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Computationally informed interventions for targeting compulsive behaviors

Published:September 06, 2022DOI:https://doi.org/10.1016/j.biopsych.2022.08.028

      ABSTRACT

      Compulsive behaviors are central to addiction and obsessive-compulsive disorder and can be understood as a failure of adaptive decision-making. Particularly, they can be conceptualized as an imbalance in behavioral control, such that behavior is guided predominantly by learned rather than inferred outcome expectations. Inference is a computational process required for adaptive behavior, and recent work across species has identified the neural circuitry that support inference-based decision-making. This includes the orbitofrontal cortex, which has long been implicated in disorders of compulsive behavior. Inspired by evidence that modulating orbitofrontal cortex activity can alter inference-based behaviors, here we discuss non-invasive approaches to target these circuits in humans. Specifically, we discuss the potential of network-targeted transcranial magnetic stimulation and real-time neurofeedback to modulate the neural underpinnings of inference. Both interventions leverage recent advances in our understanding of the neurocomputational mechanisms of inference-based behavior and may be used to complement current treatment approaches for behavioral disorders.

      KEYWORDS

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      REFERENCES

        • Redish A.D.
        • Jensen S.
        • Johnson A.
        A unified framework for addiction: vulnerabilities in the decision process.
        The Behavioral and brain sciences. 2008; 31 (; discussion 437-487): 415-437
        • Balleine B.W.
        • Delgado M.R.
        • Hikosaka O.
        The role of the dorsal striatum in reward and decision-making.
        J Neurosci. 2007; 27: 8161-8165
        • O'Doherty J.P.
        • Cockburn J.
        • Pauli W.M.
        Learning, Reward, and Decision Making.
        Annu Rev Psychol. 2017; 68: 73-100
        • Behrens T.E.J.
        • Muller T.H.
        • Whittington J.C.R.
        • Mark S.
        • Baram A.B.
        • Stachenfeld K.L.
        • et al.
        What Is a Cognitive Map? Organizing Knowledge for Flexible Behavior.
        Neuron. 2018; 100: 490-509
        • Balleine B.W.
        The Meaning of Behavior: Discriminating Reflex and Volition in the Brain.
        Neuron. 2019; 104: 47-62
        • Tricomi E.
        • Balleine B.W.
        • O'Doherty J.P.
        A specific role for posterior dorsolateral striatum in human habit learning.
        Eur J Neurosci. 2009; 29: 2225-2232
        • Yin H.H.
        • Knowlton B.J.
        • Balleine B.W.
        Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning.
        Eur J Neurosci. 2004; 19: 181-189
        • Malvaez M.
        • Wassum K.M.
        Regulation of habit formation in the dorsal striatum.
        Curr Opin Behav Sci. 2018; 20: 67-74
        • Wikenheiser A.M.
        • Schoenbaum G.
        Over the river, through the woods: cognitive maps in the hippocampus and orbitofrontal cortex.
        Nat Rev Neurosci. 2016; 17: 513-523
        • Yin H.H.
        • Knowlton B.J.
        • Balleine B.W.
        Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning.
        Eur J Neurosci. 2005; 22: 505-512
        • Atallah H.E.
        • McCool A.D.
        • Howe M.W.
        • Graybiel A.M.
        Neurons in the ventral striatum exhibit cell-type-specific representations of outcome during learning.
        Neuron. 2014; 82: 1145-1156
        • Kahnt T.
        • Schoenbaum G.
        Cross-species studies on orbitofrontal control of inference-based behavior.
        Behav Neurosci. 2021; 135: 109-119
        • Wang F.
        • Kahnt T.
        Neural circuits for inference-based decision-making.
        Curr Opin Behav Sci. 2021; 41: 10-14
        • Wilson R.C.
        • Takahashi Y.K.
        • Schoenbaum G.
        • Niv Y.
        Orbitofrontal cortex as a cognitive map of task space.
        Neuron. 2014; 81: 267-279
        • Buckner R.L.
        The role of the hippocampus in prediction and imagination.
        Annu Rev Psychol. 2010; 61: C21-28
        • Malvaez M.
        • Shieh C.
        • Murphy M.D.
        • Greenfield V.Y.
        • Wassum K.M.
        Distinct cortical-amygdala projections drive reward value encoding and retrieval.
        Nat Neurosci. 2019; 22: 762-769
        • Fiuzat E.C.
        • Rhodes S.E.
        • Murray E.A.
        The Role of Orbitofrontal-Amygdala Interactions in Updating Action-Outcome Valuations in Macaques.
        J Neurosci. 2017; 37: 2463-2470
        • Malkova L.
        • Gaffan D.
        • Murray E.A.
        Excitotoxic lesions of the amygdala fail to produce impairment in visual learning for auditory secondary reinforcement but interfere with reinforcer devaluation effects in rhesus monkeys.
        J Neurosci. 1997; 17: 6011-6020
        • Jones J.L.
        • Esber G.R.
        • McDannald M.A.
        • Gruber A.J.
        • Hernandez A.
        • Mirenzi A.
        • et al.
        Orbitofrontal cortex supports behavior and learning using inferred but not cached values.
        Science. 2012; 338: 953-956
        • Rudebeck P.H.
        • Saunders R.C.
        • Prescott A.T.
        • Chau L.S.
        • Murray E.A.
        Prefrontal mechanisms of behavioral flexibility, emotion regulation and value updating.
        Nat Neurosci. 2013; 16: 1140-1145
        • Daw N.D.
        • Niv Y.
        • Dayan P.
        Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control.
        Nat Neurosci. 2005; 8: 1704-1711
        • Lee S.W.
        • Shimojo S.
        • O'Doherty J.P.
        Neural computations underlying arbitration between model-based and model-free learning.
        Neuron. 2014; 81: 687-699
        • Schoenbaum G.
        • Chang C.Y.
        • Lucantonio F.
        • Takahashi Y.K.
        Thinking Outside the Box: Orbitofrontal Cortex, Imagination, and How We Can Treat Addiction.
        Neuropsychopharmacology. 2016; 41: 2966-2976
        • Luscher C.
        • Robbins T.W.
        • Everitt B.J.
        The transition to compulsion in addiction.
        Nat Rev Neurosci. 2020; 21: 247-263
        • Friedman N.P.
        • Robbins T.W.
        The role of prefrontal cortex in cognitive control and executive function.
        Neuropsychopharmacology. 2022; 47: 72-89
        • Groman S.M.
        • Massi B.
        • Mathias S.R.
        • Lee D.
        • Taylor J.R.
        Model-Free and Model-Based Influences in Addiction-Related Behaviors.
        Biol Psychiatry. 2019; 85: 936-945
        • Robbins T.W.
        • Vaghi M.M.
        • Banca P.
        Obsessive-Compulsive Disorder: Puzzles and Prospects.
        Neuron. 2019; 102: 27-47
        • Gillan C.M.
        • Papmeyer M.
        • Morein-Zamir S.
        • Sahakian B.J.
        • Fineberg N.A.
        • Robbins T.W.
        • et al.
        Disruption in the balance between goal-directed behavior and habit learning in obsessive-compulsive disorder.
        Am J Psychiatry. 2011; 168: 718-726
        • Voon V.
        • Derbyshire K.
        • Ruck C.
        • Irvine M.A.
        • Worbe Y.
        • Enander J.
        • et al.
        Disorders of compulsivity: a common bias towards learning habits.
        Mol Psychiatry. 2015; 20: 345-352
        • Everitt B.J.
        • Robbins T.W.
        Drug Addiction: Updating Actions to Habits to Compulsions Ten Years On.
        Annu Rev Psychol. 2016; 67: 23-50
        • Kalivas P.W.
        • Volkow N.
        • Seamans J.
        Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission.
        Neuron. 2005; 45: 647-650
        • Kalivas P.W.
        • Volkow N.D.
        The neural basis of addiction: a pathology of motivation and choice.
        Am J Psychiatry. 2005; 162: 1403-1413
        • Young K.A.
        • Franklin T.R.
        • Roberts D.C.S.
        • Jagannathan K.
        • Suh J.J.
        • Wetherill R.R.
        • et al.
        Nipping Cue Reactivity in the Bud: Baclofen Prevents Limbic Activation Elicited by Subliminal Drug Cues.
        J Neurosci. 2014; 34: 5038-5043
        • Ersche K.D.
        • Lim T.V.
        • Murley A.G.
        • Rua C.
        • Vaghi M.M.
        • White T.L.
        • et al.
        Reduced Glutamate Turnover in the Putamen Is Linked With Automatic Habits in Human Cocaine Addiction.
        Biol Psychiatry. 2021; 89: 970-979
        • Goldstein R.Z.
        • Tomasi D.
        • Alia-Klein N.
        • Honorio Carrillo J.
        • Maloney T.
        • Woicik P.A.
        • et al.
        Dopaminergic response to drug words in cocaine addiction.
        J Neurosci. 2009; 29: 6001-6006
        • Everitt B.J.
        • Robbins T.W.
        Neural systems of reinforcement for drug addiction: from actions to habits to compulsion.
        Nat Neurosci. 2005; 8: 1481-1489
        • Zilverstand A.
        • Huang A.S.
        • Alia-Klein N.
        • Goldstein R.Z.
        Neuroimaging Impaired Response Inhibition and Salience Attribution in Human Drug Addiction: A Systematic Review.
        Neuron. 2018; 98: 886-903
        • Wilson S.J.
        • Sayette M.A.
        • Fiez J.A.
        Prefrontal responses to drug cues: a neurocognitive analysis.
        Nat Neurosci. 2004; 7: 211-214
        • Ersche K.D.
        • Gillan C.M.
        • Jones P.S.
        • Williams G.B.
        • Ward L.H.
        • Luijten M.
        • et al.
        Carrots and sticks fail to change behavior in cocaine addiction.
        Science. 2016; 352: 1468-1471
        • Wied H.M.
        • Jones J.L.
        • Cooch N.K.
        • Berg B.A.
        • Schoenbaum G.
        Disruption of model-based behavior and learning by cocaine self-administration in rats.
        Psychopharmacology (Berl). 2013; 229: 493-501
      1. Lucantonio F, Caprioli D, Schoenbaum G (2014): Transition from 'model-based' to 'model-free' behavioral control in addiction: Involvement of the orbitofrontal cortex and dorsolateral striatum. Neuropharmacology. 76 Pt B:407-415.

        • Carmichael S.T.
        • Price J.L.
        Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys.
        J Comp Neurol. 1996; 371: 179-207
        • Zald D.H.
        • McHugo M.
        • Ray K.L.
        • Glahn D.C.
        • Eickhoff S.B.
        • Laird A.R.
        Meta-analytic connectivity modeling reveals differential functional connectivity of the medial and lateral orbitofrontal cortex.
        Cereb Cortex. 2014; 24: 232-248
        • Kahnt T.
        • Tobler P.N.
        Dopamine Modulates the Functional Organization of the Orbitofrontal Cortex.
        J Neurosci. 2017; 37: 1493-1504
        • Kahnt T.
        • Chang L.J.
        • Park S.Q.
        • Heinzle J.
        • Haynes J.D.
        Connectivity-based parcellation of the human orbitofrontal cortex.
        J Neurosci. 2012; 32: 6240-6250
        • Lopez-Persem A.
        • Bastin J.
        • Petton M.
        • Abitbol R.
        • Lehongre K.
        • Adam C.
        • et al.
        Four core properties of the human brain valuation system demonstrated in intracranial signals.
        Nat Neurosci. 2020; 23: 664-675
        • Howard J.D.
        • Kahnt T.
        Identity-Specific Reward Representations in Orbitofrontal Cortex Are Modulated by Selective Devaluation.
        J Neurosci. 2017; 37: 2627-2638
        • Chib V.S.
        • Rangel A.
        • Shimojo S.
        • O'Doherty J.P.
        Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex.
        J Neurosci. 2009; 29: 12315-12320
        • Howard J.D.
        • Kahnt T.
        To be specific: The role of orbitofrontal cortex in signaling reward identity.
        Behav Neurosci. 2021; 135: 210-217
        • McNamee D.
        • Rangel A.
        • O'Doherty J.P.
        Category-dependent and category-independent goal-value codes in human ventromedial prefrontal cortex.
        Nat Neurosci. 2013; 16: 479-485
        • Howard J.D.
        • Gottfried J.A.
        • Tobler P.N.
        • Kahnt T.
        Identity-specific coding of future rewards in the human orbitofrontal cortex.
        Proc Natl Acad Sci U S A. 2015; 112: 5195-5200
        • Zeithamova D.
        • Dominick A.L.
        • Preston A.R.
        Hippocampal and ventral medial prefrontal activation during retrieval-mediated learning supports novel inference.
        Neuron. 2012; 75: 168-179
        • Morton N.W.
        • Schlichting M.L.
        • Preston A.R.
        Representations of common event structure in medial temporal lobe and frontoparietal cortex support efficient inference.
        Proc Natl Acad Sci U S A. 2020; 117: 29338-29345
        • Wang F.
        • Schoenbaum G.
        • Kahnt T.
        Interactions between human orbitofrontal cortex and hippocampus support model-based inference.
        PLoS Biol. 2020; 18e3000578
        • Wang F.
        • Howard J.D.
        • Voss J.L.
        • Schoenbaum G.
        • Kahnt T.
        Targeted Stimulation of an Orbitofrontal Network Disrupts Decisions Based on Inferred, Not Experienced Outcomes.
        J Neurosci. 2020; 40: 8726-8733
        • Holland P.C.
        • Straub J.J.
        Differential effects of two ways of devaluing the unconditioned stimulus after Pavlovian appetitive conditioning.
        J Exp Psychol Anim Behav Process. 1979; 5: 65-78
        • Colwill R.M.
        • Rescorla R.A.
        Postconditioning Devaluation of a Reinforcer Affects Instrumental Responding.
        J Exp Psychol Anim B. 1985; 11: 120-132
        • Murray E.A.
        • Moylan E.J.
        • Saleem K.S.
        • Basile B.M.
        • Turchi J.
        Specialized areas for value updating and goal selection in the primate orbitofrontal cortex.
        Elife. 2015; 4
        • Reber J.
        • Feinstein J.S.
        • O'Doherty J.P.
        • Liljeholm M.
        • Adolphs R.
        • Tranel D.
        Selective impairment of goal-directed decision-making following lesions to the human ventromedial prefrontal cortex.
        Brain. 2017; 140: 1743-1756
        • Howard J.D.
        • Reynolds R.
        • Smith D.E.
        • Voss J.L.
        • Schoenbaum G.
        • Kahnt T.
        Targeted Stimulation of Human Orbitofrontal Networks Disrupts Outcome-Guided Behavior.
        Curr Biol. 2020; 30: 490-498 e494
        • Stalnaker T.A.
        • Cooch N.K.
        • McDannald M.A.
        • Liu T.L.
        • Wied H.
        • Schoenbaum G.
        Orbitofrontal neurons infer the value and identity of predicted outcomes.
        Nat Commun. 2014; 5: 3926
        • Howard J.D.
        • Kahnt T.
        Identity prediction errors in the human midbrain update reward-identity expectations in the orbitofrontal cortex.
        Nat Commun. 2018; 9: 1611
        • Critchley H.D.
        • Rolls E.T.
        Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex.
        J Neurophysiol. 1996; 75: 1673-1686
        • Gottfried J.A.
        • O'Doherty J.
        • Dolan R.J.
        Encoding predictive reward value in human amygdala and orbitofrontal cortex.
        Science. 2003; 301: 1104-1107
        • Gallagher M.
        • McMahan R.W.
        • Schoenbaum G.
        Orbitofrontal cortex and representation of incentive value in associative learning.
        J Neurosci. 1999; 19: 6610-6614
        • Gardner M.P.H.
        • Conroy J.S.
        • Shaham M.H.
        • Styer C.V.
        • Schoenbaum G.
        Lateral Orbitofrontal Inactivation Dissociates Devaluation-Sensitive Behavior and Economic Choice.
        Neuron. 2017; 96: 1192-1203 e1194
        • Parkes S.L.
        • Ravassard P.M.
        • Cerpa J.C.
        • Wolff M.
        • Ferreira G.
        • Coutureau E.
        Insular and Ventrolateral Orbitofrontal Cortices Differentially Contribute to Goal-Directed Behavior in Rodents.
        Cereb Cortex. 2018; 28: 2313-2325
        • Izquierdo A.
        • Suda R.K.
        • Murray E.A.
        Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency.
        J Neurosci. 2004; 24: 7540-7548
        • West E.A.
        • DesJardin J.T.
        • Gale K.
        • Malkova L.
        Transient inactivation of orbitofrontal cortex blocks reinforcer devaluation in macaques.
        J Neurosci. 2011; 31: 15128-15135
        • Rhodes S.E.
        • Murray E.A.
        Differential effects of amygdala, orbital prefrontal cortex, and prelimbic cortex lesions on goal-directed behavior in rhesus macaques.
        J Neurosci. 2013; 33: 3380-3389
        • Hoffeld D.R.
        • Kendall S.B.
        • Thompson R.F.
        • Brogden W.J.
        Effect of amount of preconditioning training upon the magnitude of sensory preconditioning.
        Journal of Experimental Psychology. 1960; 59: 198-204
        • Brogden W.J.
        Sensory pre-conditioning.
        Journal of Experimental Psychology. 1939; 25: 323-332
        • Sadacca B.F.
        • Jones J.L.
        • Schoenbaum G.
        Midbrain dopamine neurons compute inferred and cached value prediction errors in a common framework.
        Elife. 2016; 5
        • Sharpe M.J.
        • Batchelor H.M.
        • Schoenbaum G.
        Preconditioned cues have no value.
        Elife. 2017; 6
        • Sadacca B.F.
        • Wied H.M.
        • Lopatina N.
        • Saini G.K.
        • Nemirovsky D.
        • Schoenbaum G.
        Orbitofrontal neurons signal sensory associations underlying model-based inference in a sensory preconditioning task.
        Elife. 2018; 7
        • Hart E.E.
        • Gardner M.P.H.
        • Schoenbaum G.
        Anterior cingulate neurons signal neutral cue pairings during sensory preconditioning.
        Curr Biol. 2022; 32: 725-732 e723
        • Hart E.E.
        • Sharpe M.J.
        • Gardner M.P.
        • Schoenbaum G.
        Responding to preconditioned cues is devaluation sensitive and requires orbitofrontal cortex during cue-cue learning.
        Elife. 2020; 9
        • Roberts A.C.
        Primate orbitofrontal cortex and adaptive behaviour.
        Trends Cogn Sci. 2006; 10: 83-90
        • Berlin H.A.
        • Rolls E.T.
        • Kischka U.
        Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions.
        Brain. 2004; 127: 1108-1126
        • Zald D.H.
        • Andreotti C.
        Neuropsychological assessment of the orbital and ventromedial prefrontal cortex.
        Neuropsychologia. 2010; 48: 3377-3391
        • Franklin T.R.
        • Acton P.D.
        • Maldjian J.A.
        • Gray J.D.
        • Croft J.R.
        • Dackis C.A.
        • et al.
        Decreased gray matter concentration in the insular, orbitofrontal, cingulate, and temporal cortices of cocaine patients.
        Biol Psychiatry. 2002; 51: 134-142
        • Goldstein R.Z.
        • Tomasi D.
        • Rajaram S.
        • Cottone L.A.
        • Zhang L.
        • Maloney T.
        • et al.
        Role of the anterior cingulate and medial orbitofrontal cortex in processing drug cues in cocaine addiction.
        Neuroscience. 2007; 144: 1153-1159
        • Volkow N.D.
        • Fowler J.S.
        Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex.
        Cereb Cortex. 2000; 10: 318-325
        • Ersche K.D.
        • Williams G.B.
        • Robbins T.W.
        • Bullmore E.T.
        Meta-analysis of structural brain abnormalities associated with stimulant drug dependence and neuroimaging of addiction vulnerability and resilience.
        Curr Opin Neurobiol. 2013; 23: 615-624
        • Nakao T.
        • Okada K.
        • Kanba S.
        Neurobiological model of obsessive-compulsive disorder: evidence from recent neuropsychological and neuroimaging findings.
        Psychiatry Clin Neurosci. 2014; 68: 587-605
        • Menzies L.
        • Chamberlain S.R.
        • Laird A.R.
        • Thelen S.M.
        • Sahakian B.J.
        • Bullmore E.T.
        Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited.
        Neurosci Biobehav Rev. 2008; 32: 525-549
        • Ahmari S.E.
        Using mice to model Obsessive Compulsive Disorder: From genes to circuits.
        Neuroscience. 2016; 321: 121-137
        • Xue A.M.
        • Foerde K.
        • Walsh B.T.
        • Steinglass J.E.
        • Shohamy D.
        • Bakkour A.
        Neural Representations of Food-Related Attributes in the Human Orbitofrontal Cortex during Choice Deliberation in Anorexia Nervosa.
        J Neurosci. 2022; 42: 109-120
        • Adinoff B.
        • Devous M.D.
        • Sr .,
        • Cooper D.B.
        • Best S.E.
        • Chandler P.
        • Harris T.
        • et al.
        Resting regional cerebral blood flow and gambling task performance in cocaine-dependent subjects and healthy comparison subjects.
        Am J Psychiatry. 2003; 160: 1892-1894
        • Smith D.G.
        • Jones P.S.
        • Williams G.B.
        • Bullmore E.T.
        • Robbins T.W.
        • Ersche K.D.
        Overlapping decline in orbitofrontal gray matter volume related to cocaine use and body mass index.
        Addiction biology. 2015; 20: 194-196
        • Ersche K.D.
        • Barnes A.
        • Jones P.S.
        • Morein-Zamir S.
        • Robbins T.W.
        • Bullmore E.T.
        Abnormal structure of frontostriatal brain systems is associated with aspects of impulsivity and compulsivity in cocaine dependence.
        Brain. 2011; 134: 2013-2024
        • Ersche K.D.
        • Jones P.S.
        • Williams G.B.
        • Smith D.G.
        • Bullmore E.T.
        • Robbins T.W.
        Distinctive personality traits and neural correlates associated with stimulant drug use versus familial risk of stimulant dependence.
        Biol Psychiatry. 2013; 74: 137-144
        • Goldstein R.Z.
        • Alia-Klein N.
        • Tomasi N.D.
        • Zhang L.
        • Cottone L.A.
        • Maloney T.
        • et al.
        Is Decreased Prefrontal Cortical Sensitivity to Monetary Reward Associated With Impaired Motivation and Self-Control in Cocaine Addiction?.
        American Journal of Psychiatry. 2007; 164: 43-51
        • Bachi K.
        • Parvaz M.A.
        • Moeller S.J.
        • Gan G.
        • Zilverstand A.
        • Goldstein R.Z.
        • et al.
        Reduced Orbitofrontal Gray Matter Concentration as a Marker of Premorbid Childhood Trauma in Cocaine Use Disorder.
        Front Hum Neurosci. 2018; 12: 51
        • Ersche K.D.
        • Meng C.
        • Ziauddeen H.
        • Stochl J.
        • Williams G.B.
        • Bullmore E.T.
        • et al.
        Brain networks underlying vulnerability and resilience to drug addiction.
        Proc Natl Acad Sci U S A. 2020; 117: 15253-15261
        • Harrison B.J.
        • Soriano-Mas C.
        • Pujol J.
        • Ortiz H.
        • Lopez-Sola M.
        • Hernandez-Ribas R.
        • et al.
        Altered corticostriatal functional connectivity in obsessive-compulsive disorder.
        Arch Gen Psychiatry. 2009; 66: 1189-1200
        • Chamberlain S.R.
        • Menzies L.
        • Hampshire A.
        • Suckling J.
        • Fineberg N.A.
        • del Campo N.
        • et al.
        Orbitofrontal dysfunction in patients with obsessive-compulsive disorder and their unaffected relatives.
        Science. 2008; 321: 421-422
        • Lucantonio F.
        • Stalnaker T.A.
        • Shaham Y.
        • Niv Y.
        • Schoenbaum G.
        The impact of orbitofrontal dysfunction on cocaine addiction.
        Nat Neurosci. 2012; 15: 358-366
        • Moorman D.E.
        The role of the orbitofrontal cortex in alcohol use, abuse, and dependence.
        Progress in neuro-psychopharmacology & biological psychiatry. 2018;
        • Lucantonio F.
        • Takahashi Y.K.
        • Hoffman A.F.
        • Chang C.Y.
        • Bali-Chaudhary S.
        • Shaham Y.
        • et al.
        Orbitofrontal activation restores insight lost after cocaine use.
        Nat Neurosci. 2014; 17: 1092-1099
        • Nimitvilai S.
        • Uys J.D.
        • Woodward J.J.
        • Randall P.K.
        • Ball L.E.
        • Williams R.W.
        • et al.
        Orbitofrontal neuroadaptations and cross-species synaptic biomarkers in heavy drinking macaques.
        J Neurosci. 2017;
        • Takahashi Y.K.
        • Roesch M.R.
        • Stalnaker T.A.
        • Haney R.Z.
        • Calu D.J.
        • Taylor A.R.
        • et al.
        The orbitofrontal cortex and ventral tegmental area are necessary for learning from unexpected outcomes.
        Neuron. 2009; 62: 269-280
        • Lucantonio F.
        • Kambhampati S.
        • Haney R.Z.
        • Atalayer D.
        • Rowland N.E.
        • Shaham Y.
        • et al.
        Effects of prior cocaine versus morphine or heroin self-administration on extinction learning driven by overexpectation versus omission of reward.
        Biol Psychiatry. 2015; 77: 912-920
        • West E.A.
        • Niedringhaus M.
        • Ortega H.K.
        • Haake R.M.
        • Frohlich F.
        • Carelli R.M.
        Noninvasive Brain Stimulation Rescues Cocaine-Induced Prefrontal Hypoactivity and Restores Flexible Behavior.
        Biol Psychiatry. 2021; 89: 1001-1011
        • Chen B.T.
        • Yau H.J.
        • Hatch C.
        • Kusumoto-Yoshida I.
        • Cho S.L.
        • Hopf F.W.
        • et al.
        Rescuing cocaine-induced prefrontal cortex hypoactivity prevents compulsive cocaine seeking.
        Nature. 2013; 496: 359-362
        • Folloni D.
        • Verhagen L.
        • Mars R.B.
        • Fouragnan E.
        • Constans C.
        • Aubry J.F.
        • et al.
        Manipulation of Subcortical and Deep Cortical Activity in the Primate Brain Using Transcranial Focused Ultrasound Stimulation.
        Neuron. 2019; 101: 1109-1116 e1105
        • Polania R.
        • Nitsche M.A.
        • Ruff C.C.
        Studying and modifying brain function with non-invasive brain stimulation.
        Nat Neurosci. 2018; 21: 174-187
        • Lefaucheur J.P.
        Transcranial magnetic stimulation.
        Hand Clinic. 2019; 160: 559-580
        • Vlachos A.
        • Muller-Dahlhaus F.
        • Rosskopp J.
        • Lenz M.
        • Ziemann U.
        • Deller T.
        Repetitive magnetic stimulation induces functional and structural plasticity of excitatory postsynapses in mouse organotypic hippocampal slice cultures.
        J Neurosci. 2012; 32: 17514-17523
        • Brown J.C.
        • DeVries W.H.
        • Korte J.E.
        • Sahlem G.L.
        • Bonilha L.
        • Short E.B.
        • et al.
        NMDA receptor partial agonist, d-cycloserine, enhances 10 Hz rTMS-induced motor plasticity, suggesting long-term potentiation (LTP) as underlying mechanism.
        Brain stimulation. 2020; 13: 530-532
        • Hanlon C.A.
        • Dowdle L.T.
        • Correia B.
        • Mithoefer O.
        • Kearney-Ramos T.
        • Lench D.
        • et al.
        Left frontal pole theta burst stimulation decreases orbitofrontal and insula activity in cocaine users and alcohol users.
        Drug and alcohol dependence. 2017; 178: 310-317
        • Li X.
        • Sahlem G.L.
        • Badran B.W.
        • McTeague L.M.
        • Hanlon C.A.
        • Hartwell K.J.
        • et al.
        Transcranial magnetic stimulation of the dorsal lateral prefrontal cortex inhibits medial orbitofrontal activity in smokers.
        Am J Addict. 2017; 26: 788-794
        • Ekhtiari H.
        • Tavakoli H.
        • Addolorato G.
        • Baeken C.
        • Bonci A.
        • Campanella S.
        • et al.
        Transcranial electrical and magnetic stimulation (tES and TMS) for addiction medicine: A consensus paper on the present state of the science and the road ahead.
        Neurosci Biobehav Rev. 2019; 104: 118-140
        • Rapinesi C.
        • Kotzalidis G.D.
        • Ferracuti S.
        • Sani G.
        • Girardi P.
        • Del Casale A.
        Brain Stimulation in Obsessive-Compulsive Disorder (OCD): A Systematic Review.
        Curr Neuropharmacol. 2019; 17: 787-807
        • Nauczyciel C.
        • Le Jeune F.
        • Naudet F.
        • Douabin S.
        • Esquevin A.
        • Verin M.
        • et al.
        Repetitive transcranial magnetic stimulation over the orbitofrontal cortex for obsessive-compulsive disorder: a double-blind, crossover study.
        Translational psychiatry. 2014; 4: e436
        • Nakamura-Palacios E.M.
        • Lopes I.B.
        • Souza R.A.
        • Klauss J.
        • Batista E.K.
        • Conti C.L.
        • et al.
        Ventral medial prefrontal cortex (vmPFC) as a target of the dorsolateral prefrontal modulation by transcranial direct current stimulation (tDCS) in drug addiction.
        J Neural Transm (Vienna). 2016; 123: 1179-1194
        • Price R.B.
        • Gillan C.M.
        • Hanlon C.
        • Ferrarelli F.
        • Kim T.
        • Karim H.T.
        • et al.
        Effect of Experimental Manipulation of the Orbitofrontal Cortex on Short-Term Markers of Compulsive Behavior: A Theta Burst Stimulation Study.
        Am J Psychiatry. 2021; 178: 459-468
        • Paus T.
        • Jech R.
        • Thompson C.J.
        • Comeau R.
        • Peters T.
        • Evans A.C.
        Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex.
        J Neurosci. 1997; 17: 3178-3184
        • Cho S.S.
        • Strafella A.P.
        rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex.
        PLoS One. 2009; 4e6725
        • Strafella A.P.
        • Paus T.
        • Barrett J.
        • Dagher A.
        Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus.
        J Neurosci. 2001; 21: RC157
        • van Schouwenburg M.R.
        • O'Shea J.
        • Mars R.B.
        • Rushworth M.F.
        • Cools R.
        Controlling human striatal cognitive function via the frontal cortex.
        J Neurosci. 2012; 32: 5631-5637
        • Bergmann T.O.
        • Varatheeswaran R.
        • Hanlon C.A.
        • Madsen K.H.
        • Thielscher A.
        • Siebner H.R.
        Concurrent TMS-fMRI for causal network perturbation and proof of target engagement.
        Neuroimage. 2021; 237118093
        • Gratton C.
        • Lee T.G.
        • Nomura E.M.
        • D'Esposito M.
        The effect of theta-burst TMS on cognitive control networks measured with resting state fMRI.
        Frontiers in systems neuroscience. 2013; 7: 124
        • Hebscher M.
        • Voss J.L.
        Testing network properties of episodic memory using non-invasive brain stimulation.
        Curr Opin Behav Sci. 2020; 32: 35-42
        • Luber B.
        • Davis S.W.
        • Deng Z.D.
        • Murphy D.
        • Martella A.
        • Peterchev A.V.
        • et al.
        Using diffusion tensor imaging to effectively target TMS to deep brain structures.
        Neuroimage. 2022; 249118863
        • Wang J.X.
        • Rogers L.M.
        • Gross E.Z.
        • Ryals A.J.
        • Dokucu M.E.
        • Brandstatt K.L.
        • et al.
        Targeted enhancement of cortical-hippocampal brain networks and associative memory.
        Science. 2014; 345: 1054-1057
        • Howard J.D.
        • Kahnt T.
        Causal investigations into orbitofrontal control of human decision making.
        Curr Opin Behav Sci. 2021; 38: 14-19
        • Weiss F.
        • Zhang J.
        • Aslan A.
        • Kirsch P.
        • Gerchen M.F.
        Feasibility of training the dorsolateral prefrontal-striatal network by real-time fMRI neurofeedback.
        Scientific reports. 2022; 12: 1669
        • Scheinost D.
        • Hsu T.W.
        • Avery E.W.
        • Hampson M.
        • Constable R.T.
        • Chun M.M.
        • et al.
        Connectome-based neurofeedback: A pilot study to improve sustained attention.
        Neuroimage. 2020; 212116684
        • Watanabe T.
        • Sasaki Y.
        • Shibata K.
        • Kawato M.
        Advances in fMRI Real-Time Neurofeedback.
        Trends Cogn Sci. 2017; 21: 997-1010
        • Shibata K.
        • Watanabe T.
        • Sasaki Y.
        • Kawato M.
        Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.
        Science. 2011; 334: 1413-1415
        • Taschereau-Dumouchel V.
        • Cortese A.
        • Chiba T.
        • Knotts J.D.
        • Kawato M.
        • Lau H.
        Towards an unconscious neural reinforcement intervention for common fears.
        Proc Natl Acad Sci U S A. 2018; 115: 3470-3475
      2. Taschereau-Dumouchel V, Cushing C, Lau H (2022): Real-Time Functional MRI in the Treatment of Mental Health Disorders. Annual review of clinical psychology.

        • Bartholdy S.
        • Musiat P.
        • Campbell I.C.
        • Schmidt U.
        The potential of neurofeedback in the treatment of eating disorders: a review of the literature.
        European eating disorders review : the journal of the Eating Disorders Association. 2013; 21: 456-463
        • Surmeli T.
        • Ertem A.
        Obsessive compulsive disorder and the efficacy of qEEG-guided neurofeedback treatment: a case series.
        Clinical EEG and neuroscience. 2011; 42: 195-201
        • Martz M.E.
        • Hart T.
        • Heitzeg M.M.
        • Peltier S.J.
        Neuromodulation of brain activation associated with addiction: A review of real-time fMRI neurofeedback studies.
        Neuroimage Clin. 2020; 27102350
        • Hanlon C.A.
        • Hartwell K.J.
        • Canterberry M.
        • Li X.
        • Owens M.
        • Lematty T.
        • et al.
        Reduction of cue-induced craving through realtime neurofeedback in nicotine users: the role of region of interest selection and multiple visits.
        Psychiatry research. 2013; 213: 79-81
        • Li X.
        • Hartwell K.J.
        • Borckardt J.
        • Prisciandaro J.J.
        • Saladin M.E.
        • Morgan P.S.
        • et al.
        Volitional reduction of anterior cingulate cortex activity produces decreased cue craving in smoking cessation: a preliminary real-time fMRI study.
        Addiction biology. 2013; 18: 739-748
        • Hartwell K.J.
        • Hanlon C.A.
        • Li X.
        • Borckardt J.J.
        • Canterberry M.
        • Prisciandaro J.J.
        • et al.
        Individualized real-time fMRI neurofeedback to attenuate craving in nicotine-dependent smokers.
        Journal of psychiatry & neuroscience : JPN. 2016; 41: 48-55
        • Horrell T.
        • El-Baz A.
        • Baruth J.
        • Tasman A.
        • Sokhadze G.
        • Stewart C.
        • et al.
        Neurofeedback Effects on Evoked and Induced EEG Gamma Band Reactivity to Drug-related Cues in Cocaine Addiction.
        Journal of neurotherapy. 2010; 14: 195-216
        • Karch S.
        • Keeser D.
        • Hummer S.
        • Paolini M.
        • Kirsch V.
        • Karali T.
        • et al.
        Modulation of Craving Related Brain Responses Using Real-Time fMRI in Patients with Alcohol Use Disorder.
        PLoS One. 2015; 10e0133034
        • Subramanian L.
        • Skottnik L.
        • Cox W.M.
        • Luhrs M.
        • McNamara R.
        • Hood K.
        • et al.
        Neurofeedback Training versus Treatment-as-Usual for Alcohol Dependence: Results of an Early-Phase Randomized Controlled Trial and Neuroimaging Correlates.
        European addiction research. 2021; 27: 381-394
      3. Karch S, Krause D, Lehnert K, Konrad J, Haller D, Rauchmann BS, et al. (2021): Functional and clinical outcomes of FMRI-based neurofeedback training in patients with alcohol dependence: a pilot study. European archives of psychiatry and clinical neuroscience.

        • MacInnes J.J.
        • Dickerson K.C.
        • Chen N.K.
        • Adcock R.A.
        Cognitive Neurostimulation: Learning to Volitionally Sustain Ventral Tegmental Area Activation.
        Neuron. 2016; 89: 1331-1342
        • Kirschner M.
        • Sladky R.
        • Haugg A.
        • Stampfli P.
        • Jehli E.
        • Hodel M.
        • et al.
        Self-regulation of the dopaminergic reward circuit in cocaine users with mental imagery and neurofeedback.
        EBioMedicine. 2018; 37: 489-498
        • Cortese A.
        • Yamamoto A.
        • Hashemzadeh M.
        • Sepulveda P.
        • Kawato M.
        • De Martino B.
        Value signals guide abstraction during learning.
        Elife. 2021; 10
        • Weiss F.
        • Zamoscik V.
        • Schmidt S.N.L.
        • Halli P.
        • Kirsch P.
        • Gerchen M.F.
        Just a very expensive breathing training? Risk of respiratory artefacts in functional connectivity-based real-time fMRI neurofeedback.
        Neuroimage. 2020; 210116580
        • Sorger B.
        • Scharnowski F.
        • Linden D.E.J.
        • Hampson M.
        • Young K.D.
        Control freaks: Towards optimal selection of control conditions for fMRI neurofeedback studies.
        Neuroimage. 2019; 186: 256-265
        • Guerrero Moreno J.
        • Biazoli Jr., C.E.
        • Baptista A.F.
        • Trambaiolli L.R.
        Closed-loop neurostimulation for affective symptoms and disorders: An overview.
        Biological psychology. 2021; 161108081