Cognitive inflexibility in Obsessive-Compulsive Disorder

doi:10.1016/j.neuroscience.2016.07.030

Neuroscience

Volume 345, 14 March 2017, Pages 243-255

https://doi.org/10.1016/j.neuroscience.2016.07.030 Get rights and content

Highlights

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Deficits in cognitive flexibility have been described in Obsessive-Compulsive Disorder (OCD).
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These deficits may contribute to symptomatology.
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Classical neuropsychological probes test multiple constructs simultaneously.
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More specific behavioral tests, supplemented by neuroimaging, are needed.

Abstract

Obsessive-Compulsive Disorder (OCD) is characterized by maladaptive patterns of repetitive, inflexible cognition and behavior that suggest a lack of cognitive flexibility. Consistent with this clinical observation, many neurocognitive studies suggest behavioral and neurobiological abnormalities in cognitive flexibility in individuals with OCD. Meta-analytic reviews support a pattern of cognitive inflexibility, with effect sizes generally in the medium range. Heterogeneity in assessments and the way underlying constructs have been operationalized point to the need for better standardization across studies, as well as more refined overarching models of cognitive flexibility and executive function (EF). Neuropsychological assessments of cognitive flexibility include measures of attentional set shifting, reversal and alternation, cued task-switching paradigms, cognitive control measures such as the Trail-Making and Stroop tasks, and several measures of motor inhibition. Differences in the cognitive constructs and neural substrates associated with these measures suggest that performance within these different domains should be examined separately. Additional factors, such as the number of consistent trials prior to a shift and whether a shift is explicitly signaled or must be inferred from a change in reward contingencies, may influence performance, and thus mask or accentuate deficits. Several studies have described abnormalities in neural activation in the absence of differences in behavioral performance, suggesting that our behavioral probes may not be adequately sensitive, but also offering important insights into potential compensatory processes. The fact that deficits of moderate effect size are seen across a broad range of classic neuropsychological tests in OCD presents a conceptual challenge, as clinical symptomatology suggests greater specificity. Traditional cognitive probes may not be sufficient to delineate specific domains of deficit in this and other neuropsychiatric disorders; a new generation of behavioral tasks that test more specific underlying constructs, supplemented by neuroimaging to provide insight into the underlying processes, may be needed.

Section snippets

Cognitive inflexibility in OCD: face validity and conceptual challenges

Obsessive-Compulsive Disorder (OCD) is characterized by maladaptive patterns of repetitive, inflexible cognition and behavior. Clinically, individuals with OCD have difficulty shifting between mental processes to generate adaptive behavioral responses, especially in the context of their symptoms. In keeping with this, many neurocognitive studies suggest abnormalities in cognitive flexibility in individuals with OCD (e.g. Remijnse et al., 2006, Chamberlain et al., 2007, Chamberlain et al., 2008,

Cognitive inflexibility in OCD: attentional set shifting

Attentional set shifting is the “ability to switch attention from one aspect of a stimulus to another in an ongoing task, in accordance with changing reinforcement contingencies” (Chamberlain et al., 2005). Efficient set shifting is a core aspect of cognitive flexibility (Dajani and Uddin, 2015). There are several different types of set shifting, which appear to be associated with distinct neural substrates. These are generally defined within the context of simple discrimination tasks in which

Cognitive inflexibility in OCD: reversal learning

Reversal learning also requires shifting from one stimulus to another based on feedback. In this case, however, shifts relate to entire composite stimuli, rather than to individual stimulus attributes. Reversal learning occurs when a stimulus that was previously neutral becomes salient, or when a stimulus that was previously rewarded becomes neutral. Reversal-specific learning is associated with activation of the lateral orbitofrontal cortex (OFC) (Ghahremani et al., 2010). Neurobiological

Cognitive inflexibility in OCD: alternation tasks

In Object Alternation (OAT) and Delayed Alternation (DAT) tasks, shifts are performed on every trial. In the OAT, optimal performance requires selecting a different stimulus on every trial – that is, avoiding repeatedly selecting the same stimulus. The DAT is similar except that optimal performance requires alternation between targets at different points in space.

Patients with OCD have been found to have deficits in the OAT and DAT, with some consistency, though effect sizes have varied across

Cognitive inflexibility in OCD: cued task switching

Task switching is another core aspect of cognitive flexibility (Dajani and Uddin, 2015). It describes situations in which subjects must change strategy based on an explicit instruction or cue, rather than inferring changed contingencies from the pattern of reward receipt. Task-switching paradigms (Braver et al., 2003, Gu et al., 2008, Remijnse et al., 2013) typically include both task-repeat and task-switch trials; the number of consistent trials presented before a signaled task switch can be

Cognitive inflexibility in OCD: inhibition of cognitive and motor prepotent responses

Another category of measures often examined when assessing cognitive flexibility, typified by the Stroop Color Word Test (CWT), more specifically tests the inhibition of prepotent responses. Whether or not inhibition is a core component of cognitive flexibility is the subject of some disagreement in the literature; but a failure to inhibit prepotent responses can clearly lead to inflexible behavior. Importantly, responses can become prepotent in a variety of ways; extended repetition during

Cognitive flexibility in OCD: updating

Updating is the constant monitoring and rapid addition/deletion of working memory contents (Miyake et al., 2000, Miyake and Friedman, 2012). The ability to successfully update working memory is thought to be a key component of cognitive flexibility (Dajani and Uddin, 2015). The ability to acquire new information and manipulate it in real time is critical to adjusting one’s behavior to meet the demands of a changing environment. Updating can be measured through tests such as the n-back. In this

Habit, action, and model-based versus model-free learning

Dual-system theories posit that actions and choices may be supported by either a goal-oriented or a habitual system (Balleine and Dickinson, 1998). Recent computational literature draws a similar distinction between model-based and model-free strategies for action selection (Daw et al., 2011). Goal-oriented, model based choice permits flexibility but requires substantial cognitive resources. Habitual or model-free behavior is more efficient in familiar situations, in which past experience

The paradox of broad executive function deficits in OCD

The specificity of the findings summarized above has been questioned. In particular, three meta-analyses of cognitive function in OCD describe deficits of moderate effect size across almost all domains of EF, including planning, verbal fluency, visuospatial function, and motor speed (Abramovitch et al., 2013, Shin et al., 2013, Snyder et al., 2015). (Verbal working memory may be relatively spared; Snyder et al., 2015). This raises the question of whether deficits in cognitive inflexibility are

Sources of impaired performance in tests of cognitive flexibility

Implicit in the above discussion is the realization that there are multiple possible sources of impaired performance in behavioral tasks that purport to measure cognitive flexibility. Careful consideration of these different sources of variation, and exclusion of them when possible, will facilitate more precise characterization of the nature of cognitive abnormalities in patients.

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First, there may be a true group difference in the cognitive ability that a behavioral task is seeking to probe.

Conclusions

OCD is characterized by maladaptive patterns of repetitive, inflexible cognition and behavior that suggest a lack of cognitive flexibility. In keeping with this, many neurocognitive studies of individuals with OCD suggest behavioral and/or neurobiological abnormalities in cognitive flexibility (Remijnse et al., 2006, Chamberlain et al., 2007, Chamberlain et al., 2008, Gu et al., 2008, Viswanath et al., 2009). Meta-analytic reviews of neuropsychological functioning in OCD, as well as clinical

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ReviewCognitive inflexibility in Obsessive-Compulsive Disorder

Highlights

Abstract

Section snippets

Cognitive inflexibility in OCD: face validity and conceptual challenges

Cognitive inflexibility in OCD: attentional set shifting

Cognitive inflexibility in OCD: reversal learning

Cognitive inflexibility in OCD: alternation tasks

Cognitive inflexibility in OCD: cued task switching

Cognitive inflexibility in OCD: inhibition of cognitive and motor prepotent responses

Cognitive flexibility in OCD: updating

Habit, action, and model-based versus model-free learning

The paradox of broad executive function deficits in OCD

Sources of impaired performance in tests of cognitive flexibility

Conclusions

Clin Psychol Rev

Psychiatry Res

Neuropharmacology

Neuron

Neurosci Biobehav Rev

Trends Neurosci

Neuron

Brain Cogn

Schizophr Res

Biol Psychiatry

J Obsessive Compulsive Relat Disord

Neuron

Cogn Psychol

Brain Cogn

Brain Cogn

Prog Neuropsychopharmacol Biol Psychiatry

Psychiatry Res

Comparative neuropsychology of adult obsessive-compulsive disorder and attention deficit/hyperactivity disorder: implications for a novel executive overload model of OCD

J Neuropsychol

Prefrontal cortical mechanisms underlying individual differences in cognitive flexibility and stability

J Cogn Neurosci

Meta-analysis of the symptom structure of obsessive-compulsive disorder

Am J Psychiatry

Impaired cognitive flexibility and motor inhibition in unaffected first-degree relatives of patients with obsessive-compulsive disorder

Am J Psychiatry

Orbitofrontal dysfunction in patients with obsessive-compulsive disorder and their unaffected relatives

Science

Prefrontal serotonin depletion affects reversal learning but not attentional set shifting

J Neurosci

Presupplementary motor area hyperactivity during response inhibition: a candidate endophenotype of obsessive-compulsive disorder

Am J Psychiatry

Review
Cognitive inflexibility in Obsessive-Compulsive Disorder