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Four Deep Brain Stimulation Targets for Obsessive-Compulsive Disorder: Are They Different?

  • Suzanne N. Haber
    Correspondence
    Address correspondence to Suzanne Haber, Ph.D., at.
    Affiliations
    Department of Pharmacology and Physiology, University of Rochester School of Medicine and Dentistry, Rochester, New York

    Department of Psychiatry, McLean Hospital, Harvard Medical School, Belmont, Massachusetts
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  • Anastasia Yendiki
    Affiliations
    Athinoula A. Martinos Center for Biomedical Imaging, Harvard University and Massachusetts General Hospital, Boston, Massachusetts
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  • Saad Jbabdi
    Affiliations
    Wellcome Centre for Integrative Neuroimaging, Oxford Centre for Functional MRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
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      Abstract

      Deep brain stimulation is a promising therapeutic approach for patients with treatment-resistant obsessive-compulsive disorder, a condition linked to abnormalities in corticobasal ganglia networks. Effective targets are placed in one of four subcortical areas with the goal of capturing prefrontal, anterior cingulate, and basal ganglia connections linked to the limbic system. These include the anterior limb of the internal capsule, the ventral striatum, the subthalamic nucleus, and a midbrain target. The goal of this review is to examine these 4 targets with respect to the similarities and differences of their connections. Following a review of the connections for each target based on anatomic studies in nonhuman primates, we examine the accuracy of diffusion magnetic resonance imaging tractography to replicate those connections in nonhuman primates, before evaluating the connections in the human brain based on diffusion magnetic resonance imaging tractography. Results demonstrate that the four targets generally involve similar connections, all of which are part of the internal capsule. Nonetheless, some connections are unique to each site. Delineating the similarities and differences across targets is a critical step for evaluating and comparing the effectiveness of each and how circuits contribute to the therapeutic outcome. It also underscores the importance that the terminology used for each target accurately reflects its position and its anatomic connections, so as to enable comparisons across clinical studies and for basic scientists to probe mechanisms underlying deep brain stimulation.

      Keywords

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      References

        • Mallet L.
        • Polosan M.
        • Jaafari N.
        • Baup N.
        • Welter M.L.
        • Fontaine D.
        • et al.
        Subthalamic nucleus stimulation in severe obsessive-compulsive disorder.
        N Engl J Med. 2008; 359: 2121-2134
        • Greenberg B.D.
        • Rauch S.L.
        • Haber S.N.
        Invasive circuitry-based neurotherapeutics: Stereotactic ablation and deep brain stimulation for OCD.
        Neuropsychopharmacology. 2010; 35: 317-336
        • Goodman W.K.
        • Foote K.D.
        • Greenberg B.D.
        • Ricciuti N.
        • Bauer R.
        • Ward H.
        • et al.
        Deep brain stimulation for intractable obsessive compulsive disorder: Pilot study using a blinded, staggered-onset design.
        Biol Psychiatry. 2010; 67: 535-542
        • Denys D.
        • Mantione M.
        • Figee M.
        • van den Munckhof P.
        • Koerselman F.
        • Westenberg H.
        • et al.
        Deep brain stimulation of the nucleus accumbens for treatment-refractory obsessive-compulsive disorder.
        Arch Gen Psychiatry. 2010; 67: 1061-1068
        • Admon R.
        • Bleich-Cohen M.
        • Weizmant R.
        • Poyurovsky M.
        • Faragian S.
        • Hendler T.
        Functional and structural neural indices of risk aversion in obsessive-compulsive disorder (OCD).
        Psychiatry Res. 2012; 203: 207-213
        • Versace A.
        • Graur S.
        • Greenberg T.
        • Lima Santos J.P.
        • Chase H.W.
        • Bonar L.
        • et al.
        Reduced focal fiber collinearity in the cingulum bundle in adults with obsessive-compulsive disorder.
        Neuropsychopharmacology. 2019; 44: 1182-1188
        • Posner J.
        • Marsh R.
        • Maia T.V.
        • Peterson B.S.
        • Gruber A.
        • Simpson H.B.
        Reduced functional connectivity within the limbic cortico-striato-thalamo-cortical loop in unmedicated adults with obsessive-compulsive disorder.
        Hum Brain Mapp. 2014; 35: 2852-2860
        • Dunlop K.
        • Woodside B.
        • Olmsted M.
        • Colton P.
        • Giacobbe P.
        • Downar J.
        Reductions in cortico-striatal hyperconnectivity accompany successful treatment of obsessive-compulsive disorder with dorsomedial prefrontal rTMS.
        Neuropsychopharmacology. 2016; 41: 1395-1403
        • Tyagi H.
        • Apergis-Schoute A.M.
        • Akram H.
        • Foltynie T.
        • Limousin P.
        • Drummond L.M.
        • et al.
        A randomized trial directly comparing ventral capsule and anteromedial subthalamic nucleus stimulation in obsessive-compulsive disorder: Clinical and imaging evidence for dissociable effects.
        Biol Psychiatry. 2019; 85: 726-734
        • Coenen V.A.
        • Schumacher L.V.
        • Kaller C.
        • Schlaepfer T.E.
        • Reinacher P.C.
        • Egger K.
        • et al.
        The anatomy of the human medial forebrain bundle: Ventral tegmental area connections to reward-associated subcortical and frontal lobe regions.
        Neuroimage Clin. 2018; 18: 770-783
        • Coenen V.A.
        • Honey C.R.
        • Hurwitz T.
        • Rahman A.A.
        • McMaster J.
        • Burgel U.
        • 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 (discussion 1114–1115): 1106-1114
        • McIntyre C.C.
        • Grill W.M.
        • Sherman D.L.
        • Thakor N.V.
        Cellular effects of deep brain stimulation: Model-based analysis of activation and inhibition.
        J Neurophysiol. 2004; 91: 1457-1469
        • Riva-Posse P.
        • Choi K.S.
        • Holtzheimer P.E.
        • Crowell A.L.
        • Garlow S.J.
        • Rajendra J.K.
        • et al.
        A connectomic approach for subcallosal cingulate deep brain stimulation surgery: Prospective targeting in treatment-resistant depression.
        Mol Psychiatry. 2018; 23: 843-849
        • Hartmann C.J.
        • Chaturvedi A.
        • Lujan J.L.
        Quantitative analysis of axonal fiber activation evoked by deep brain stimulation via activation density heat maps.
        Front Neurosci. 2015; 9: 28
        • Liebrand L.C.
        • Caan M.W.A.
        • Schuurman P.R.
        • van den Munckhof P.
        • Figee M.
        • Denys D.
        • et al.
        Individual white matter bundle trajectories are associated with deep brain stimulation response in obsessive-compulsive disorder.
        Brain Stimul. 2019; 12: 353-360
        • Barcia J.A.
        • Avecillas-Chasin J.M.
        • Nombela C.
        • Arza R.
        • Garcia-Albea J.
        • Pineda-Pardo J.A.
        • et al.
        Personalized striatal targets for deep brain stimulation in obsessive-compulsive disorder.
        Brain Stimul. 2019; 12: 724-734
        • Azriel A.
        • Farrand S.
        • Di Biase M.
        • Zalesky A.
        • Lui E.
        • Desmond P.
        • et al.
        Tractography-guided deep brain stimulation of the anteromedial globus pallidus internus for refractory obsessive-compulsive disorder: Case report.
        Neurosurgery. 2019; 86: E558-E563
        • Coenen V.A.
        • Sajonz B.
        • Reisert M.
        • Bostroem J.
        • Bewernick B.
        • Urbach H.
        • et al.
        Tractography-assisted deep brain stimulation of the superolateral branch of the medial forebrain bundle (slMFB DBS) in major depression.
        Neuroimage Clin. 2018; 20: 580-593
        • Ramasubbu R.
        • Clark D.L.
        • Golding S.
        • Dobson K.S.
        • Mackie A.
        • Haffenden A.
        • et al.
        Long versus short pulse width subcallosal cingulate stimulation for treatment-resistant depression: A randomised, double-blind, crossover trial.
        Lancet Psychiatry. 2020; 7: 29-40
        • Raymaekers S.
        • Vansteelandt K.
        • Luyten L.
        • Bervoets C.
        • Demyttenaere K.
        • Gabriels L.
        • et al.
        Long-term electrical stimulation of bed nucleus of stria terminalis for obsessive-compulsive disorder.
        Mol Psychiatry. 2017; 22: 931-934
        • Luyten L.
        • Hendrickx S.
        • Raymaekers S.
        • Gabriels L.
        • Nuttin B.
        Electrical stimulation in the bed nucleus of the stria terminalis alleviates severe obsessive-compulsive disorder.
        Mol Psychiatry. 2016; 21: 1272-1280
        • Jimenez F.
        • Velasco F.
        • Salin-Pascual R.
        • Velasco M.
        • Nicolini H.
        • Velasco A.L.
        • et al.
        Neuromodulation of the inferior thalamic peduncle for major depression and obsessive compulsive disorder.
        Acta Neurochir Suppl. 2007; 97: 393-398
        • Neudorfer C.
        • Maarouf M.
        Neuroanatomical background and functional considerations for stereotactic interventions in the H fields of Forel.
        Brain Struct Funct. 2018; 223: 17-30
        • Lehman J.F.
        • Greenberg B.D.
        • McIntyre C.C.
        • Rasmussen S.A.
        • Haber S.N.
        Rules ventral prefrontal cortical axons use to reach their targets: Implications for diffusion tensor imaging tractography and deep brain stimulation for psychiatric illness.
        J Neurosci. 2011; 31: 10392-10402
        • Safadi Z.
        • Grisot G.
        • Jbabdi S.
        • Behrens T.E.
        • Heilbronner S.R.
        • McLaughlin N.C.R.
        • et al.
        Functional segmentation of the anterior limb of the internal capsule: Linking white matter abnormalities to specific connections.
        J Neurosci. 2018; 38: 2106-2117
        • Schmahmann J.
        • Pandya D.
        Fiber Pathways of the Brain.
        Oxford University Press, New York2006
      1. Dejerine J (1895): Anatomie des Centres Nerveux. Paris Rueff.

        • Selemon L.D.
        • Goldman-Rakic P.S.
        Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey.
        J Neurosci. 1985; 5: 776-794
        • Haber S.N.
        • Kim K.S.
        • Mailly P.
        • Calzavara R.
        Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning.
        J Neurosci. 2006; 26: 8368-8376
        • Nieuwenhuys R.
        • Geeraedts L.M.
        • Veening J.G.
        The medial forebrain bundle of the rat. I. General introduction.
        J Comp Neurol. 1982; 206: 49-81
        • Nieuwenhuys R.
        The greater limbic system, the emotional motor system and the brain.
        Prog Brain Res. 1996; 107: 551-580
        • Haynes W.I.
        • Haber S.N.
        The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: Implications for basal ganglia models and deep brain stimulation.
        J Neurosci. 2013; 33: 4804-4814
        • Haber S.N.
        • Lynd-Balta E.
        • Mitchell S.J.
        The organization of the descending ventral pallidal projections in the monkey.
        J Comp Neurol. 1993; 329: 111-128
        • Parent A.
        • Smith Y.
        Organization of efferent projections of the subthalamic nucleus in the squirrel monkey as revealed by retrograde labeling methods.
        Brain Research. 1987; 436: 296-310
        • Parent A.
        • Smith Y.
        • Filion M.
        • Dumas J.
        Distinct afferents to internal and external pallidal segments in the squirrel monkey.
        Neuroscience Letters. 1989; 96: 140-144
        • Jbabdi S.
        • Lehman J.F.
        • Haber S.N.
        • Behrens T.E.
        Human and monkey ventral prefrontal fibers use the same organizational principles to reach their targets: Tracing versus tractography.
        J Neurosci. 2013; 33: 3190-3201
        • Jbabdi S.
        • Sotiropoulos S.N.
        • Haber S.N.
        • van Essen D.C.
        • Behrens T.E.
        Measuring macroscopic brain connections in vivo.
        Nat Neurosci. 2015; 18: 1546-1555
        • Li N.
        • Baldermann J.C.
        • Kibleur A.
        • Treu S.
        • Akram H.
        • Elias G.J.B.
        • et al.
        A unified connectomic target for deep brain stimulation in obsessive-compulsive disorder.
        Nat Commun. 2020; 11: 3364
        • Axer H.
        • Keyserlingk D.G.
        Mapping of fiber orientation in human internal capsule by means of polarized light and confocal scanning laser microscopy.
        J Neurosci Methods. 2000; 94: 165-175
        • Haber S.N.
        • Gdowski M.J.
        The basal ganglia.
        in: Paxinos G. Mai J.K. The Human Nervous System. 2nd ed. Elsevier Press, 677–738, 2004
        • Lynd-Balta E.
        • Haber S.N.
        The organization of midbrain projections to the striatum in the primate: Sensorimotor-related striatum versus ventral striatum.
        Neuroscience. 1994; 59: 625-640
        • McFarland N.R.
        • Haber S.N.
        Organization of thalamostriatal terminals from the ventral motor nuclei in the macaque.
        J Comp Neurol. 2001; 429: 321-336
        • Gimenez-Amaya J.M.
        • McFarland N.R.
        • de las Heras S.
        • Haber S.N.
        Organization of thalamic projections to the ventral striatum in the primate.
        J Comp Neurol. 1995; 354: 127-149
        • Smith Y.
        • Raju D.V.
        • Pare J.F.
        • Sidibe M.
        The thalamostriatal system: A highly specific network of the basal ganglia circuitry.
        Trends Neurosci. 2004; 27: 520-527
        • Smith Y.
        • Galvan A.
        • Raju D.
        • Wichmann T.
        Anatomical and functional organization of the thalamostriatal systems.
        in: Steiner H. Tseng K.-Y. Handbook of Basal Ganglia Structure and Function. Academic, London2010: 381-396
        • Calzavara R.
        • Mailly P.
        • Haber S.N.
        Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: An anatomical substrate for cognition to action.
        Eur J Neurosci. 2007; 26: 2005-2024
        • Averbeck B.B.
        • Lehman J.
        • Jacobson M.
        • Haber S.N.
        Estimates of projection overlap and zones of convergence within frontal-striatal circuits.
        J Neurosci. 2014; 34: 9497-9505
        • Russchen F.T.
        • Bakst I.
        • Amaral D.G.
        • Price J.L.
        The amygdalostriatal projections in the monkey. An anterograde tracing study.
        Brain Res. 1985; 329: 241-257
        • Fudge J.L.
        • Kunishio K.
        • Walsh P.
        • Richard C.
        • Haber S.N.
        Amygdaloid projections to ventromedial striatal subterritories in the primate.
        Neuroscience. 2002; 110: 257-275
        • Haber S.N.
        • Lynd E.
        • Klein C.
        • Groenewegen H.J.
        Topographic organization of the ventral striatal efferent projections in the rhesus monkey: An anterograde tracing study.
        J Comp Neurol. 1990; 293: 282-298
        • Zaborszky L.
        • Cullinan W.E.
        Projections from the nucleus accumbens to cholinergic neurons of the ventral pallidum: A correlated light and electron microscopic double-immunolabeling study in rat.
        Brain Res. 1992; 570: 92-101
        • Haber S.
        Anatomical relationship between the basal ganglia and the basal nucleus of Meynert in human and monkey forebrain.
        Proc Natl Acad Sci U S A. 1987; 84: 1408-1412
        • Parent M.
        • Parent A.
        The microcircuitry of primate subthalamic nucleus.
        Parkinsonism Relat Disord. 2007; 13: S292-S295
        • Mena-Segovia J.
        • Ross H.M.
        • Magill P.J.
        • Bolam J.P.
        The Pedunculopontine Nucleus: Toward a Functional Integration With the Basal Ganglia.
        Springer Science and Business Media, New York2005
        • Lavoie B.
        • Parent A.
        Pedunculopontine nucleus in the squirrel monkey: Projections to the basal ganglia as revealed by anterograde tract-tracing methods.
        J Comp Neurol. 1994; 344: 210-231
        • Haber S.N.
        • Adler A.
        • Bergman H.
        The basal ganglia.
        in: Mai J.K. Paxinos G. The Human Nervous System. 3rd ed. Academic Press, 680–740, San Diego, CA2012
        • Nambu A.
        • Takada M.
        • Inase M.
        • Tokuno H.
        Dual somatotopical representations in the primate subthalamic nucleus: Evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplimentary motor area.
        J Neurosci. 1996; 16: 2671-2683
        • Karachi C.
        • Yelnik J.
        • Tande D.
        • Tremblay L.
        • Hirsch E.C.
        • Francois C.
        The pallidosubthalamic projection: An anatomical substrate for nonmotor functions of the subthalamic nucleus in primates.
        Mov Disord. 2005; 20: 172-180
        • 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. 1996; 73: 335-357
        • Neubert F.X.
        • Mars R.B.
        • Sallet J.
        • Rushworth M.F.
        Connectivity reveals relationship of brain areas for reward-guided learning and decision making in human and monkey frontal cortex.
        Proc Natl Acad Sci U S A. 2015; 112: E2695-E2704
        • Coenen V.A.
        • Panksepp J.
        • Hurwitz T.A.
        • Urbach H.
        • Madler B.
        Human medial forebrain bundle (MFB) and anterior thalamic radiation (ATR): Imaging of two major subcortical pathways and the dynamic balance of opposite affects in understanding depression.
        J Neuropsychiatry Clin Neurosci. 2012; 24: 223-236
        • Oades R.D.
        • Halliday G.M.
        Ventral tegmental (A10) system: Neurobiology. 1. Anatomy and connectivity.
        Brain Research. 1987; 434: 117-165
        • Levitt P.
        • Rakic P.
        • Goldman-Rakic P.
        Region-specific distribution of catecholamine afferents in primate cerebral cortex: A fluorescence histochemical analysis.
        J Comp Neurol. 1984; 227: 23-36
        • Veazey R.B.
        • Amaral D.G.
        • Cowan W.M.
        The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). I. Cytoarchitectonic organization.
        J Comp Neurol. 1982; 207: 114-134
        • Nauta W.J.
        Limbic innervation of the striatum.
        Adv Neurol. 1982; 35: 41-47
        • Mai J.
        • Paxinos G.
        • Voss T.
        Atlas of the Human Brain.
        Elsevier, 2008
        • Sutoo D.
        • Akiyama K.
        • Yabe Y.
        • Kohno K.
        Quantitative analysis of immunohistochemical distributions of cholinergic and catecholaminergic systems in the human brain.
        Neuroscience. 1994; 58: 227-234
        • Holt D.J.
        • Graybiel A.M.
        • Saper C.B.
        Neurochemical architecture of the human striatum.
        J Comp Neurol. 1997; 384: 1-25
        • Coenen V.A.
        • Prescher A.
        • Schmidt T.
        • Picozzi P.
        • Gielen F.L.
        What is dorso-lateral in the subthalamic nucleus (STN)?—A topographic and anatomical consideration on the ambiguous description of today’s primary target for deep brain stimulation (DBS) surgery.
        Acta Neurochir (Wien). 2008; 150 (discussion 1165): 1163-1165
        • Jbabdi S.
        • Behrens T.E.
        • Smith S.M.
        Crossing fibres in tract-based spatial statistics.
        Neuroimage. 2010; 49: 249-256
        • Thomas C.
        • Ye F.Q.
        • Irfanoglu M.O.
        • Modi P.
        • Saleem K.S.
        • Leopold D.A.
        • et al.
        Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited.
        Proc Natl Acad Sci U S A. 2014; 111: 16574-16579
        • Maier-Hein K.H.
        • Neher P.F.
        • Houde J.C.
        • Cote M.A.
        • Garyfallidis E.
        • Zhong J.
        • et al.
        The challenge of mapping the human connectome based on diffusion tractography.
        Nat Commun. 2017; 8: 1349
        • Reveley C.
        • Seth A.K.
        • Pierpaoli C.
        • Silva A.C.
        • Yu D.
        • Saunders R.C.
        • et al.
        Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography.
        Proc Natl Acad Sci U S A. 2015; 112: E2820-E2828
        • Jbabdi S.
        • Johansen-Berg H.
        Tractography: Where do we go from here?.
        Brain Connect. 2011; 1: 169-183
        • Haber S.N.
        • Fudge J.L.
        • McFarland N.R.
        Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum.
        J Neurosci. 2000; 20: 2369-2382
        • Greenberg B.D.
        • Malone D.A.
        • Friehs G.M.
        • Rezai A.R.
        • Kubu C.S.
        • Malloy P.F.
        • et al.
        Three-year outcomes in deep brain stimulation for highly resistant obsessive-compulsive disorder.
        Neuropsychopharmacology. 2006; 31: 2384-2393
        • Nuttin B.
        • Cosyns P.
        • Demeulemeester H.
        • Gybels J.
        • Meyerson B.
        Electrical stimulation in anterior limbs of internal capsules in patients with obsessive-compulsive disorder.
        Lancet. 1999; 354: 1526
        • Nuttin B.J.
        • Gabriels L.A.
        • Cosyns P.R.
        • Meyerson B.A.
        • Andreewitch S.
        • Sunaert S.G.
        • et al.
        Long-term electrical capsular stimulation in patients with obsessive-compulsive disorder.
        Neurosurgery. 2003; 52 (discussion 1272–1274): 1263-1272
        • Petersen M.V.
        • Mlakar J.
        • Haber S.N.
        • Parent M.
        • Smith Y.
        • Strick P.L.
        • et al.
        Holographic reconstruction of axonal pathways in the human brain.
        Neuron. 2019; 104: 1056-1064.e1053
        • Lawrence N.S.
        • An S.K.
        • Mataix-Cols D.
        • Ruths F.
        • Speckens A.
        • Phillips M.L.
        Neural responses to facial expressions of disgust but not fear are modulated by washing symptoms in OCD.
        Biol Psychiatry. 2007; 61: 1072-1080
        • Vaghi M.M.
        • Vertes P.E.
        • Kitzbichler M.G.
        • Apergis-Schoute A.M.
        • van der Flier F.E.
        • Fineberg N.A.
        • et al.
        Specific frontostriatal circuits for impaired cognitive flexibility and goal-directed planning in obsessive-compulsive disorder: Evidence from resting-state functional connectivity.
        Biol Psychiatry. 2017; 81: 708-717
        • Sha Z.
        • Versace A.
        • Edmiston E.K.
        • Fournier J.
        • Graur S.
        • Greenberg T.
        • et al.
        Functional disruption in prefrontal-striatal network in obsessive-compulsive disorder.
        Psychiatry Res Neuroimaging. 2020; 300: 111081
        • Saxena S.
        • Brody A.L.
        • Ho M.L.
        • Alborzian S.
        • Maidment K.M.
        • Zohrabi N.
        • et al.
        Differential cerebral metabolic changes with paroxetine treatment of obsessive-compulsive disorder vs. major depression.
        Arch Gen Psychiatry. 2002; 59: 250-261
        • van den Heuvel O.A.
        • Veltman D.J.
        • Groenewegen H.J.
        • Cath D.C.
        • van Balkom A.J.
        • van Hartskamp J.
        • et al.
        Frontal-striatal dysfunction during planning in obsessive-compulsive disorder.
        Arch Gen Psychiatry. 2005; 62: 301-309
        • Bleich-Cohen M.
        • Hendler T.
        • Weizman R.
        • Faragian S.
        • Weizman A.
        • Poyurovsky M.
        Working memory dysfunction in schizophrenia patients with obsessive-compulsive symptoms: An fMRI study.
        Eur Psychiatry. 2014; 29: 160-166
        • Haber S.N.
        Corticostriatal circuitry.
        Dialogues Clin Neurosci. 2016; 18: 7-21
        • Lynd-Balta E.
        • Haber S.N.
        Primate striatonigral projections: A comparison of the sensorimotor-related striatum and the ventral striatum.
        J Comp Neurol. 1994; 345: 562-578
        • Makris N.
        • Rathi Y.
        • Mouradian P.
        • Bonmassar G.
        • Papadimitriou G.
        • Ing W.I.
        • et al.
        Variability and anatomical specificity of the orbitofrontothalamic fibers of passage in the ventral capsule/ventral striatum (VC/VS): Precision care for patient-specific tractography-guided targeting of deep brain stimulation (DBS) in obsessive compulsive disorder (OCD).
        Brain Imaging Behav. 2016; 10: 1054-1067
        • de Koning P.P.
        • Figee M.
        • van den Munckhof P.
        • Schuurman P.R.
        • Denys D.
        Current status of deep brain stimulation for obsessive-compulsive disorder: A clinical review of different targets.
        Curr Psychiatry Rep. 2011; 13: 274-282
        • Dougherty D.D.
        • Chou T.
        • Corse A.K.
        • Arulpragasam A.R.
        • Widge A.S.
        • Cusin C.
        • et al.
        Acute deep brain stimulation changes in regional cerebral blood flow in obsessive-compulsive disorder.
        J Neurosurg. 2016; 125: 1087-1093
        • Figee M.
        • Luigjes J.
        • Smolders R.
        • Valencia-Alfonso C.E.
        • van Wingen G.
        • de Kwaasteniet B.
        • et al.
        Deep brain stimulation restores frontostriatal network activity in obsessive-compulsive disorder.
        Nat Neurosci. 2013; 16: 386-387
        • Widge A.S.
        • Zorowitz S.
        • Basu I.
        • Paulk A.C.
        • Cash S.S.
        • Eskandar E.N.
        • et al.
        Deep brain stimulation of the internal capsule enhances human cognitive control and prefrontal cortex function.
        Nat Commun. 2019; 10: 1536
        • Figee M.
        • Vink M.
        • de Geus F.
        • Vulink N.
        • Veltman D.J.
        • Westenberg H.
        • et al.
        Dysfunctional reward circuitry in obsessive-compulsive disorder.
        Biol Psychiatry. 2011; 69: 867-874
        • van Laere K.
        • Nuttin B.
        • Gabriels L.
        • Dupont P.
        • Rasmussen S.
        • Greenberg B.D.
        • et al.
        Metabolic imaging of anterior capsular stimulation in refractory obsessive-compulsive disorder: A key role for the subgenual anterior cingulate and ventral striatum.
        J Nucl Med. 2006; 47: 740-747
        • Krieg W.
        Architectonics of the Human Cerebral Fiber Systems.
        Brain Books, Evanston, IL1973