Disruption in the balance between goal-directed behavior and habit learning in obsessive-compulsive disorder

Claire M Gillan, Martina Papmeyer, Sharon Morein-Zamir, Barbara J Sahakian, Naomi A Fineberg, Trevor W Robbins, Sanne de Wit, Claire M Gillan, Martina Papmeyer, Sharon Morein-Zamir, Barbara J Sahakian, Naomi A Fineberg, Trevor W Robbins, Sanne de Wit

Abstract

Objective: Obsessive-compulsive disorder (OCD) is characterized by repetitive, ritualistic behaviors and thought patterns. Although patients with OCD report that these compulsive behaviors are unproductive and often senseless, they are unable to desist. This study investigated whether the urge to perform compulsive acts is mediated by a disruption in the balance between flexible, goal-directed action control and habitual behavior.

Method: A total of 21 patients with OCD and 30 healthy comparison subjects participated in a set of tasks designed to assess relative goal-directed versus habitual behavioral control. In the training stage, participants were asked to respond to different pictured stimuli in order to gain rewarding outcomes. In the subsequent (instructed) outcome devaluation test and in a novel "slips-of-action" test, the authors assessed whether participants were able to flexibly adjust their behavior to changes in the desirability of the outcomes. The authors also used a questionnaire to test explicit knowledge of the relationships between stimuli, responses, and outcomes.

Results: Patients with OCD showed no deficit in their ability to use feedback to respond appropriately to stimuli in the training stage. However, their knowledge of the outcomes of these responses was impaired relative to healthy comparison subjects, and patients were more prone to slips of action, indicating a deficit in goal-directed control and an overreliance on habits.

Conclusions: This study provides the first experimental evidence for selective impairment in flexible and goal-directed behavioral control in patients with OCD. The impairment forces patients with OCD to rely instead on habits that can be triggered by stimuli regardless of the desirability of the consequences. Goal-directed actions are supported by orbitofronto-striatal circuitry, and the study findings are thus in line with findings from research that implicate dysfunction in this circuitry in the neuropathology of OCD.

Figures

FIGURE 1.
FIGURE 1.
Instrumental Learning Task Descriptiona a Panel A illustrates the three discrimination types: standard, congruent, and incongruent. Panel B illustrates the training phase. In this example from the standard discrimination, participants are presented with grapes on the outside of the box. If the incorrect (left) key is pressed, an empty box is revealed (and no points are earned). If the correct (right) key is pressed, participants are rewarded with cherries on the inside of the box (and points). Panel C illustrates the outcome devaluation test. In this example, participants are presented with two open boxes with a melon and cherries inside. The red cross (or X) superimposed on the cherries indicates that this fruit type is no longer worth any points. The correct response in this example would be to press the left key (which during training yielded the still-valuable melon outcome). Panel D illustrates the slips-of-action test. In this example, the initial instruction screen shows that the pineapple and cherries outcomes will now lead to the subtraction of points, as indicated by the red crosses. The other four outcomes are still valuable. Following the instruction screen, participants are presented with a rapid succession of the fruit stimuli (on the front door of the boxes) and are asked to press the correct keys (“Go”) when a stimulus signals the availability of a still-valuable outcome inside the box but to refrain from responding (“No-Go”) when the outcome inside the box has been devalued. In this particular example, participants should press the correct key when the apple stimulus is depicted on the front door (“Go”) but should refrain from responding to the grapes stimulus (“No-Go”).
FIGURE 2.
FIGURE 2.
Response Accuracy Over the Course of Six Blocks in the Instrumental Discrimination Training for Participants in a Study of Goal-Directed Behavior and Habit Learning in Obsessive-Compulsive Disorder (OCD)a a Error bars denote standard deviations.
FIGURE 3.
FIGURE 3.
Performance on the Slips-of-Action Test and the Explicit Response and Outcome Questionnaire in a Study of Goal-Directed Behavior and Habit Learning in Obsessive-Compulsive Disorder (OCD)a a The upper panel shows the percentage of responses made by the OCD and comparison groups in the slips-of-action test, and the lower panel shows the mean accuracy scores for the OCD and comparison groups on the explicit response and outcome questionnaire. Error bars denote standard deviations. b While there was no group difference in percentage response to valuable outcomes, patients with OCD responded significantly more often for outcomes that were devalued relative to comparison subjects (F=17.43, df=1, 38, p<0.001). c Groups did not differ in their knowledge of the correct responses from the training stage. Patients with OCD, however, showed significantly worse outcome knowledge relative to comparison subjects (F=14.92, df=1, 49, p<0.001).

References

    1. Fineberg NA, Potenza MN, Chamberlain SR, Berlin HA, Menzies L, Bechara A, Sahakian BJ, Robbins TW, Bullmore ET, Hollander E: Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review. Neuropsychopharmacology 2010; 35:591–604
    1. Graybiel AM, Rauch SL: Toward a neurobiology of obsessive-compulsive disorder. Neuron 2000; 28:343–347
    1. Boulougouris V, Chamberlain SR, Robbins TW: Cross-species models of OCD spectrum disorders. Psychiatry Res 2009; 170:15–21
    1. Dickinson A, Balleine B: Actions and responses: the dual psychology of behavior, in Spatial Representation: Problems in Philosophy and Psychology. Edited by Eilan N, McCarthy RA, Brewer B. Malden, Mass, Blackwell Scientific Publishing, 1993, pp 277–293
    1. de Wit S, Dickinson A: Associative theories of goal-directed behaviour: a case for animal-human translational models. Psychol Res 2009; 73:463–476
    1. Adams C, Dickinson A: Instrumental responding following reinforcer devaluation. Q J Exp Psychol 1981; 33:109–121
    1. Adams C: Variations in the sensitivity of instrumental responding to reinforcer devaluation. Q J Exp Psychol 1982; 34B:77–98
    1. Thorndike A: Animal Intelligence: Experimental Studies. New York, Macmillan, 1911
    1. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW: The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 2005; 22:513–523
    1. Killcross S, Coutureau E: Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 2003; 13:400–408
    1. Corbit LH, Balleine BW: The role of prelimbic cortex in instrumental conditioning. Behav Brain Res 2003; 146:145–157
    1. Valentin VV, Dickinson A, O'Doherty JP: Determining the neural substrates of goal-directed learning in the human brain. J Neurosci 2007; 27:4019–4026
    1. de Wit S, Corlett PR, Aitken MR, Dickinson A, Fletcher PC: Differential engagement of the ventromedial prefrontal cortex by goal-directed and habitual behavior toward food pictures in humans. J Neurosci 2009; 29:11330–11338
    1. Everitt BJ, Robbins TW: Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 2005; 8:1481–1489
    1. Menzies L, Williams GB, Chamberlain SR, Ooi C, Fineberg N, Suckling J, Sahakian BJ, Robbins TW, Bullmore ET: White matter abnormalities in patients with obsessive-compulsive disorder and their first-degree relatives. Am J Psychiatry 2008; 165:1308–1315
    1. Saxena S, Rauch SL: Functional neuroimaging and the neuroanatomy of obsessive-compulsive disorder. Psychiatr Clin North Am 2000; 23:563–586
    1. Tricomi EM, Delgado MR, Fiez JA: Modulation of caudate activity by action contingency. Neuron 2004; 41:281–292
    1. Tanaka SC, Balleine BW, O'Doherty JP: Calculating consequences: brain systems that encode the causal effects of actions. J Neurosci 2008; 28:6750–6755
    1. Yin HH, Knowlton BJ, Balleine BW: Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 2004; 19:181–189
    1. Tricomi E, Balleine BW, O'Doherty JP: A specific role for posterior dorsolateral striatum in human habit learning. Eur J Neurosci 2009; 29:2225–2232
    1. Coutureau E, Killcross S: Inactivation of the infralimbic prefrontal cortex reinstates goal-directed responding in overtrained rats. Behav Brain Res 2003; 146:167–174
    1. Alexander GE, DeLong MR, Strick PL: Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986; 9:357–381
    1. de Wit S, Barker RA, Dickinson T, Cools R: Habitual versus goal-directed action control in Parkinson's disease. J Cogn Neurosci 2011; 23:1218–1229
    1. de Wit S, Niry D, Wariyar R, Aitken MR, Dickinson A: Stimulus-outcome interactions during instrumental discrimination learning by rats and humans. J Exp Psychol Anim Behav Process 2007; 33:1–11
    1. Crockett MJ, Clark L, Robbins TW: Reconciling the role of serotonin in behavioral inhibition and aversion: acute tryptophan depletion abolishes punishment-induced inhibition in humans. J Neurosci 2009; 29:11993–11999
    1. Camille N, Coricelli G, Sallet J, Pradat-Diehl P, Duhamel JR, Sirigu A: The involvement of the orbitofrontal cortex in the experience of regret. Science 2004; 304:1167–1170
    1. Nelson HE: National Adult Reading Test (NART): Test Manual. Windsor, UK, NFER-Nelson, 1982
    1. Goodman WK, Price LH, Rasmussen SA, Mazure C, Fleischmann RL, Hill CL, Heninger GR, Charney DS: The Yale-Brown Obsessive Compulsive Scale (Y-BOCS), part 1: development, use, and reliability. Arch Gen Psychiatry 1989; 46:1006–1011
    1. Foa EB, Huppert JD, Leiberg S, Langner R, Kichic R, Hajcak G, Salkovskis PM: The Obsessive-Compulsive Inventory: development and validation of a short version. Psychol Assess 2002; 14:485–496
    1. Mataix-Cols D, Rosario-Campos MC, Leckman JF: A multidimensional model of obsessive-compulsive disorder. Am J Psychiatry 2005; 162:228–238
    1. Montgomery SA, Åsberg M: A new depression scale designed to be sensitive to change. Br J Psychiatry 1979; 134:382–389
    1. Spielberger CD: State-Trait Anxiety Inventory (STAI). Palo Alto, Calif, Consulting Psychologists Press, 1985
    1. Schwabe L, Wolf OT: Stress prompts habit behavior in humans. J Neurosci 2009; 29:7191–7198
    1. Schwabe L, Wolf OT: Socially evaluated cold pressor stress after instrumental learning favors habits over goal-directed action. Psychoneuroendocrinology 2010; 35:977–986
    1. Eysenck MW, Derakshan N, Santos R, Calvo MG: Anxiety and cognitive performance: attentional control theory. Emotion 2007; 7:336–353
    1. Glascher J, Hampton AN, O'Doherty JP: Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. Cereb Cortex 2009; 19:483–495
    1. Menzies L, Chamberlain SR, Laird AR, Thelen SM, Sahakian BJ, Bullmore ET: Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited. Neurosci Biobehav Rev 2008; 32:525–549
    1. Rauch SL, Jenike MA, Alpert NM, Baer L, Breiter HC, Savage CR, Fischman AJ: Regional cerebral blood flow measured during symptom provocation in obsessive-compulsive disorder using oxygen 15-labeled carbon dioxide and positron emission tomography. Arch Gen Psychiatry 1994; 51:62–70
    1. Saxena S, Brody AL, Schwartz JM, Baxter LR: Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder. Br J Psychiatry Suppl 1998; 35:26–37
    1. Chamberlain SR, Fineberg NA, Menzies LA, Blackwell AD, Bullmore ET, Robbins TW, Sahakian BJ: Impaired cognitive flexibility and motor inhibition in unaffected first-degree relatives of patients with obsessive-compulsive disorder. Am J Psychiatry 2007; 164:335–338
    1. Balleine BW, O'Doherty JP: Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 2010; 35:48–69
    1. Joel D, Zohar O, Afek M, Hermesh H, Lerner L, Kuperman R, Gross-Isseroff R, Weizman A, Inzelberg R: Impaired procedural learning in obsessive-compulsive disorder and Parkinson's disease, but not in major depressive disorder. Behav Brain Res 2005; 157:253–263
    1. Rauch SL, Wedig MM, Wright CI, Martis B, McMullin KG, Shin LM, Cannistraro PA, Wilhelm S: Functional magnetic resonance imaging study of regional brain activation during implicit sequence learning in obsessive-compulsive disorder. Biol Psychiatry 2007; 61:330–336
    1. Kathmann N, Rupertseder C, Hauke W, Zaudig M: Implicit sequence learning in obsessive-compulsive disorder: further support for the fronto-striatal dysfunction model. Biol Psychiatry 2005; 58:239–244
    1. de Wit S, Barker RA, Dickinson T, Cools R: Habitual versus goal-directed action control in Parkinson's disease. J Cogn Neurosci 2010; 23:1218–1229
    1. Clarke HF, Walker SC, Dalley JW, Robbins TW, Roberts AC: Cognitive inflexibility after prefrontal serotonin depletion is behaviorally and neurochemically specific. Cereb Cortex 2007; 17:18–27
    1. Nonkes LJ, Tomson K, Maertin A, Dederen J, Maes JH, Homberg J: Orbitofrontal cortex and amygdalar over-activity is associated with an inability to use the value of expected outcomes to guide behaviour in serotonin transporter knockout rats. Neurobiol Learn Mem 2010; 94:65–72

Source: PubMed

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