Obsessive Compulsive Disorder: A Pathology of Self-Confidence?
Authors: Julian Kiverstein, Erik Rietveld, Heleen A. Slagter, Damiaan Denys
Journal: Trends in Cognitive Sciences (2019)

A striking change OCD patients repeatedly describe following treatment with deep brain stimulation (DBS) of the ventral anterior limb of internal capsule (vALIC) is an immediate increase in self-confidence. We show how the DBS-induced changes in self-confidence reported by our patients can be understood neurocognitively in terms of active inference. A striking change OCD patients repeatedly describe following treatment with deep brain stimulation (DBS) of the ventral anterior limb of internal capsule (vALIC) is an immediate increase in self-confidence. We show how the DBS-induced changes in self-confidence reported by our patients can be understood neurocognitively in terms of active inference. Patients with obsessive compulsive disorder (OCD) experience unwanted intrusive thoughts ('obsessions') expressive of their anxious mode of relating to the world. They feel strong urges to repeatedly perform ritual-like behaviours ('compulsions'). Our group at the Amsterdam University Medical Center currently treats 80 treatment-refractory OCD patients with DBS, an innovative treatment method in which a 'neurostimulator' is surgically implanted, providing stimulation to areas deep in the brain. In our OCD patients, stimulation is applied to areas located in the ventral striatum, near the ventral anterior limb of the internal capsule (vALIC)/nucleus accumbens. In the first placebo-controlled clinical study published on striatal-DBS for OCD, our group demonstrated a 72% symptom reduction in responders [1Denys D. et al.Deep brain stimulation of the nucleus accumbens for treatment refractory obsessive-compulsive disorder.Arch. Gen. Psychiatry. 2010; 67: 1061-1068Crossref PubMed Scopus (510) Google Scholar]. In contrast to regular drug treatments, OCD patients responded to DBS immediately (sometimes within seconds to minutes) when adequate stimulation parameters were identified. One of the most striking changes patients repeatedly describe, both in the clinic and in qualitative interviews we carried out [2De Haan S. et al.Effects of deep brain stimulation on the lived experience of obsessive compulsive disorder patients: in-depth interviews with 18 patients.PLoS One. 2015; 10e0135524Crossref PubMed Scopus (69) Google Scholar], is an immediate and persisting increase in self-confidence. Simultaneously, patients report a reduction in anxiety-related obsessions, while improvement in compulsivity symptoms typically requires additional behavioural therapy. In this article, we propose that the primary effect of DBS may be to increase the patient's self-confidence. Our hypothesis is based in part on clinical observation and qualitative interviews we conducted [2De Haan S. et al.Effects of deep brain stimulation on the lived experience of obsessive compulsive disorder patients: in-depth interviews with 18 patients.PLoS One. 2015; 10e0135524Crossref PubMed Scopus (69) Google Scholar]. Furthermore, we have observed that when DBS stimulation parameters are set too high, the patient behaves more impulsively, a sign of excessive self-confidence [3Luigjes J. et al.Deep brain stimulation increases impulsivity in two patients with obsessive compulsive disorder.Int. Clin. Psychopharmocol. 2011; 26: 38-40Google Scholar]. Drawing on the active inference framework [4Friston K.F. et al.Active inference: a process theory.Neural Comput. 2017; 29: 1-49Crossref PubMed Scopus (456) Google Scholar], we hypothesise that DBS-induced changes in precision expectations may provide a neurocognitive explanation of the rapid change in self-confidence that our patients report. People are self-confident when they trust their abilities and surroundings. Self-confidence allows them to be open to the various action possibilities that are relevant to them [2De Haan S. et al.Effects of deep brain stimulation on the lived experience of obsessive compulsive disorder patients: in-depth interviews with 18 patients.PLoS One. 2015; 10e0135524Crossref PubMed Scopus (69) Google Scholar]. We will therefore understand self-confidence in terms of the person's experience of their power to act in the world. Self-confidence can be given a neurocognitive description in terms of 'active inference', the process of action selection that minimises the 'surprise' expected as a consequence of acting [4Friston K.F. et al.Active inference: a process theory.Neural Comput. 2017; 29: 1-49Crossref PubMed Scopus (456) Google Scholar]. Agents expect their future sensory states to match those they value or desire, and are surprised when such expectations are violated. In active inference terms, an agent can be said to act with self-confidence when they trust their actions will lead to the outcomes they expect, and thereby minimise surprise [5Friston K.F. et al.The anatomy of choice: dopamine and decision-making.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014; 36920130481Crossref PubMed Scopus (152) Google Scholar]. Self-confidence is reduced in OCD. The person's power to act in the world is severely diminished by their illness. OCD patients anticipate dangers such as contamination, and threats such as causing harm to others, or performing actions they find morally repugnant [6Abramowitz J.S. et al.Obsessive-compulsive disorder.Lancet. 2009; 374: 491-499Abstract Full Text Full Text PDF PubMed Scopus (347) Google Scholar]. The reduced self-confidence our patients report is the result of their actions being driven by their anticipation of threat and danger. We suggest that DBS increases self-confidence by allowing the patient to again be open to other possibilities for action and not only those that relate to their fear and anxiety. Neil Levy has recently suggested OCD may be due to an imbalance in the relative influence of top-down predictions and incoming sensory information [7Levy N. Obsessive-compulsive disorder as a disorder of attention.Mind Lang. 2018; 33: 3-16Crossref Scopus (16) Google Scholar]. In OCD, the agent anticipates threats such as contamination. Expectations of this type are assigned high precision. 'Precision' refers to the confidence or certainty an agent has in the predictions of an action policy (see [5Friston K.F. et al.The anatomy of choice: dopamine and decision-making.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014; 36920130481Crossref PubMed Scopus (152) Google Scholar] and Box 1). The person with OCD acts on action policies driven by their anxiety and fear. They pay no attention to conflicting sensory information, instead actively sampling the world in search of evidence confirming their anxiety-fuelled expectations. If the patients expect more dangers and they assign high precision to such expectations, they will as a result perceive more dangers even when there is no danger present in the environment.Box 1Active Inference in an Agent-Environment SystemActive inference is the process of selecting actions with sensory consequences that minimise long-term surprise [4Friston K.F. et al.Active inference: a process theory.Neural Comput. 2017; 29: 1-49Crossref PubMed Scopus (456) Google Scholar, 5Friston K.F. et al.The anatomy of choice: dopamine and decision-making.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014; 36920130481Crossref PubMed Scopus (152) Google Scholar]. 'Surprise' is quantified as prediction-error, the mismatch between top-down predictions of action policies and current sensory inputs. In earlier work we have argued for an interpretation of active inference in terms of the self-organising dynamics of a whole agent-environment system [11Bruineberg J. Rietveld E. Self-organisation, free-energy minimsation and optimal grip on a field of affordances.Front. Hum. Neurosci. 2014; 8: 599Crossref PubMed Scopus (317) Google Scholar]. Prediction errors map onto relevant affordances: the possibilities for action the environment offers to agents. Precision expectations, we have suggested, determine the degree of influence of multiple relevant affordances on an agent's behaviour by weighing the salience of prediction errors. Thus active inference, we have argued, does not just happen in the brain but in the skilled engagement of the agent with a field of relevant affordances (Figure I). Active inference is the process of selecting actions with sensory consequences that minimise long-term surprise [4Friston K.F. et al.Active inference: a process theory.Neural Comput. 2017; 29: 1-49Crossref PubMed Scopus (456) Google Scholar, 5Friston K.F. et al.The anatomy of choice: dopamine and decision-making.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014; 36920130481Crossref PubMed Scopus (152) Google Scholar]. 'Surprise' is quantified as prediction-error, the mismatch between top-down predictions of action policies and current sensory inputs. In earlier work we have argued for an interpretation of active inference in terms of the self-organising dynamics of a whole agent-environment system [11Bruineberg J. Rietveld E. Self-organisation, free-energy minimsation and optimal grip on a field of affordances.Front. Hum. Neurosci. 2014; 8: 599Crossref PubMed Scopus (317) Google Scholar]. Prediction errors map onto relevant affordances: the possibilities for action the environment offers to agents. Precision expectations, we have suggested, determine the degree of influence of multiple relevant affordances on an agent's behaviour by weighing the salience of prediction errors. Thus active inference, we have argued, does not just happen in the brain but in the skilled engagement of the agent with a field of relevant affordances (Figure I). In work on active inference, neurotransmitters such as dopamine are hypothesized to weigh the precision of action policies, ensuring agents act on policies which they have high confidence will minimise future surprise [5Friston K.F. et al.The anatomy of choice: dopamine and decision-making.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014; 36920130481Crossref PubMed Scopus (152) Google Scholar]. The ventral striatum is well known for playing a role in dopaminergic function [8Glimcher P.W. Understanding dopamine and reinforcement learning: the dopamine reward learning hypothesis.Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 15647-15654Crossref PubMed Scopus (505) Google Scholar]. Thus there is good reason to think the ventral striatum, in communication with a wide range of other areas, plays a role in weighing the precision of action policies [5Friston K.F. et al.The anatomy of choice: dopamine and decision-making.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014; 36920130481Crossref PubMed Scopus (152) Google Scholar]. We previously found that vALIC-DBS reduces excessive functional connectivity between the ventral striatum and medial prefrontal cortex, which critically predicted decreases in OCD symptoms [9Figee M. et al.Deep brain stimulation restores frontostriatal network activity in obsessive-compulsive disorder.Nat. Neurosci. 2013; 16: 386-387Crossref PubMed Scopus (297) Google Scholar]. Finding the optimal level of DBS in the ventral striatum normalises communication between these brain areas. Recent work in healthy individuals suggests that the ventral striatum and ventromedial prefrontal cortex track choice-dependent and choice-independent subjective confidence, respectively [10Bang D. Fleming S. Distinct encoding of decision confidence in human medial prefrontal cortex.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 6082-6087Crossref PubMed Scopus (92) Google Scholar]. This finding agrees with our hypothesis that the ventral striatum plays a key role in setting the precision on action policies. We hypothesise that people with OCD weigh the precision of their action policies, in part, based on their fearful and anxious mode of relating to the world. This has the consequence that their anxious anticipations are in the driving seat when it comes to selecting the action possibilities that drive their behaviour (Box 1). The effect of DBS is to restore the context-sensitive weighing of precision expectations. This allows the person to better anticipate what is relevant to them, and thus to once again be open to the many action possibilities of significance to them. It is the recovery of their readiness for and grip on the world that accounts for their increased self-confidence (see Figure I in Box 1). DBS may prove an effective treatment for OCD patients because it allows the patient to once again be open to the many possible actions the world offers, and thereby increases their self-confidence. The subsequent improvements in OCD symptoms may be contingent on their regaining the power to act in the world. To test our hypothesis, future studies are needed that examine the effect of vALIC-DBS on precision expectations using behavioural tasks. These should also examine the underlying neural changes, which likely include changes in communication between the ventral striatum and a wider network of connected regions, including the ventromedial prefrontal cortex. More research is also needed to establish whether the effects on self-confidence can only be achieved through DBS of the vALIC. Stimulating the subthalamic nucleus (STN) has been shown to reduce compulsivity, but is less anxiolytic than vALIC-DBS [12Mallet L. et al.Subthalamic nucleus stimulation in severe obsessive compulsive disorder.New Engl. J. Med. 2008; 359: 2121-2134Crossref PubMed Scopus (679) Google Scholar]. How does stimulation of STN, compared with vALIC, impact the patients' openness to action possibilities and self-confidence? Our prediction is that as long as anxiety-related anticipation is not reduced, the patient will remain at least partly closed off from the many possibilities they care about and their self-confidence will remain relatively low. DBS changes the structure of a patient's field of inviting affordances [2De Haan S. et al.Effects of deep brain stimulation on the lived experience of obsessive compulsive disorder patients: in-depth interviews with 18 patients.PLoS One. 2015; 10e0135524Crossref PubMed Scopus (69) Google Scholar]. This is, we suggest, why the patient experiences more self-confidence. As long as precision is high for anxious anticipations, this will result in the person focusing only on the dominant affordance(s) relating to their anxious state of anticipation. When anxiety reduces, the person is once again open to dealing with the many other action possibilities the environment makes available. The result of this openness and readiness for the world is increased self-confidence. We would like to thank Mark Miller, Judy Luigjes, and three anonymous referees for very helpful feedback on this article. J.K. and E.R. are supported by a European Research Council Starting Grant (679190) awarded to E.R. and by an Amsterdam Brain and Cognition Research Grant (awarded to D.D., E.R., and H.A.S.). H.A.S. is supported by an ERC Starting Grant (679399) awarded to H.A.S.