Funktionelle Neuroanatomie der Depression

Thomas Kammer

doi:10.1055/a-1690-0497

Nervenheilkunde 2022; 41(03): 161-175
DOI: 10.1055/a-1690-0497

Übersichtsartikel

Funktionelle Neuroanatomie der Depression

Grundlagen und neue therapeutische Anwendungen durch HirnstimulationFunctional neuroanatomy of major depressionPrinciples and actual therapeutic aspects of brain stimulation

Thomas Kammer

¹Sektion für Neurostimulation, Klinik für Psychiatrie und Psychotherapie III, Universitätsklinikum Ulm

› Institutsangaben

Abstract

ZUSAMMENFASSUNG

Zur funktionellen Neuroanatomie der Depression gehört schon lange die Einsicht, dass es kein „Depressionszentrum“ gibt, sondern vielmehr Bereiche von grauer Substanz (kortikale Areale und subkortikale Kerne), die durch Nervenfaserbündel verbunden sind und daher oft als „Netzwerke“ oder „Schaltkreise“ bezeichnet werden. In den letzten Jahrzehnten ist es besonders durch die funktionelle Bildgebung möglich geworden, diese Netzwerke sowohl bei gesunden Probanden als auch bei Patienten mit Depression darzustellen, und Änderungen in der funktionellen Verknüpfung der Netzwerke zu identifizieren, die im Zusammenhang mit der Psychopathologie stehen. Vor diesem Hintergrund ist auch das Verständnis gewachsen, wie Hirnstimulationsverfahren wie die tiefe Hirnstimulation (THS) oder die repetitive transkranielle Magnetstimulation (rTMS) durch Modulation der Netzwerkfunktion ihre therapeutische Wirkung entfalten. In einem Rückblick wird die Entwicklung der funktionellen Bildgebung sowie der Hirnstimulationsverfahren nachgezeichnet und es werden aktuelle Entwicklungen des Einsatzes dieser Verfahren erörtert. Neuere Studien zur rTMS-Behandlung postulieren, dass der optimale Stimulationsort in Abhängigkeit von der psychopathologischen Ausprägung der Depression ausgewählt werden kann, unter Berücksichtigung der veränderten Konnektivität. Im Bereich der THS ist ein Fallbericht erschienen, in dem zunächst ein Mapping mit 10 implantierten Elektroden durchgeführt wurde. Verschiedene Stimulationsorte haben zu reproduzierbaren instantanen Veränderungen der Psychopathologie geführt. Die Patientin ist nun mit einer Closed-loop-Stimulation chronisch versorgt, die über Aktivität der rechten Amygdala geregelt wird.

ABSTRACT

In contrast to older concepts of a „depression center“ in the brain, the current view of functional anatomy of major depression comprises distributed parts of cortical and subcortical grey matter, connected by fibers, constituting so called networks, circuits, or loops, respectively. These networks can be measured by means of functional imaging in healthy subjects, as well as in depressed patients, yielding differences in connectivity related to psychopathology. In the light of this background, a more rational understanding of the therapeutic action of deep brain stimulation (DBS) as well as transcranial magnetic stimulation (rTMS) appears possible. The concurrent development of functional imaging and brain stimulation techniques is reviewed and translational applications are discussed. In recent rTMS treatment studies it is postulated that an optimal stimulation site can be chosen, dependent upon patterns of psychopathology and specific changes in connectivity. As regards THS, a case report has been published recently demonstrating a mapping procedure based on 10 implanted electrodes. Different stimulation sites resulted in immediate, reproducible positive changes of mood. This patient is now doing well for several months through treatment with closed-loop stimulation controlled by activity of the right amygdala.

Schlüsselwörter

Depression - Netzwerke - Schaltkreise - Magnetstimulation - tiefe Hirnstimulation - Stimulationsorte - funktionelle Konnektivität

Key words

Major depression - networks - loops - magnetic stimulation - deep brain stimulation - stimulation sites - functional connectivity

Volltext

Referenzen

Literatur
1 Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann Rev Neurosci 1986; 09: 357-381
2 Alexander GE, Crutcher MD, DeLong MR. Basal ganglia-thalamocortical circuits: Parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 1990; 85: 119-146
3 Anand A, Li Y, Wang Y. et al Activity and connectivity of brain mood regulating circuit in depression: A functional magnetic resonance study. Biol Psychiatry 2005; 57: 1079-1088
4 Baccaro A, Wang YP, Brunoni AR. et al Does stroke laterality predict major depression and cognitive impairment after stroke? Two-year prospective evaluation in the EMMA study. Prog Neuropsychopharmacol Biol Psychiatry 2019; 94: 109639
5 Baeken C, Vanderhasselt MA, Remue J. et al Intensive HF-rTMS treatment in refractory medication-resistant unipolar depressed patients. J Affect Disord 2013; 151: 625-631
6 Baxter LR, Phelps ME, Mazziotta JC. et al Cerebral Metabolic Rates for Glucose in Mood Disorders. Arch Gen Psychiatry 1985; 42: 441-447
7 Baxter LR, Schwartz JM, Phelps ME. et al Reduction of Prefrontal Cortex Glucose-Metabolism Common to Three Types of Depression. Arch Gen Psychiatry 1989; 46: 243-250
8 Berlim MT, Van den Eynde F, Daskalakis ZJ. A systematic review and meta-analysis on the efficacy and acceptability of bilateral repetitive transcranial magnetic stimulation (rTMS) for treating major depression. Psychol Med 2013; 43: 2245-2254
9 Berridge KC. From prediction error to incentive salience: mesolimbic computation of reward motivation. Eur J Neurosci 2012; 35: 1124-1143
10 Biswal B, Yetkin FZ, Haughton VM. et al Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 1995; 34: 537-541
11 Blumberger DM, Vila-Rodriguez F, Thorpe KE. et al Effectiveness of theta burst versus high-frequency repetitive transcranial magnetic stimulation in patients with depression (THREE-D): a randomised non-inferiority trial. Lancet 2018; 391: 1683-1692
12 Brunoni AR, Chaimani A, Moffa AH. et al Repetitive Transcranial Magnetic Stimulation for the Acute Treatment of Major Depressive Episodes A Systematic Review With Network Meta-analysis. JAMA Psychiatry 2017; 74: 143-152
13 Buckner RL, Krienen FM. The evolution of distributed association networks in the human brain. Trends Cogn Sci 2013; 17: 648-665
14 Carson AJ, MacHale S, Allen K. et al Depression after stroke and lesion location: a systematic review. Lancet 2000; 356: 122-126
15 Coenen VA, Bewernick BH, Kayser S. et al Superolateral medial forebrain bundle deep brain stimulation in major depression: a gateway trial. Neuropsychopharmacol 2019; 44: 1224-1232
16 Cole EJ, Stimpson KH, Bentzley BS. et al Stanford Accelerated Intelligent Neuromodulation Therapy for Treatment-Resistant Depression. Am J Psychiatry 2020; 177: 716-726
17 Corbetta M, Ramsey L, Callejas A. et al Common Behavioral Clusters and Subcortical Anatomy in Stroke. Neuron 2015; 85: 927-941
18 Dinga R, Schmaal L, Penninx BWJH. et al Evaluating the evidence for biotypes of depression: Methodological replication and extension of Drysdale. et al, (2017). Neuroimage Clin 2019; 22: 101796
19 Doucet GE, Lee WH, Frangou S. Evaluation of the spatial variability in the major resting-state networks across human brain functional atlases. Hum Brain Mapp 2019; 40: 4577-4587
20 Dougherty DD, Rezai AR, Carpenter LL. et al A Randomized Sham-Controlled Trial of Deep Brain Stimulation of the Ventral Capsule/Ventral Striatum for Chronic Treatment-Resistant Depression. Biol Psychiatry 2015; 78: 240-248
21 Douven E, Kohler S, Rodriguez MMF. et al Imaging Markers of Post-Stroke Depression and Apathy: a Systematic Review and Meta-Analysis. Neuropsychol Rev 2017; 27: 202-219
22 Downar J, Geraci J, Salomons TV. et al Anhedonia and Reward-Circuit Connectivity Distinguish Nonresponders from Responders to Dorsomedial Prefrontal Repetitive Transcranial Magnetic Stimulation in Major Depression. Biol Psychiatry 2014; 76: 176-185
23 Drevets WC, Videen TO, Price JL. et al A Functional Anatomical Study of Unipolar Depression. J Neurosci 1992; 12: 3628-3641
24 Drysdale AT, Grosenick L, Downar J. et al Resting-state connectivity biomarkers define neurophysiological subtypes of depression. Nat Med 2017; 23: 28-38
25 Egorova N, Cumming T, Shirbin C. et al Lower cognitive control network connectivity in stroke participants with depressive features. Transl Psychiatry 2018; 07: 4
26 Eitan R, Fontaine D, Benoit M. et al One year double blind study of high vs low frequency subcallosal cingulate stimulation for depression. J Psychiatr Res 2018; 96: 124-134
27 Feinsod M, Kreinin B, Chistyakov A. et al Preliminary evidence for a beneficial effect of low-frequency, repetitive transcranial magnetic stimulation in patients with major depression and schizophrenia. Depress Anxiety 1998; 07: 65-68
28 Fitzgerald PB, Benitez J, de Castella A. et al A randomized, controlled trial of sequential bilateral repetitive transcranial magnetic stimulation for treatment-resistant depression. Am J Psychiatry 2006; 163: 88-94
29 Fitzgerald PB, Laird AR, Maller J. et al A meta-analytic study of changes in brain activation in depression. Hum Brain Mapp 2008; 29: 683-695
30 Folstein MF, Maiberger R, Mchugh PR. Mood Disorder as a Specific Complication of Stroke. J Neurol Neurosurg Psychiatry 1977; 40: 1018-1020
31 Fox MD, Snyder AZ, Vincent JL. et al The human brain is intrinsically organized into dynamic, anticorrelated functional networks. P Natl Acad Sci USA 2005; 102: 9673-9678
32 Fox MD, Halko MA, Eldaief MC. et al Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation (TMS). Neuroimage 2012; 62: 2232-2243
33 Frank AM, Ceballos-Baumann A. Tiefe Hirnstimulation bei idiopathischem Parkinson-Syndrom und essenziellem Tremor: Grundlagen, Indikationsstellung, peri- und intraoperatives Vorgehen, Psychosomatik und Rehabilitation. Nervenheilkunde 2005; 24: 884-902
34 Fu CHY, Williams SCR, Cleare AJ. et al Attenuation of the neural response to sad faces in major depression by antidepressant treatment – A prospective, event-related functional magnetic resonance imaging study. Arch Gen Psychiatry 2004; 61: 877-889
35 Gainotti G. Emotional behavior and hemispheric side of the lesion. Cortex 1972; 08: 41-55
36 George MS, Ketter TA, Post RM. Prefrontal cortex dysfunction in clinical depression. Depression 1994; 02: 59-72
37 George MS, Wassermann EM, Williams WA. et al Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression. Neuroreport 1995; 06: 1853-1856
38 George MS, Lisanby SH, Avery D. et al Daily Left Prefrontal Transcranial Magnetic Stimulation Therapy for Major Depressive Disorder A Sham-Controlled Randomized Trial. Arch Gen Psychiatry 2010; 67: 507-516
39 Gozzi SA, Wood AG, Chen J. et al Imaging predictors of poststroke depression: methodological factors in voxel-based analysis. BMJ Open 2014; 04: e004948
40 Gross M, Nakamura L, Pascual-Leone A. et al Has repetitive transcranial magnetic stimulation (rTMS) treatment for depression improved? A systematic review and meta-analysis comparing the recent vs. the earlier rTMS studies. Acta Psychiatr Scand 2007; 116: 165-173
41 Hamilton M. A Rating Scale for Depression. J Neurol Neurosurg Psychiatry 1960; 23: 56-62
42 Harms MP, Somerville LH, Ances BM. et al Extending the Human Connectome Project across ages: Imaging protocols for the Lifespan Development and Aging projects. Neuroimage 2018; 183: 972-984
43 Herwig U, Fallgatter AJ, Höppner J. et al Antidepressant effects of augmentative transcranial magnetic stimulation: Randomised multicentre trial. Br J Psychiatry 2007; 191: 441-448
44 Holtzheimer PE, Husain MM, Lisanby SH. et al Subcallosal cingulate deep brain stimulation for treatment-resistant depression: a multisite, randomised, sham-controlled trial. Lancet Psychiatry 2017; 04: 839-849
45 Höppner J, Schulz M, Irmisch G. et al Antidepressant efficacy of two different rTMS procedures – High frequency over left versus low frequency over right prefrontal cortex compared with sham stimulation. Eur Arch Psychiatry Clin Neurosci 2003; 253: 103-109
46 House A, Dennis M, Warlow C. et al Mood Disorders after Stroke and Their Relation to Lesion Location – a Ct Scan Study. Brain 1990; 113: 1113-1129
47 Insel T, Cuthbert B, Garvey M. et al Research Domain Criteria (RDoC): Toward a New Classification Framework for Research on Mental Disorders. Am J Psychiatry 2010; 167: 748-751
48 Johnstone T, van Reekum CM, Urry HL. et al Failure to regulate: Counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J Neurosci 2007; 27: 8877-8884
49 Kaiser RH, Andrews-Hanna JR, Wager TD. et al Large-Scale Network Dysfunction in Major Depressive Disorder A Meta-analysis of Resting-State Functional Connectivity. JAMA Psychiatry 2015; 72: 603-611
50 Kischka U, Spitzer M, Kammer T. Frontal-subkortikale neuronale Schaltkreise. Fortschritte Neurol Psychiatrie 1997; 65: 221-231
51 Klein E, Kreinin I, Christyakov A. et al Therapeutic efficacy of right prefrontal slow repetitive transcranial magnetic stimulation in major depression – A double-blind controlled study. Arch Gen Psychiatry 1999; 56: 315-320
52 Koenigs M, Huey ED, Calamia M. et al Distinct Regions of Prefrontal Cortex Mediate Resistance and Vulnerability to Depression. J Neurosci 2008; 28: 12341-12348
53 Landis T, Regard M. Lateralität und Depression. Eine Untersuchung an Patienten mit Insulten im Versorgungsgebiet der A. cerebri posterior. In: Oepen G (Hrsg.). Psychiatrie des rechten und linken Gehirns. Köln: Deutscher Ärzte-Verlag 1988: 181-186
54 Levkovitz Y, Isserles M, Padberg F. et al Efficacy and safety of deep transcranial magnetic stimulation for major depression: a prospective multicenter randomized controlled trial. World Psychiatry 2015; 14: 64-73
55 Maglanoc LA, Landro NI, Jonassen R. et al Data-Driven Clustering Reveals a Link Between Symptoms and Functional Brain Connectivity in Depression. Biol Psychiatry Cogn Neurosci Neuroimaging 2019; 04: 16-26
56 Malone DA, Dougherty DD, Rezai AR. et al Deep Brain Stimulation of the Ventral Capsule/Ventral Striatum for Treatment-Resistant Depression. Biol Psychiatry 2009; 65: 267-275
57 Mayberg HS, Lozano AM, Voon V. et al Deep brain stimulation for treatment-resistant depression. Neuron 2005; 45: 651-660
58 Merkl A, Aust S, Schneider GH. et al Deep brain stimulation of the subcallosal cingulate gyrus in patients with treatment-resistant depression: A double-blinded randomized controlled study and long-term follow-up in eight patients. J Affect Disord 2018; 227: 521-529
59 Naidech AM, Polnaszek KL, Berman MD. et al Hematoma Locations Predicting Delirium Symptoms After Intracerebral Hemorrhage. Neurocrit Care 2016; 24: 397-403
60 Nys GMS, van Zandvoort MJE, van der Worp HB. et al Early depressive symptoms after stroke: neuropsychological correlates and lesion characteristics. J Neurol Sci 2005; 228: 27-33
61 O’Reardon JP, Solvason HB, Janicak PG. et al Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biol Psychiatry 2007; 62: 1208-16
62 Padmanabhan JL, Cooke D, Joutsa J. et al A Human Depression Circuit Derived From Focal Brain Lesions. Biol Psychiatry 2019; 86: 749-758
63 Pascual-Leone A, Rubio B, Pallardo F. et al Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. Lancet 1996; 348: 233-237
64 Peters SK, Dunlop K, Downar J. Cortico-Striatal-Thalamic Loop Circuits of the Salience Network: A Central Pathway in Psychiatric Disease and Treatment. Front Syst Neurosci 2016; 10: 104
65 Pfister R, Demmel W. Tiefe Hirnstimulation beim idiopathischen Parkinson-Syndrom. Indikationsstellung und Patientenberatung, Nachsorge und postoperative Prognose. Nervenheilkunde 2021; 40: 786-793
66 Plewnia C, Pasqualetti P, Grosse S. et al Treatment of major depression with bilateral theta burst stimulation: A randomized controlled pilot trial. J Affect Disord 2014; 156: 219-223
67 Price RB, Gates K, Kraynak TE. et al Data-Driven Subgroups in Depression Derived from Directed Functional Connectivity Paths at Rest. Neuropsychopharmacol 2017; 42: 2623-2632
68 Raymaekers S, Luyten L, Bervoets C. et al Deep brain stimulation for treatment-resistant major depressive disorder: a comparison of two targets and long-term follow-up. Transl Psychiatry 2017; 07: E1251
69 Robinson RG, Kubos KL, Starr LB. et al Mood Disorders in Stroke Patients – Importance of Location of Lesion. Brain 1984; 107: 81-93
70 Roth Y, Zangen A, Hallett M. A coil design for transcranial magnetic stimulation of deep brain regions. J Clin Neurophysiol 2002; 19: 361-370
71 Sambataro F, Wolf ND, Pennuto M. et al Revisiting default mode network function in major depression: evidence for disrupted subsystem connectivity. Psychol Med 2014; 44: 2041-2051
72 Scangos KW, Khambhati AN, Daly PM. et al Closed-loop neuromodulation in an individual with treatment-resistant depression. Nat Med 2021; 27: 1696-1700
73 Scangos KW, Makhoul GS, Sugrue LP. et al State-dependent responses to intracranial brain stimulation in a patient with depression. Nat Med 2021; 27: 229-234
74 Schlaepfer TE, Cohen MX, Frick C. et al Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacol 2008; 33: 368-377
75 Schlaepfer TE, Bewernick BH, Kayser S. et al Rapid Effects of Deep Brain Stimulation for Treatment-Resistant Major Depression. Biol Psychiatry 2013; 73: 1204-1212
76 Schlaepfer TE, Meyer-Lindenberg A, Synofzik M. et al Invasive Brain Stimulation in the Treatment of Psychiatric Illness Proposed Indications and Approaches. Dtsch Arztebl Int 2021; 118: 31-36
77 Schroll H, Hamker FH. Computational models of basal-ganglia pathway functions: focus on functional neuroanatomy. Front Syst Neurosci 2013; 07: 122
78 Schultz W. Neuronal Reward and Decision Signals: From Theories to Data. Physiol Rev 2015; 95: 853-951
79 Sheline YI, Barch DM, Donnelly JM. et al Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: An fMRI study. Biol Psychiatry 2001; 50: 651-658
80 Sheline YI, Barch DM, Price JL. et al The default mode network and self-referential processes in depression. P Natl Acad Sci USA 2009; 106: 1942-1947
81 Siddiqi SH, Taylor SF, Cooke D. et al Distinct Symptom-Specific Treatment Targets for Circuit-Based Neuromodulation. Am J Psychiatry 2020; 177: 435-446
82 Siddiqi SH, Schaper FLWVJ, Horn A. et al Brain stimulation and brain lesions converge on common causal circuits in neuropsychiatric disease. Nat Hum Behav 2021; 05: 1707
83 Siegle GJ, Steinhauer SR, Thase ME. et al Can’t shake that feeling: Assessment of sustained event-related fMRI amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry 2002; 51: 693-707
84 Siegle GJ, Thompson W, Carter CS. et al Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: Related and independent features. Biol Psychiatry 2007; 61: 198-209
85 Slotema CW, Blom JD, Hoek HW. et al Should We Expand the Toolbox of Psychiatric Treatment Methods to Include Repetitive Transcranial Magnetic Stimulation (rTMS)? A Meta-Analysis of the Efficacy of rTMS in Psychiatric Disorders. J Clin Psychiatry 2010; 71: 873-884
86 Tokuda T, Yoshimoto J, Shimizu Y. et al Identification of depression subtypes and relevant brain regions using a data-driven approach. Sci Rep 2018; 08: 14082
87 Tozzi L, Anene ET, Gotlib IH. et al Convergence, preliminary findings and future directions across the four human connectome projects investigating mood and anxiety disorders. Neuroimage 2021; 245: 118694
88 Uddin LQ, Yeo BTT, Spreng RN. Towards a Universal Taxonomy of Macro-scale Functional Human Brain Networks. Brain Topogr 2019; 32: 926-942
89 Van Essen DC, Smith SM, Barch DM. et al The WU-Minn Human Connectome Project: An overview. Neuroimage 2013; 80: 62-79
90 Wang JX, Rogers LM, Gross EZ. et al Targeted enhancement of cortical-hippocampal brain networks and associative memory. Science 2014; 345: 1054-1057
91 Wang YL, Tang S, Zhang LQ. et al Data-driven clustering differentiates subtypes of major depressive disorder with distinct brain connectivity and symptom features. Br J Psychiatry 2021; 219: 606-613
92 Zhang DY, Raichle ME. Disease and the brain’s dark energy. Nat Rev Neurol 2010; 06: 15-28
93 Plewnia C, Brendel B, Schwippel T. et al Treatment of major depressive disorder with bilateral theta burst stimulation: study protocol for a randomized, double-blind, placebo-controlled multicenter trial (TBS-D). Eur Arch Psychiatry Clin Neurosci 2021; 271: 1231-1243