Advertisement
Review Article| Volume 37, 100100, March 2023

Personalized definition of surgical targets in major depression and obsessive-compulsive disorder: A potential role for low-intensity focused ultrasound?

  • Salvador M. Guinjoan
    Affiliations
    Laureate Institute for Brain Research and Department of Psychiatry, Oklahoma University Health Sciences Center at Tulsa, Laureate Institute for Brain Research, 6655 S. Yale Ave., Tulsa, OK 74136, United States of America
    Search for articles by this author
Published:February 27, 2023DOI:https://doi.org/10.1016/j.pmip.2023.100100

      Abstract

      Major Depressive Disorder (MDD) and Obsessive-Compulsive Disorder (OCD) are common and potentially incapacitating conditions. Even when recognized and adequately treated, in over a third of patients with these conditions the response to first-line pharmacological and psychotherapeutic measures is not satisfactory. After more assertive measures including pharmacological augmentation (and in the case of depression, transcranial magnetic stimulation, electroconvulsive therapy, or treatment with ketamine or esketamine), a significant number of individuals remain severely symptomatic. In these persons, different ablation and deep-brain stimulation (DBS) psychosurgical techniques have been employed. However, apart from the cost and potential morbidity associated with surgery, on average only about half of patients show adequate response, which limits the widespread application of these potentially life-saving interventions. Possible reasons are considered for the wide variation in outcomes across different series of patients with MDD or OCD exposed to ablative or DBS psychosurgery, including interindividual anatomical and etiological variability. Low-intensity focused ultrasound (LIFU) is an emerging technique that holds promise in its ability to achieve anatomically circumscribed, noninvasive, and reversible neuromodulation of deep brain structures. A possible role for LIFU in the personalized presurgical definition of neuromodulation targets in the individual patient is discussed, including a proposed roadmap for clinical trials addressed at testing whether this technique can help to improve psychosurgical outcomes.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Personalized Medicine in Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Avecillas-Chasin J.M.
        • Hurwitz T.A.
        • Bogod N.M.
        • Honey C.R.
        Tractography-guided anterior capsulotomy for major depression and obsessive-compulsive disorder: targeting the emotion network.
        Operat Neurosurg. 2022; 20: 407-412
        • Baer K.-J.
        • Greiner W.
        • Jochum T.
        • Friedrich M.
        • Wagner G.
        • Sauer H.
        The influence of major depression and its treatment on heart rate variability and pupillary light reflex parameters.
        J Affect Disord. 2004; 82: 245-252
        • Baldermann J.C.
        • Schüller T.
        • Kohl S.
        • Voon V.
        • Li N.
        • Hollunder B.
        • et al.
        Connectomic deep-brain stimulation for obsessive-compulsive disorder.
        Biol Psychiatry. 2021; 90: 678-688https://doi.org/10.1016/j.biopsych.2021.07.010
        • Bergfeld I.O.
        • Mantione M.
        • Hoogendoorn M.L.C.
        • Ruhe H.G.
        • Notten P.
        • van Laarhoven J.
        • et al.
        Deep brain stimulation of the ventral anterior limb of the internal capsule for treatment-resistant depression: a randomized clinical trial.
        JAMA Psychiat. 2016; 73: 456-464https://doi.org/10.1001/jamapsychiatry.2016.0152
        • Boutet A.
        • et al.
        Functional MRI safety and artifacts during deep brain stimulation: experience in 102 patients.
        Radiology. 2019; 293 ([PubMed: 31385756]): 174-183
        • Bouwens van der Vlis T.A.M.
        • Ackermans L.
        • Mulders A.E.P.
        • Vrij C.A.
        • Schruers K.
        • Temel Y.
        • et al.
        Ventral capsule/ventral striatum stimulation in obsessive-compulsive disorder: toward a unified connectomic target for deep brain stimulation?.
        Neuromodulation. 2021; 24: 316-323
        • Bowary P.
        • Greenberg B.D.
        Noninvasive focused ultrasound for neuromodulation: A review.
        Psychiatr Clin N Am. 2018; 41: 505-514
        • Brinker S.T.
        • Preiswerk F.
        • White P.J.
        • Mariano T.Y.
        • McDannold N.J.
        • Bubrick E.J.
        Focused ultrasound platform for investigating therapeutic modulation across the human hippocampus.
        Ultrasound Med Biol. 2020; 46: 1270-1274
        • Chan N.Y.
        Catheter cryoablation for atrioventricular nodal reentrant tachycardia. Chapter 4 in The Practice of Catheter Cryoablation for Cardiac Arrhythmias. Chichester, United Kingdom, Wiley-Blackwell2014: 36-46
        • Darmani G.
        • Bergmann T.O.
        • Butts Pauly K.
        • Caskey C.F.
        • de Lecea L.
        • Fomenko A.
        • et al.
        Non-invasive transcranial ultrasound stimulation for neuromodulation.
        Clin Neurophysiol. 2022; 135: 51-73
        • Davidson B.
        • Hamani C.
        • Huang Y.
        • Jones R.M.
        • Meng Y.
        • Giacobbe P.
        • et al.
        Magnetic resonance-guided focused ultrasound capsulotomy for treatment-resistant psychiatric disorders.
        Oper Neurosurg. 2020; 19: 741-749
        • Davidson D.
        • Eapen-John D.
        • Mithani K.
        • Rabin J.S.
        • Meng Y.
        • Cao X.
        • et al.
        Lesional psychiatric neurosurgery: meta-analysis of clinical outcomes using a transdiagnostic approach.
        J Neurol Neurosurg Psychiatry. 2022; 93: 207-215
        • de Guevara M.S.
        • Schauffele S.I.
        • Nicola-Siri L.C.
        • Fahrer R.D.
        • Ortíz-Frágola E.
        • Martínez-Martínez J.A.
        • et al.
        Worsening of depressive symptoms 6 months after an acute coronary event in older adults is associated with impairment of cardiac autonomic function.
        J Affect Disord. 2004; 80: 257-262
        • Dougherty D.D.
        • Weiss A.P.
        • Cosgrove G.R.
        • Alpert N.M.
        • Cassem E.H.
        • Nierenberg A.A.
        • et al.
        Cerebral metabolic correlates as potential predictors of response to anterior cingulotomy for treatment of major depression.
        J Neurosurg. 2003; 99: 1010-1017
        • Figee M.
        • Mayberg H.S.
        The future of personalized brain stimulation.
        Nat Med. 2021; 27: 196-197
        • Fry W.J.
        • Tucker D.
        • Fry F.J.
        • Wulff V.J.
        Physical factors involved in ultrasonically induced changes in living systems: II. Amplitude duration relations and the effect of hydrostatic pressure for nerve tissue.
        J Acoust Soc Am. 1951; 23: 364-368
        • Fry F.J.
        • Ades H.W.
        • Fry W.J.
        Production of reversible changes in the central nervous system by ultrasound.
        Science. 1958; 127: 83-84
        • Germann J.
        • Elias G.J.B.
        • Neudorfer C.
        • Boutet A.
        • Chow C.T.
        • Wong E.H.Y.
        • et al.
        Potential optimization of focused ultrasound capsulotomy for obsessive compulsive disorder.
        Brain. 2021; 144: 3529-3540
        • Godlewska B.R.
        • Browning M.
        • Norbury R.
        • Igoumenou A.
        • Cowen P.J.
        • Harmer C.J.
        Predicting treatment response in depression: the role of the anterior cingulate cortex.
        Int J Neuropsychopharmacol. 2018; 21: 988-996
        • Guinjoan S.M.
        • Bernabó J.L.
        • Cardinali D.P.
        Cardiovascular tests of autonomic function and sympathetic skin responses in patients with major depression.
        J Neurol Neurosurg Psychiatry. 1995; 59: 299-302
        • Guinjoan S.M.
        • Mayberg H.S.
        • Costanzo E.Y.
        • Fahrer R.D.
        • Tenca E.
        • Antico J.
        • 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: 265-277
        • Haber S.N.
        • Yendiki A.
        • Jbabdi S.
        Four deep brain stimulation targets for obsessive-compulsive disorder: are they different?.
        Biol Psychiatry. 2021; 90: 667-677
        • Hancu I.
        • et al.
        On the (Non-)equivalency of monopolar and bipolar settings for deep brain stimulation fMRI studies of Parkinson’s disease patients.
        J Magn Reson Imaging. 2019; 49 ([PubMed: 30552842]): 1736-1749
        • Harvey E.N.
        • Loomis A.L.
        High frequency sound waves of small intensity and their biological effects.
        Nature. 1928; 121: 622-624
        • Jeurissen B.
        • Descoteaux M.
        • Mori S.
        • Leemans A.
        Diffusion MRI fiber tractography of the brain.
        NMR Biomed. 2019; 32: e3785
        • Kahn L.
        • Sutton B.
        • Winston H.R.
        • Abosch A.
        • Thompson J.A.
        • Davis R.A.
        Deep brain stimulation for obsessive-compulsive disorder: real world experience post-FDA-humanitarian use device approval.
        Front Psychiatry. 2021; 12568932
        • Krauss J.K.
        • Lipsman N.
        • Aziz T.
        • Boutet A.
        • Brown P.
        • Chang J.W.
        • et al.
        Technology of deep brain stimulation: current status and future directions.
        Nat Rev Neurol. 2021; 17: 75-87
        • Lee M.A.
        • Morady F.
        • Kadish A.
        • Schamp D.J.
        • Chin M.C.
        • Scheinman M.M.
        • et al.
        Catheter modification of the atrioventricular junction with radiofrequency energy for control of atrioventricular nodal reentry tachycardia.
        Circulation. 1991; 83: 827-835
        • Lee D.J.
        • Lozano C.S.
        • Dallapiazza R.F.
        • Lozano A.M.
        Current and future directions of deep brain stimulation for neurological and psychiatric disorders.
        J Neurosurg. 2019; 131: 333-342
        • 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
        • Lippitz B.
        • Mindus P.
        • Meyerson B.
        • Kihlstrom L.
        • Lindquist C.
        Lesion topography and outcome after thermocapsulotomy or gamma knife capsulotomy for obsessive-compulsive disorder: relevance of the right hemisphere.
        Neurosurgery. 1999; 44 (PMID: 10069581): 452-458https://doi.org/10.1097/00006123-199903000-00005
        • Makris N.
        • Rathi Y.
        • Mouradian P.
        • Bonmassar G.
        • Papadimitriou G.
        • Ing W.I.
        • et al.
        Variability and anatomical specificity of 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 Imag Behav. 2016; 10: 1054-1067
        • Marchetti I.
        • Mor N.
        • Chiorri C.
        • Koster E.H.W.
        The Brief State Rumination Inventory (BSRI): Validation and psychometric evaluation.
        Cogn Ther Res. 2018; 42: 447-460
        • Mayberg H.S.
        • Lozano A.M.
        • Voon V.
        • McNeely H.E.
        • Seminowicz D.
        • Hamani C.
        • et al.
        Deep brain stimulation for treatment-resistant depression.
        Neuron. 2005; 45: 651-660
        • Munoz F.
        • Meaney A.
        • Gross A.
        • Liu K.
        • Pouliopoulos A.N.
        • Liu D.
        • et al.
        Long term study of motivational and cognitive effects of low-intensity focused ultrasound neuromodulation in the dorsal striatum of nonhuman primates.
        Brain Stimul. 2022; 15: 360-372
        • Paulo D.L.
        • Bick S.K.
        Advanced imaging in psychiatric neurosurgery: toward personalized treatment.
        Neuromodulation. 2022; 25: 195-201
        • Rezai A.R.
        • et al.
        Is magnetic resonance imaging safe for patients with neurostimulation systems used for deep brain stimulation?.
        Neurosurgery. 2005; 57 ([PubMed: 16284576]): 1056-1062
      1. Riva-Posse P, Choi KS, Holtzheimer PE, McIntyre CC, Gross RE, Chaturvedi, A Crowell AL, Garlow SJ, Rajendra JK, Mayberg HS (2014): Defining critical white matter pathways mediating successful subcallosal cingulate deep brain stimulation for treatment-resistant depression. Biol Psychiatry 2014; 76: 963–969.

        • 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
        • Riva-Posse P.
        • Inman C.S.
        • Choi K.S.
        • Crowell A.L.
        • Gross R.E.
        • Hamann S.
        • et al.
        Autonomic arousal elicited by subcallosal cingulate stimulation is explained by white matter connectivity.
        Brain Stimul. 2019; 12: 743-751
        • Ruan H.
        • Wang Y.
        • Li Z.
        • Tong G.
        • Wang Z.
        A systematic review of treatment outcome predictors in deep brain stimulation for refractory obsessive-compulsive disorder.
        Brain Sci. 2022; 12: 936
        • Ruscio A.M.
        • Stein D.J.
        • Chiu W.T.
        • Kesler R.C.
        The epidemiology of obsessive-compulsive disorder in the National Comorbidity Survey Replication.
        Mol Psychiatry. 2010; 15: 53-63
      2. Sanchez SM, Tsuchiyagaito A, Kuplicki R, Park H, Khalsa SS, Paulus MP, Guinjoan SM (2022): Cardiac autonomic changes in response to low-intensity focused ultrasound of the right ventral anterior limb of the internal capsule. Focused Ultrasound Neuromodulation Conference meeting (FUN2022), September 26-28, Mainz, Germany.

        • Sarwar T.
        • Ramamohanarao K.
        • Zalesky A.
        Mapping connectomes with diffusion MRI: deterministic or probabilistic tractography??.
        Magn Reason Med. 2019; 81: 1368-1384
        • Scangos K.W.
        • Makhoul G.S.
        • Sugrue L.P.
        • Chang E.F.
        • Krystal A.D.
        State-dependent responses to intracranial brain stimulation in a patient with depression.
        Nature Med. 2021; 27: 229-231
        • Scangos K.W.
        • Khambhati A.N.
        • Daly P.M.
        • Makhoul G.S.
        • Sugrue L.P.
        • Zamanian H.
        • et al.
        Closed-loop neuromodulation in an individual with treatment-resistant depression.
        Nat Med. 2021; 27: 1696-1700https://doi.org/10.1038/s41591-021-01480-w. PMID: 34608328
      3. Smart OL, Tiruvadi VR, Mayberg HS (2015): Multimodal approaches to define network oscillations in depression. Biol Psychiatry 77: 1061-1070.

        • Smart O.
        • Choi K.S.
        • Riva-Posse P.
        • Tiruvadi V.
        • Rajendra J.
        • Waters A.C.
        • et al.
        Initial unilateral exposure to deep brain stimulation in treatment-resistant depression patients alters spectral power in the subcallosal cingulate.
        Front Comput Neurosci. 2018; 12: 43
        • Smith E.E.
        • Choi K.S.
        • Veerakumar A.
        • Obatusin M.
        • Howell B.
        • Smith A.H.
        • et al.
        Time-frequency signatures evoked by single-pulse deep brain stimulation to the subcallosal cingulate.
        Front Hum Neurosci. 2022; 16939258
        • Stahl D.
        • Cabrera L.
        • Gibb T.
        Should DBS for psychiatric disorders be considered a form of psychosurgery? Ethical and legal considerations.
        Sci Eng Ethics. 2018; 24: 1119-11142
      4. Takagi SF, Higashino S, Shibuya T, Osawa N (1960): The actions of ultrasound on the myelinated nerve, the spinal cord and the brain. Jpn J Physiol 10(2):183–193.

        • Tufail Y.
        • Matyushov A.
        • Baldwin N.
        • Tauchmann M.L.
        • Georges J.
        • Yoshihiro A.
        • et al.
        Transcranial pulsed ultrasound stimulates intact brain circuits.
        Neuron. 2010; 66: 681-694
        • 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
        • Tyler W.J.
        • Tufail Y.
        • Finsterwald M.
        • Tauchmann M.L.
        • Olson E.J.
        • Majestic C.
        • et al.
        Remote excitation of neuronal circuits using low-intensity, low-frequency ultrasound.
        PLoS One. 2008; 3: e3511
        • van der Wal J.M.
        • Bergfeld I.O.
        • Lok A.
        • Mantione M.
        • Figee M.
        • Notten P.
        • et al.
        Long-term deep brain stimulation of the ventral anterior limb of the internal capsule for treatment-resistant depression.
        J Neurol Neurosurg Psychiatry. 2020; 91: 189-195
      5. Velling VA, Shklyaruk SP (1988): Modulation of the functional state of the brain with the aid of focused ultrasonic action. Neurosci Behav Physiol 18(5):369–375.

        • Varjao Vieira E.
        • Ricci Arantes P.
        • Hamani C.
        • Iglesio R.
        • Paiva Duarte K.
        • Jacobsen Teixeira M.
        • et al.
        Neurocircuitry of deep brain stimulation for obsessive-compulsive disorder as revealed by tractography: a systematic review.
        Front Psychiatry. 2021; 12680484
        • Widge A.S.
        • Zhang F.
        • Gosai A.
        • Papadimitrou G.
        • Wilson-Braun P.
        • Tsintou M.
        • et al.
        Patient-specific connectomic models correlate with, but do not reliably predict, outcomes in deep brain stimulation for obsessive-compulsive disorder.
        Neuropsychopharmacol. 2022; 47: 965-972
        • World Health Organization
        Depression and other common mental disorders.
        Global Health Estimates. 2017;
        • Zeng K.
        • Darmani G.
        • Fomenko A.
        • Xia X.
        • Tran S.
        • Nankoo J.-F.
        • et al.
        Induction of human motor cortex plasticity by theta burst transcranial ultrasound stimulation.
        Ann Neurol, in press. 2022; https://doi.org/10.1002/ana.26294
        • Zhang C.
        • Kim S.G.
        • Li J.
        • Zhang Y.
        • Lv Q.
        • Zeljic K.
        • et al.
        Anterior limb of the internal capsule tractography: relationship with capsulotomy outcomes in obsessive-compulsive disorder.
        J Neurol Neurosurg Psychiatry. 2021; 92: 637-644
        • Zhang F.
        • Daducci A.
        • He Y.
        • Schiavi S.
        • Seguin C.
        • Smith R.E.
        • et al.
        Quantitative mapping of the brain's structural connectivity using diffusion MRI tractography: A review.
        Neuroimage. 2022; 249118870
        • Nemeroff C.B.
        The state of our understanding of the pathophysiology and optimal treatment of depression: Glass half full or half empty?.
        Am J Psychiatry. 2020; 177: 671-685
        • Jacquesson T.
        • Cotton F.
        • Attye A.
        • Zaouche S.
        • Tringali S.
        • Bosc J.
        • et al.
        Probabilistic tractography to predict the position of cranial nerves displaced by skull base tumors: value for surgical strategy through a case series of 62 patients.
        Neurosurgery. 2019; 85: E125-E136
        • Wende T.
        • Hoffmann K.T.
        • Meixensberger J.
        Tractography in neurosurgery: a systematic review of current applications.
        J Neurol Surg A Cent Eur Neurosurg. 2020; 81: 442-455
        • Sánchez S.M.
        • Duarte-Abritta B.
        • Abulafia C.
        • De Pino G.
        • Bocaccio H.
        • Castro M.N.
        • Sevlever G.E.
        • Fonzo G.A.
        • Nemeroff C.B.
        • Gustafson D.R.
        • Guinjoan S.M.
        • Villarreal M.F.
        White matter fiber density abnormalities in cognitively normal adults at risk for late-onset Alzheimer's disease.
        Journal of Psychiatric Research. 2020; 122: 79-87
        • Breet E.
        • Kidd M.
        • McGregor N.W.
        • Stein D.J.
        • Lochner C.
        Suicide ideation and attempts in obsessive-compulsive disorder.
        Ann Clin Psychiatry. 2019; 31: 192-199
        • Skapinakis P.
        • Politis S.
        • Karampas A.
        • Petrikis P.
        • Mavreas V
        Prevalence, comorbidity, quality of life and use of services of obsessive-compulsive disorder and subthreshold obsessive-compulsive symptoms in the general adult population of Greece. In.
        J Psychiatry Clin Pract. 2019; 23: 215-224