005).
23. Kabat, H., Magoun, H. W. & Ranson, S. W. Electrical stimulation of points in the forebrain and midbrain. The resultant alteration in blood pressure. Arch. Neurol. Psychiatry 34, 931-955 (1935).
24. Hyam, J. A. et al. Controlling the lungs via the brain: a novel neurosurgical method to improve lung function in humans. Neurosurgery 70, 469-477 (2012).
25. Pereira, E. A., Wang, S., Paterson, D. J., Stein, J. F. & Aziz, T. Z. Sustained reduction of hypertension by deep brain stimulation. J. Clin. Neurosci. 1, 124-127 (2010).
26. Thornton, J. M. et al. Identification of higher brain centres that may encode the cardiorespiratory response to exercise in humans. J. Physiol. 3, 823-836 (2001).
27. Thornton, J. M., Aziz, T. Z., Schlugman, D. & Paterson, D. J. Electrical stimulation of the midbrain increases heart rate and arterial blood pressure in awake humans. J. Physiol. 539, 615-621 (2002).
28. Green, A. L. et al. Identifying cardiorespiratory neurocircuitry involved in central command during exercise in humans. J. Physiol. 2, 605-612 (2007).
29. Green, A. L. & Paterson, D. J. Identification of neurocircuitry controlling cardiovascular function in humans using functional neurosurgery: implications for exercise control. Exp. Physiol. 9, 1022-1028 (2008).
30. Williamson, J. W., Fadel, P. J. & Mitchell, J. H. New insights into central cardiovascular control during exercise in humans: a central command update. Exp. Physiol. 1, 51-58 (2006).
31. Benarroch, E. E. Central Autonomic Network: Functional Organization and Clinical Correlations 29-60 (Futura Publishing Company Inc, Armonk, New York, 1997)
32. Loewy, A. D. Forebrain nuclei involved in autonomic control. Prog. Brain Res. 87, 253-268 (1991).
33. Janig, W. & Habler, J. H. Neurophysiological analysis of target-related sympathetic pathways-from animal to human: similarities and differences. Acta Physiol. Scand. 524, 279-292 (2000).
34. Lovick, T. A. Integrated activity of cardiovascular and pain regulatory systems: role in adaptive behavioural responses. Prog. Neurobiol. 5, 631-644 (1993).
35. Dampney, R. A. Functional organization of central pathways regulating the cardiovascular system. Physiol. Rev. 74, 323-364 (1994).
36. Dampney, R. A. et al. Central mechanisms underlying short-and long-term regulation of the cardiovascular system. Clin. Exp. Pharmacol. Physiol. 29, 261-268 (2002).
37. Ross, C. A. et al. Tonic vasomotor control by the rostral ventrolateral medulla: effect of electrical or chemical stimulation of the area containing C1 adrenaline neurons on arterial pressure, heart rate, and plasma catecholamines and vasopressin. J. Neurosci. 4, 474-494 (1984).
38. Wieling, W. & Karemaker, J. M. Measurement of heart rate and blood pressure to evaluate disturbances in neurocardiovascular control. In Autonomic Failure: a Textbook of Clinical Disorders of the Autonomic Nervous System 4th edn Ch. 21 (eds Mathias, C. & Bannister, R.) 196-210 (Oxford University Press, Oxford, 2001).
39. Goodwin, G. M., McCloskey, D. I. & Mitchell, J. H. Cardiovascular and respiratory responses to changes in central command during isometric exercise at a constant muscle tension. J. Physiol. 226, 173-190 (1972).
40. Krogh, A. & Lindhard, J. The regulation of respiration and circulation during the initial stages of muscular work. J. Physiol. 47, 112-136 (2008).
41. Critchley, H. D., Corfield, D. R., Chandler, P., Mathias, C. J. & Dolan, R. J. Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans. J. Physiol. 1, 259-270 (2000).
42. Williamson, J. W. et al. Hypnotic manipulation of effort sense during dynamic exercise: cardiovascular responses and brain activation. J. Appl. Physiol. 90, 1392-1399 (2001).
43. Williamson, J. W. et al. Brain activation by central command during actual and imagined handgrip under hypnosis. J. Appl. Physiol. 92, 1317-1324 (2002).
44. Williamson, J. W., McColl, R. & Mathews, D. Evidence for central command activation of the human insular cortex during exercise. J. Appl. Physiol.94, 1726-1734 (2003).
45. Hamani, C., Saint-Cyr, J. A., Fraser, J., Kaplitt, M. & Lozano, A. M. The subthalamic nucleus in the context of movement disorders. Brain 127, 4-20 (2004).
46. Joel, D. & Weiner, I. The connections of the primate subthalamic nucleus: indirect pathways and the open-interconnected scheme of basal ganglia-thalamocortical circuitry. Brain Res. Brain Res. Rev. 23, 62-78 (1997).
47. Parent, A. & Hazrati, L. N. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res. Brain Res. Rev. 20, 128-154 (1995).
48. Shink, E., Bevan, M. D., Bolam, J. P. & Smith, Y. The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey. Neuroscience 73, 335-357 (1996).
49. Sauleau, P. et al. Motor and non motor effects during intraoperative subthalamic nucleus stimulation for Parkinson's disease. J. Neurol. 252, 457-464 (2005).
50. Spencer, W. G. The effect produced upon respiration by faradic excitation of the cerebrum in the monkey, dog, cat and rabbit. Philos. Trans. B185, 609-657 (1894).
51. Chapman, W. P., Livingston, K. E. & Poppen, J. L. Effect upon blood pressure of electrical stimulation of the tips of the temporal lobes in man. J. Neurophysiol. 1, 65-71 (1950).
52. Pool, J. L. & Ransohoff, J. Autonomic effects on stimulating rostral portion of cingulate gyri in man. J. Neurophysiol. 12, 385-392 (1949).
53. Loewy, A. D. Forebrain nuclei involved in autonomic control. Prog. Brain Res. 87, 253-268 (1991).
54. Hess, W. R. In Hypothalamus und Thalamus: Experimental-Dokumente (ed. Hind, R. A) 22-23 (Thieme, Stuttgart, 1956).
55. Lipp, A. et al. Sympathetic activation due to deep brain stimulation in the region of the STN. Neurology 65, 774-775 (2005).
56. van Viljet, J. A., Vein, A. A., Ferrari, M. D. & van Dijk, J. G. Cardiovascular autonomic function tests in cluster headache. Cephalalgia 26 329-331 (2006).
57. May, A. et al. Correlation between structural and functional changes in brain in an idiopathic headache syndrome. Nat. Med. 5, 836-838 (1999).
58. Leone, M., Franzini, A. & Bussone, G. Stereotactic stimulation of posterior hypothalamic gray matter in a patient with intractable cluster headache. N. Engl. J. Med. 345, 1428-1429 (2001).
59. Leone, M. Deep brain stimulation in headache. Lancet Neurol. 5, 873-877 (2006).
60. [No authors listed] Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Eur. Heart J. 17, 354-381 (1996).
61. Tubani, L. et al. Heart rate variability in cluster headache. Ann. Ital. Med. Int. 18, 42-46 (2003).
62. Russel, D. & Storstein, L. Cluster headache: a computerized analysis of 24 h Holter ECG recording and description of ECG rhythm disturbances. Cephalalgia 3, 83-107 (1983).
63. Pollak, P. et al. Intraoperative micro-and macrostimulation of the subthalamic nucleus in Parkinson's disease. Mov. Disord. 3, S155-S161 (2002).
64. Mian, M. K., Campos, M., Sheth, S. A. & Eskandar, E. N. Deep brain stimulation for obsessive-compulsive disorder: past, present, and future. Neurosurg. Focus 2, E10 (2010).
65. Okun, M. S. et al. Deep brain stimulation in the internal capsule and nucleus accumbens region: responses observed during active and sham programming. J. Neurol. Neurosurg. Psychiatry 78, 310-314 (2007).
66. Shapira, N. A. et al. Panic and fear induced by deep brain stimulation. J. Neurol. Neurosurg. Psychiatry 77, 410-412 (2006).
67. Stemper, B. et al. Deep brain stimulation improves orthostatic regulation of patients with Parkinson disease. Neurology 67, 1781-1785 (2006).
68. Ludwig, J. et al. Effects of subthalamic nucleus stimulation and levodopa on the autonomic nervous system in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 78, 742-745 (2006).
69. Holmberg, B., Corneliusson O & Elam, M. Bilateral stimulation of nucleus subthalamicus in advanced Parkinson's disease: no effects on, and of, autonomic dysfunction. Mov. Disord. 8, 976-981 (2005).
70. Trachani, E. et al. Effects of subthalamic nucleus deep brain stimulation on sweating function in Parkinson's disease. Clin. Neurol. Neurosurg. 3, 213-217 (2010).
71. Ghione, S. Hypertension-associated hypalgesia. Evidence in experimental animals and humans, pathophysiological mechanisms, and potential clinical consequences. Hypertension 28, 494-504 (1996).
72. Carrive, P. & Bandler, R. Control of extracranial and hindlimb blood flow by the midbrain periaqueductal grey of the cat. Exp. Brain Res. 84, 599-606 (1991).
73. Carrive, P. & Bandler, R. Viscerotopic organization of neurones subserving hypotensive reactions within the midbrain periaqueductal grey: a correlative functional and anatomical study. Brain Res. 541, 206-215 (1991).
74. Lovick, T. Pain relief from deep brain stimulation at midbrain sites-a contribution from vagal processes? Exp. Neurol. 2, 240-242 (2010).
75. Viltart, O., Sartor D. M. & Verberne, A. J. Chemical stimulation of visceral afferents activates medullary neurones projecting to the central amygdala and periaqueductal grey. Brain Res. Bull. 71, 51-59 (2006).
76. Reis, D. J., Miura, M., Weinbren, M. & Gunne, L. M. Brain catecholamines: relation to defense reaction evoked by acute brainstem transaction in cat. Science 156, 1768-1770 (2006).
77. McGaraughty, S., Farr, D. & Heinricher, M. M. Lesions of the periaqueductal gray disrupt input to the rostral ventromedial medulla following microinjections of morphine into the medial or basolateral nuclei of the amygdala. Brain Res. 1009, 223-227 (2004).
78. Bittencourt, A. S., Carobrez, A. P., Zamprogno, L. P., Tufik S. & Schenberg, L. C. Organization of single components of defensive behaviors within distinct columns of periaqueductal gray matter of the rat: role of N?methyl?d-aspartic acid glutamate receptors. Neuroscience 125, 71-89 (2004).
79. Finnegan, T. F., Chen, S. R. & Pan, H. L. Effect of the ? opioid on excitatory and inhibitory synaptic inputs to periaqueductal gray-projecting neurones in the amygdala. J. Pharmacol. Exp. Ther. 312, 441-448 (2005).
80. Johnson, P. L., Lightman. S. L. & Lowry, C. A. A functional subset of serotonergic neurones in the rat ventrolateral periaqueductal gray implicated in the inhibition of sympathoexcitation and panic. Ann. NY Acad. Sci. 1018, 58-64 (2004).
81. Abrahams, V. C., Hilton, S. M. & Zbrozyna, A. W. Active muscle vasodilation produced by stimulation of the brain stem: its significance in the defense reaction. J. Physiol. 154, 491-513 (1960).
82. Duggan, A. W. & Morton, C. R. Periaqueductal grey stimulation: an association between selective inhibition of dorsal horn neurones and changes in peripheral circulation. Pain 15, 237-248 (1983).
83. Lovick, T. A. Ventrolateral medullary lesions block the antinociceptive and cardiovascular responses elicited by stimulating the dorsal periaqueductal grey matter in rats. Pain 21, 241-252 (1985).
84. Lovick, T. A. Inhibitory modulation of the cardiovascular defence response by the ventrolateral periaqueductal grey matter in rats. Exp. Brain Res. 89. 133-139 (1992).
85. Green, A. L. et al. Intra-operative deep brain stimulation of the periaqueductal grey matter modulates blood pressure and heart rate variability in humans. Neuromodulation 3, 174-181 (2010).
86. Green, A. L. et al. Controlling the heart via the brain: a potential new therapy for orthostatic hypotension. Neurosurgery 58, 1176-1183 (2006).
87. Patel, N. K. et al. Deep brain stimulation relieves refractory hypertension. Neurology 76, 405-407 (2010).
88. Green, A. L. et al. Stimulating the human midbrain to reveal the link between pain and blood pressure. Pain 3, 349-359 (2006).
89. Haldane, J. S. Organism and Environment as Illustrated by the Physiology of Breathing (Yale University Press, New Haven, 1917).
90. Fink, G. R. et al. Human cerebral activity with increasing inspiratory force: a study using positron emission tomography. J. Appl. Physiol. 3, 1295-1305 (1996).
91. McKay, L. C., Adams, L., Frackowiak R. S. & Corfield, D. R. A bilateral cortico-bulbar network associated with breath holding in humans, determined by functional magnetic resonance imaging. Neuroimage 40, 1824-1832 (2008).
92. Pattinson, K. T. et al. Determination of the human brainstem respiratory control network and its cortical connections in vivo using functional and structural imaging. Neuroimage 44, 295-305 (2009).
93. Barnes, P. J. Neural control of airway function: new perspectives. Mol. Aspects Med. 11, 351-423 (1990).
94. Hadziefendic, S. and Haxhiu, M. A. CNS innervation of vagal preganglionic neurons controlling peripheral airways: a transneuronal labelling study using pseudorabies virus. J. Auton Nerv. Sys. 76, 135-145 (1999).
95. Haxhiu, M. A., Jansen, A. S., Cherniack, N. S. & Loewy, A. D. CNS innervation of airway-related parasympathetic preganglionic neurons: a transneuronal labelling study using pseudorabies virus. Brain Res. Bull. 618, 115-134 (1993).
96. Haxhiu, M. A., Kc, P., Moore, C. T., Acquah, S. S., Wilson, C. G. et al. Brain stem excitatory and inhibitory signalling pathways regulating bronchoconstrictive responses. J. Appl. Physiol. 98, 1961-1982 (2005).
97. Herzog, J. et al. Subthalamic stimulation modulates cortical control of urinary bladder in Parkinson's disease. Brain 129, 3366-3375 (2006).
98. Dalmose, A. L., Bjarkam, C. R., Sorenson, J. C., Djurhuus, J. C. & Jorgensen, T. M. Effects of high frequency deep brain stimulation on urine storage and voiding function in conscious minipigs. Neurourol. Urodyn. 23, 265-272 (2004).
99. Finazzi-Agro, E. et al. Effects of subthalamic nucleus stimulation on urodynamic findings in patients with Parkinson's disease. J. Urol. 169, 1388-1391 (2003).
100. Seif, C. et al. Effect of subthalamic nucleus stimulation on the function of the urinary bladder. Ann. Neurol. 55, 118-120 (2004).
101. Aviles-Olmos, I. et al. Urinary incontinence following deep brain stimulation of the pedunculopontine nucleus. Acta Neurochir. (Wien) 12, 2357-2360 (2011).
102. Jensen, K. N., Deding, D., Soørensen, J. C. & Bjarkam, C. R. Long-term implantation of deep brain stimulation electrodes in the pontine micturition centre of the Göttingen mini-pig. Acta Neurochir. (Wien) 7, 785-794 (2009).
103. Halim, A., Baumgartner. L. & Binder, D. K. Effect of deep brain stimulation on autonomic dysfunction in patients with Parkinson's disease. J. Clin. Neurosci. 6 804-806 (2011).
104. Ciucci, M. R., Barkmeier-Kramer, J. M. & Sherman, S. J. Subthalamic nucleus deep brain stimulation improves deglutition in Parkinson's disease. Mov. Disord. 23, 676-683 (2008).
105. Cechetto, D. F. & Chen, S. J. Subcortical sites mediating sympathetic responses from insular cortex in rats. Am. J. Physiol. 258, R245-R255 (1990).
106. Craig, A. D. Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn. Sci. 19, 566-571 (2005).
107. Napadow, V. et al. Brain correlates of autonomic modulation: combining heart rate variability with fMRI. Neuroimage 42, 169-177 (2008).