The role of the orbitofrontal cortex in normally developing compulsive-like behaviors and obsessive–compulsive disorder

doi:10.1016/S0278-2626(03)00274-4

Brain and Cognition

Volume 55, Issue 1, June 2004, Pages 220-234

https://doi.org/10.1016/S0278-2626(03)00274-4 Get rights and content

Abstract

Mounting evidence concerning obsessive–compulsive disorders points to abnormal functioning of the orbitofrontal cortices. First, patients with obsessive–compulsive disorder (OCD) perform poorly on tasks that rely on response suppression/motor inhibition functions mediated by the orbitofrontal cortex relative to both normal and clinical controls. Second, patients with OCD exhibit functional hyperactivity in lateral orbitofrontal and related structures corresponding with symptom severity. In this article, we compare these neurocognitive correlates of OCD with the executive and neural underpinnings of “compulsive-like” behaviors that are common in normal childhood. We discuss the phenomenology and natural history of normative compulsive-like behaviors as well as the behavioral, emotional, and cognitive continuities between typical and pathological obsessive–compulsive behaviors. We then examine associations between children’s executive performance deficits and their observed compulsive-like characteristics. We relate these patterns to executive deficits shown by adults with OCD. Finally, we speculate on the developmental neurobiology of children’s compulsive-like behaviors, with particular attention to orbitofrontal functions including behavioral and emotional regulation, and we suggest similarities and differences with the neurobiology of OCD. In making these comparisons, we hope to open a dialogue between researchers who study underlying brain pathologies associated with OCD and those who explore the neurocognitive bases of normal development.

Introduction

In this article, we discuss recent research and theory on the development of rituals, habits, and compulsive behaviors, and the possible role of the orbitofrontal cortices in the development and maintenance of these behavioral patterns. Our discussion begins with a review of the neurocognitive deficits associated with obsessive–compulsive disorder—inferred from tasks of executive function as well as neuroimaging studies. After relating these deficits to covariance between children’s compulsive and executive activities, we consider how interactions between the executive and emotional functions of the orbitofrontal cortex play a role in both pathological and normative compulsive behavior patterns.

Section snippets

Obsessive–compulsive disorder

Obsessive–Compulsive Disorder (OCD) is an anxiety disorder characterized by intrusive, troubling thoughts that are perceived as the products of one’s own mind (i.e., not thought insertion as in hallucinations associated with schizophrenia) or repetitive, compulsive behaviors (APA, 1997). The obsessions or compulsions are time-consuming, and lead to impairment in functioning. The thoughts and behaviors associated with OCD are viewed as senseless, and egodystonic—that is, they are counter to the

The neuropsychology of OCD¹

The behaviors associated with (adult-onset) OCD have been linked to a wide variety of cognitive deficits (Tallis, 1997). These findings are relatively inconsistent, largely born of differences in methodological approaches, such as inclusion–exclusion criteria for subjects, medication status, matching approaches, co-morbidities, as well as assessment measures (Schultz et al., 1999). Nonetheless, some patterns do emerge, suggesting that OC behaviors are associated with neuropsychological deficits.

The neurobiology of OCD

As noted earlier, several regions of the prefrontal cortices presumably subserve the executive functions. Specifically, the dorsolateral prefrontal cortex (DLPFC) is associated with cognitive set-shifting, planning, and working memory (Schultz et al., 1999). Though some questions remain as to the specificity of the DLPFC in set-shifting ability, a recent meta-analytic study suggests that WCST perseverative errors are more common in patients with damage to the dorsolateral prefrontal cortices as

Normative childhood rituals and “compulsive-like” behaviors

Rituals, perseverative, and compulsive behaviors, and other repetitive behavior patterns (as well as circumscribed interest patterns) have been studied, almost exclusively, in the context of brain injury and psychopathology. But increasingly, researchers are gaining an appreciation for the remarkable similarities between the broad range of repetitive behaviors that define severe psychopathology and those behaviors that are ubiquitous among typically developing young children. Thus, in the

The phenomenology and natural history of compulsive-like behaviors

As is the case with the symptom expression of OCD, the features of children’s compulsive-like behaviors are varied and multifaceted. By around age two children begin to engage in repetitive behaviors and to establish routines, particularly surrounding mealtime and bedtime. With regard to the bedtime ritual, children may require that parents engage in the same behaviors each night, such as reading a certain book, or watching the same video over and over. Children may involve a treasured object,

Developing executive functions and their hypothesized neural substrates

As noted earlier, executive functions refer to a broad range of cognitive and behavior control capabilities, that appear to undergo a period of development from infancy through the preschool years and beyond. Most relevant to our discussion are those EFs that underpin response inhibition, set-shifting, and selecting among competing behavioral tendencies. These are the capabilities that allow children to control their impulses, behave flexibly, with attention to contextual cues, and formulate

Associations between neuropsychological performance and normal compulsive-like behaviors

Our recent work has demonstrated that, in school-aged children, tasks of set-shifting and response inhibition/motor suppression are related to the frequency and intensity of typically developing children’s compulsive-like behaviors. Children six to eleven years of age were administered a series of computer-generated tasks assessing set-shifting and response inhibition (Evans and Iobst, 2003a, Evans and Iobst, 2003b).

Motor suppression/response inhibition tasks were as follows:

1.
Color

A hypothesized developmental neurobiology of normative compulsive-like behaviors

So far we have reported that children’s compulsive-like behaviors appear by about the age of two years, then increase in prevalence and remain highly characteristic of normal development until about the age of five, when they start to diminish in prominence. These behaviors include the repetition of invariant sequences, often based on attention to small changes in the environment, as well as a tendency toward excessive precision or symmetry, and they are related to anxiety both at the trait and

Acknowledgements

The first author would like to thank Dr. Robert Schultz of Yale University for his comments and to acknowledge that portions of the section on neurobiology appeared in Schultz, Evans, and Wolf (1999) (see Footnote 1). The first author also thanks Dr. Elizabeth Capaldi of Bucknell University for her insightful comments and support, and Ashley Pietrafesa for her assistance.

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The role of the orbitofrontal cortex in normally developing compulsive-like behaviors and obsessive–compulsive disorder

Abstract

Introduction

Section snippets

Obsessive–compulsive disorder

The neuropsychology of OCD1

The neurobiology of OCD

Normative childhood rituals and “compulsive-like” behaviors

The phenomenology and natural history of compulsive-like behaviors

Developing executive functions and their hypothesized neural substrates

Associations between neuropsychological performance and normal compulsive-like behaviors

A hypothesized developmental neurobiology of normative compulsive-like behaviors

Acknowledgements

Psychiatry Research

Brain and Cognition

Clinical Neurophysiology

Brain and Language

Psychiatry Research

Acta Psychologica

Developmental Brain Research

Trends in Cognitive Sciences

Biological Psychiatry

Biological Psychiatry

Journal of the American Academy of Child and Adolescent Psychiatry

Journal of the American Academy of Child and Adolescent Psychiatry

Archives of Clinical Neuropsychology

Neuropsychopharmacology

Biological Psychiatry

Child and Psychiatric Clinics of North America

Journal of the American Academy of Child and Adolescent Psychiatry

Anatomic basis of cognitive–emotional interactions in the primate prefrontal cortex

Neuroscience and Biobehavioral Reviews

Brain imaging as a tool in establishing a theory of brain pathology in obsessive compulsive disorder

Journal of Clinical Psychiatry

Local cerebral glucose metabolic rates in obsessive–compulsive disorder: A comparison with rates in unipolar depression and in normal controls

Archives of General Psychiatry

Caudate glucose metabolic rate changes with both drug and behavior therapy for obsessive–compulsive disorder

Archives of General Psychiatry

Emotion, decision making and the orbitofrontal cortex

Cerebral Cortex

Computerized tomography and neuropsychological test measures in children with obsessive–compulsive disorder

American Journal of Psychiatry

Developmental issues in obsessive–compulsive disorder

Journal of Child Psychology and Psychiatry and Allied Disciplines

Conflict monitoring versus selection-for-action in anterior cingulate cortex

Nature

Functional magnetic resonance imaging of symptom provocation in obsessive–compulsive disorder

Archives of General Psychiatry

Anterior cingulate cortex, error monitoring and the online maintenance of performance

Science

Parsing executive processes: Strategic vs. evaluative functions of the anterior cingulate cortex

Proceedings of the National Academy of Sciences

Sensitivity of prefrontal cortex to changed in target probability: A functional MRI study

Human Brain Mapping

A developmental functional MRI study of prefrontal activation during performance of a Go-No-Go task

Journal of Cognitive Neuroscience

The right brain hemisphere is dominant in human infants

Brain

Neuropsychological abnormalities in obsessive–compulsive disorder and their assessments

International Review of Psychiatry

A meta-analytic review of the sensitivity of the Wisconsin Card Sorting Test to frontal and lateralized frontal brain damage

Neuropsychology

Regulatory processes and the development of cognitive representations

Development and Psychopathology

Neurobiology of the structure of personality: Dopamine, facilitation of incentive motivation, and extraversion

Behavioral and Brain Sciences

Comparison of human infants and rhesus monkeys on Piaget’s A-not-B task: Evidence for dependence on dorsolateral prefrontal cortex

Experimental Brain Research

Prefrontal cortex cognitive deficits in children treated early and continuously for PKU

Monographs of the Society for Research in Child Development

The beginnings of social understanding

The development of ritualization

Rituals and other syncretic tools: Insights from Werner’s comparative psychology

Journal of Adult Development

Compulsive-like behavior in individuals with Down syndrome: Its relation to MA level, adaptive and maladaptive behavior

Child Development

Rituals, fears and phobias in young children: Insights from development, psychopathology and neurobiology

Child Psychiatry and Human Development

Tic disorders

Ritual, habit, and perfectionism: The prevalence and development of compulsive-like behavior in normal young children

The neuropsychology of OCD¹