Evidence for a mechanistic model of cognitive control

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Abstract

A core deficit observed in a number of disorders of childhood is an inability to inhibit or suppress inappropriate thoughts and behaviors (e.g. attention deficit/hyperactivity disorder, obsessive compulsive disorder and Tourette's syndrome). Two regions of the brain that have been implicated in these disorders are the frontal lobes and the basal ganglia. The common problem in inhibitory control and the common brain regions implicated across this range of developmental disorders suggest a single underlying biological mechanism. Yet, the symptomatology observed across these disorders is distinct. A number of parallel circuits that involve basal ganglia and frontal cortex have been described. Each of these basal ganglia thalamocortical circuits controls a different set of cortically mediated behaviors that range from skeletal and eye movements to cognitive and emotional actions. An important neuromodulator in the basal ganglia thalamocortical circuitry is dopamine, particularly at the level of the prefrontal cortex and striatum. These circuits are assumed to facilitate cortically mediated behaviors by inhibiting conflicting behaviors and dopamine is assumed to play a significant neuromodulatory role in these circuits. Accordingly, we have recently developed a model of inhibitory mechanisms whereby the basal ganglia are involved in inhibition of behaviors while the frontal cortex is involved in representing and maintaining the conditions in which we respond or act. Dopamine is suggested to play an important role in the ability to maintain these internal representations against interference. Converging evidence for this model is presented from developmental, clinical, neuroimaging and lesion studies.

Introduction

A critical component of cognitive processes is the ability to suppress or override competing attentional and behavioral responses [1], [2], [3]. How is it that we learn or gain the ability to override these responses? The importance of examining the neural basis of cognitive control is underscored by its disruption in a number of childhood disorders. For example, a core deficit observed in childhood disorders is an inability to inhibit or suppress inappropriate thoughts and behaviors as in attention deficit/hyperactivity disorder (ADHD), obsessive compulsive disorder and Tourette's syndrome. This paper addresses the development, biological basis and potential genetic factors that underlie this ability.

A major contribution in psychological theory has been the identification of controlled processing as a central component of human cognition [4], [5]. This construct has been refined and included in a number of theories of attention and memory [3], [6], [7], [8] and referred to in a number of ways (e.g. ‘central executive’, ‘attentional bias’). Each of these coined terms are suggestive of a mechanism that is required to direct or guide appropriate attentional responses or actions [9]. For example, Shallice [7] proposed a ‘supervisory attention system’ as a system for inhibiting or replacing routine, reflexive behaviors and thoughts with more appropriate behaviors and thoughts. Desimone and Duncan [8] describe top-down biasing signals as important in attending to relevant information by virtue of mutual inhibition or suppression of irrelevant information. A common theme that has emerged from this work is that a primary function of cognitive control is to reduce conflict in processing of information [1], [2], [3]. Thus, one critical component of cognitive control is the ability to suppress or override competing attentional and behavioral responses. This aspect of cognitive control is the focus of the current paper.

Section snippets

Development of cognitive control

Clearly, the ability to suppress irrelevant information and actions becomes more efficient with age. A number of classic developmental studies have demonstrated that these cognitive processes develop throughout childhood and adolescence [10], [11], [12], [13]. Several theorists have argued that the development of attention and memory related processes is due to increases in processing speed and efficiency and not due to an increase in mental capacity [14], [15], [16]. According to this view,

Brain circuitry implicated in cognitive control

The importance of examining the neural basis of cognitive control is underscored by its disruption in a number of childhood disorders. A core deficit observed in these disorders is an inability to inhibit or suppress inappropriate thoughts and behaviors (e.g. ADHD, obsessive compulsive disorder and Tourette's syndrome). For example, children with ADHD have problems focusing attention and are often characterized as distractible and impulsive [32], [33]. Children with Tourette's syndrome have

Dopamine and cognitive control

An important neuromodulator in the basal ganglia thalamocortical circuitry is dopamine, particularly at the level of the prefrontal cortex and striatum. Several lines of evidence suggest that dopamine plays an important role in the ability to maintain internal representations of contextual information against interference. First, it has been shown that activation of mesocortical dopaminergic neurons via apomorphine enhances activity in the prefrontal cortex, a brain region implicated in

Brain development and cognitive control

Information about the developing human brain is relatively sketchy despite the significant gains in the fields of pediatric neuroimaging and developmental neurobiology. This is particularly the case during early and late childhood - a time when significant leaps in cognitive control take place. In part, this is due to low mortality rates across this age range in addition to the rare occurrence of autopsies on this population [104]. Nonetheless, postmortem studies of both human and nonhuman

Behavioral studies

A theoretically driven approach to characterizing cognitive control is to probe inhibition of different types of information and at different stages of cognitive processing (stimulus selection, response selection, and response execution). Accordingly, we have developed a battery of tasks that require (1) inhibition of a stimulus set (e.g. distractors versus target); (2) inhibition of a behavioral set (e.g. remapping from one set of responses to a new set of responses); and (3) inhibition of a

Discussion and summary

This paper presents a mechanistic model of inhibitory control whereby the inhibitory mechanism is the same across circuits (i.e. at the level of the basal ganglia), but the type of information represented by each circuit (i.e. maintained in the frontal cortex) is different. Accordingly, the basal ganglia are involved in suppression of actions while the frontal cortex is involved in representing and maintaining information and conditions to which we respond or act. Dopamine plays a

Acknowledgements

This work was supported in part by a 5-K01 MH01297-03, the Charles A. Dana Foundation, the John D. and Catherine T. MacArthur Foundation, and a John Merck Scholarship in the Biology of Developmental Disabilities to B.J.C., the Netherlands Royal Academy of the Arts and Sciences and the Foundation De Drie Lichten to S.D.

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