Toward an Understanding of the Neural Circuitry of Major Depressive Disorder Through the Clinical Response to Deep Brain Stimulation of Different Anatomical Targets

Current Behavioral Neuroscience Reports

Volumn 1, Issue 2, 2014, Pages 55-63

  Crowell, Andrea L ^a   Riva Posse, Patricio ^a   Garlow, Steven J ^a   Mayberg, Helen S ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Deep brain stimulation; Depression; Functional neurosurgery; Lateral habenula; Medial forebrain bundle; Neurocircuitry; Nucleus accumbens; Subcallosal cingulate; Ventral capsule ventral striatum

Indexed keywords

EID: 84923574544     PISSN: None     EISSN: 21962979     Source Type: Journal    
DOI: 10.1007/s40473-014-0008-z     Document Type: Article

References (60)

1. Holtzheimer PE, Mayberg HS. Stuck in a rut: rethinking depression and its treatment. Trends Neurosci. 2011;34(1):1–9. DOI: 10.1016/j.tins.2010.10.004
2. Rajkowska G et al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry. 1999;45(9):1085–98. DOI: 10.1016/S0006-3223(99)00041-4
3. Ongur D, Drevets WC, Price JL. Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A. 1998;95(22):13290–5. DOI: 10.1073/pnas.95.22.13290
4. Gittins RA, Harrison PJ. A morphometric study of glia and neurons in the anterior cingulate cortex in mood disorder. J Affect Disord. 2011;133(1–2):328–32. DOI: 10.1016/j.jad.2011.03.042
5. Ongur D, Price JL. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex. 2000;10(3):206–19. DOI: 10.1093/cercor/10.3.206
6. Barbas H et al. Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neurosci. 2003;4:25. DOI: 10.1186/1471-2202-4-25
7. Petrides M, Pandya DN. Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns. Eur J Neurosci. 1999;11(3):1011–36. DOI: 10.1046/j.1460-9568.1999.00518.x
8. Haber SN. The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat. 2003;26(4):317–30. DOI: 10.1016/j.jchemneu.2003.10.003
9. Baxter Jr LR et al. Reduction of prefrontal cortex glucose metabolism common to three types of depression. Arch Gen Psychiatry. 1989;46(3):243–50. DOI: 10.1001/archpsyc.1989.01810030049007
10. Siegle GJ et al. Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol Psychiatry. 2007;61(2):198–209. DOI: 10.1016/j.biopsych.2006.05.048
11. Mayberg HS et al. Reciprocal limbic-cortical function and negative mood: Converging PET findings in depression and normal sadness. Am J Psychiatr. 1999;156(5):675–82.
12. Epstein J et al. Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. Am J Psychiatry. 2006;163(10):1784–90. DOI: 10.1176/appi.ajp.163.10.1784
13. Fales CL et al. Antidepressant treatment normalizes hypoactivity in dorsolateral prefrontal cortex during emotional interference processing in major depression. J Affect Disord. 2009;112(1–3):206–11. DOI: 10.1016/j.jad.2008.04.027
14. Mayberg HS. Targeted electrode-based modulation of neural circuits for depression. J Clin Invest. 2009;119(4):717–25. DOI: 10.1172/JCI38454
15. Pizzagalli DA, Jahn AL, O'Shea JP. Toward an objective characterization of an anhedonic phenotype: a signal-detection approach. Biol Psychiatry. 2005;57(4):319–27. DOI: 10.1016/j.biopsych.2004.11.026
16. Hall GB, Milne AM, Macqueen GM, An fMRI study of reward circuitry in patients with minimal or extensive history of major depression. Eur Arch Psychiatry Clin Neurosci, 2013.
17. Wacker J, Dillon DG, Pizzagalli DA. The role of the nucleus accumbens and rostral anterior cingulate cortex in anhedonia: integration of resting EEG, fMRI, and volumetric techniques. Neuroimage. 2009;46(1):327–37. DOI: 10.1016/j.neuroimage.2009.01.058
18. Ullsperger M, von Cramon DY. Error monitoring using external feedback: specific roles of the habenular complex, the reward system, and the cingulate motor area revealed by functional magnetic resonance imaging. J Neurosci. 2003;23(10):4308–14.
19. Abelson JL et al. Deep brain stimulation for refractory obsessive-compulsive disorder. Biol Psychiatry. 2005;57(5):510–6. DOI: 10.1016/j.biopsych.2004.11.042
20. Nuttin BJ et al. Long-term Electrical Capsular Stimulation in Patients with Obsessive-Compulsive Disorder. Neurosurgery. 2003;52(6):1263–74. DOI: 10.1227/01.NEU.0000064565.49299.9A
21. Shields DC et al. Prospective assessment of stereotactic ablative surgery for intractable major depression. Biol Psychiatry. 2008;64(6):449–54. DOI: 10.1016/j.biopsych.2008.04.009
22. Steele JD et al. Anterior cingulotomy for major depression: clinical outcome and relationship to lesion characteristics. Biol Psychiatry. 2008;63(7):670–7. DOI: 10.1016/j.biopsych.2007.07.019
23. Cosgrove GR, Rauch SL. Stereotactic cingulotomy. Neurosurg Clin N Am. 2003;14(2):225–35. DOI: 10.1016/S1042-3680(02)00115-8
24. Mayberg HS et al. Regional metabolic effects of fluoxetine in major depression: serial changes and relationship to clinical response. Biol Psychiatry. 2000;48(8):830–43. DOI: 10.1016/S0006-3223(00)01036-2
25. Holtzheimer PE, Mayberg HS. Deep brain stimulation for psychiatric disorders. Annu Rev Neurosci. 2011;34:289–307.
26. Mayberg HS et al. Deep brain stimulation for treatment-resistant depression. Neuron. 2005;45(5):651–60. DOI: 10.1016/j.neuron.2005.02.014
27. Lozano AM et al. Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol Psychiatry. 2008;64(6):461–7. DOI: 10.1016/j.biopsych.2008.05.034
28. Guinjoan SM et al. Asymmetrical contribution of brain structures to treatment-resistant depression as illustrated by effects of right subgenual cingulum stimulation. J Neuropsychiatry Clin Neurosci. 2010;22(3):265–77. DOI: 10.1176/appi.neuropsych.22.3.265
29. Kennedy SH et al. Deep brain stimulation for treatment-resistant depression: follow-up after 3 to 6 years. Am J Psychiatry. 2011;168(5):502–10. This study is notable as it reports the longest follow up to date of DBS for depression. Twenty patients were followed for three to six years. Intent to treat analysis shows 60 % response rate and 40 % remission rate with three years of chronic stimulation to the subcallosal cingulate. DOI: 10.1176/appi.ajp.2010.10081187
30. Holtzheimer PE et al. Subcallosal cingulate deep brain stimulation for treatment-resistant unipolar and bipolar depression. Arch Gen Psychiatry. 2012;69(2):150–8. DOI: 10.1001/archgenpsychiatry.2011.1456
31. Lozano AM et al. A multicenter pilot study of subcallosal cingulate area deep brain stimulation for treatment-resistant depression. J Neurosurg. 2012;116(2):315–22. DOI: 10.3171/2011.10.JNS102122
32. Merkl A et al. Antidepressant effects after short-term and chronic stimulation of the subgenual cingulate gyrus in treatment-resistant depression. Exp Neurol. 2013;249:160–8. DOI: 10.1016/j.expneurol.2013.08.017
33. Puigdemont D, et al. Deep brain stimulation of the subcallosal cingulate gyrus: further evidence in treatment-resistant major depression. Int J Neuropsychopharmacol, 2011; 1-13.
34. Ramasubbu R et al. Double-blind optimization of subcallosal cingulate deep brain stimulation for treatment-resistant depression: a pilot study. J Psychiatry Neurosci. 2013;38(5):325–32. DOI: 10.1503/jpn.120160
35. Hamani C et al. Deep brain stimulation of the subcallosal cingulate gyrus for depression: anatomical location of active contacts in clinical responders and a suggested guideline for targeting. J Neurosurg. 2009;111(6):1209–15. DOI: 10.3171/2008.10.JNS08763
36. Riva-Posse P et al. Optimization of subcallosal cingulate deep brain stimulation for treatment-resistant depression using structural connectivity. Biol Psychiatry. 2013;73(9, Supplement):A1–8. 1S-344S.This study demonstrates there are three separate white matter tracts that are necessary for antidepressant response to subcallosal cingulate DBS.
37. Nuttin B et al. Electrical stimulation in anterior limbs of internal capsules in patients with obsessive-compulsive disorder. Lancet. 1999;354(9189):1526. DOI: 10.1016/S0140-6736(99)02376-4
38. Aouizerate B et al. Deep brain stimulation of the ventral caudate nucleus in the treatment of obsessive-compulsive disorder and major depression. J Neurosurg. 2004;101(4):682–6. DOI: 10.3171/jns.2004.101.4.0682
39. Hsu DT, Price JL. Midline and intralaminar thalamic connections with the orbital and medial prefrontal networks in macaque monkeys. J Comp Neurol. 2007;504(2):89–111. DOI: 10.1002/cne.21440
40. Malone Jr DA et al. Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biol Psychiatry. 2009;65(4):267–75. DOI: 10.1016/j.biopsych.2008.08.029
41. Eshel N, Roiser JP. Reward and punishment processing in depression. Biol Psychiatry. 2010;68(2):118–24. DOI: 10.1016/j.biopsych.2010.01.027
42. Ferry AT et al. Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J Comp Neurol. 2000;425(3):447–70. DOI: 10.1002/1096-9861(20000925)425:3<447::AID-CNE9>3.0.CO;2-V
43. Vassoler FM et al. Deep brain stimulation of the nucleus accumbens shell attenuates cocaine reinstatement through local and antidromic activation. J Neurosci. 2013;36:14446–54. Showed that DBS to the nucleus accumbens shell attenuated cocaine reinstatement, not by inactivating the target nucleus or fibers of passage, but through antidromic activation of inhibitory interneurons in the prefrontal cortex. DOI: 10.1523/JNEUROSCI.4804-12.2013
44. Warden MR et al. A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge. Nature. 2012;492(7429):428–32.
45. Schlaepfer TE et al. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology. 2008;33(2):368–77. DOI: 10.1038/sj.npp.1301408
46. Bewernick BH et al. Long-term effects of nucleus accumbens deep brain stimulation in treatment-resistant depression: evidence for sustained efficacy. Neuropsychopharmacology. 2012;37(9):1975–85. DOI: 10.1038/npp.2012.44
47. Bewernick BH et al. Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression. Biol Psychiatry. 2010;67(2):110–6. DOI: 10.1016/j.biopsych.2009.09.013
48. Coenen VA et al. Cross-species affective functions of the medial forebrain bundle-implications for the treatment of affective pain and depression in humans. Neurosci Biobehav Rev. 2011;35(9):1971–81. DOI: 10.1016/j.neubiorev.2010.12.009
49. Coenen VA et al. Medial forebrain bundle stimulation as a pathophysiological mechanism for hypomania in subthalamic nucleus deep brain stimulation for Parkinson's disease. Neurosurgery. 2009;64(6):1106–14. discussion 1114-5. DOI: 10.1227/01.NEU.0000345631.54446.06
50. Schlaepfer TE et al. Rapid effects of deep brain stimulation for treatment-resistant major depression. Biol Psychiatry. 2013;73(12):1204–12. DOI: 10.1016/j.biopsych.2013.01.034
51. Coenen VA, Madler B, Schlaepfer TE. Reply to: medial forebrain bundle stimulation-speed access to an old or entry into a new depression neurocircuit? Biol Psychiatry. 2013;74(12):e45–6. DOI: 10.1016/j.biopsych.2013.06.017
52. Jimenez F et al. A patient with a resistant major depression disorder treated with deep brain stimulation in the inferior thalamic peduncle. Neurosurgery. 2005;57(3):585–93. DOI: 10.1227/01.NEU.0000170434.44335.19
53. Sartorius A, Henn FA. Deep brain stimulation of the lateral habenula in treatment resistant major depression. Med Hypotheses. 2007;69(6):1305–8. DOI: 10.1016/j.mehy.2007.03.021
54. Shumake J, Edwards E, Gonzalez-Lima F. Opposite metabolic changes in the habenula and ventral tegmental area of a genetic model of helpless behavior. Brain Res. 2003;963(1–2):274–81. DOI: 10.1016/S0006-8993(02)04048-9
55. Matsumoto M, Hikosaka O. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature. 2007;447(7148):1111–5. DOI: 10.1038/nature05860
56. Caldecott-Hazard S, Mazziotta J, Phelps M. Cerebral correlates of depressed behavior in rats, visualized using 14C-2-deoxyglucose autoradiography. J Neurosci. 1988;8(6):1951–61.
57. Danna CL, Shepard PD, Elmer GI. The habenula governs the attribution of incentive salience to reward predictive cues. Front Hum Neurosci. 2013;7:781. DOI: 10.3389/fnhum.2013.00781
58. Sartorius A et al. Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol Psychiatry. 2010;67(2):e9–e11.
59. Gutman DA et al. A tractography analysis of two deep brain stimulation white matter targets for depression. Biol Psychiatry. 2009;65(4):276–82. DOI: 10.1016/j.biopsych.2008.09.021
60. Lujan JL et al. Axonal pathways linked to therapeutic and nontherapeutic outcomes during psychiatric deep brain stimulation. Hum Brain Mapp. 2012;33(4):958–68. Demonstrates five white matter tracts shared by most subjects who responded to DBS to the ventral capsule/ventral striatum. There was one white matter tract common to all tre + atment non-responders. DOI: 10.1002/hbm.21262