Elsevier

Progress in Neurobiology

Volume 108, September 2013, Pages 44-79
Progress in Neurobiology

Inhibition and impulsivity: Behavioral and neural basis of response control

https://doi.org/10.1016/j.pneurobio.2013.06.005Get rights and content

Highlights

  • Inhibition is a fundamental aspect of every organized cognitive or behavioral response.

  • Deficient inhibitory processes (impulsivity) profoundly affect everyday life.

  • Impulsivity is considered the core feature of several psychiatric disorders.

  • Prefrontal cortex and subcortical structures cooperate for the inhibition of unwanted responses.

Abstract

In many circumstances alternative courses of action and thoughts have to be inhibited to allow the emergence of goal-directed behavior. However, this has not been the accepted view in the past and only recently has inhibition earned its own place in the neurosciences as a fundamental cognitive function. In this review we first introduce the concept of inhibition from early psychological speculations based on philosophical theories of the human mind. The broad construct of inhibition is then reduced to its most readily observable component which necessarily is its behavioral manifestation. The study of ‘response inhibition’ has the advantage of dealing with a relatively simple and straightforward process, the overriding of a planned or already initiated action. Deficient inhibitory processes profoundly affect everyday life, causing impulsive conduct which is generally detrimental for the individual. Impulsivity has been consistently linked to several types of addiction, attention deficit/hyperactivity disorder, mania and other psychiatric conditions. Our discussion of the behavioral assessment of impulsivity will focus on objective laboratory tasks of response inhibition that have been implemented in parallel for humans and other species with relatively few qualitative differences. The translational potential of these measures has greatly improved our knowledge of the neurobiological basis of behavioral inhibition and impulsivity. We will then review the current models of behavioral inhibition along with their expression via underlying brain regions, including those involved in the activation of the brain's emergency ‘brake’ operation, those engaged in more controlled and sustained inhibitory processes and other ancillary executive functions.

Section snippets

Historical introduction

In the words of the father of American psychology William James (1842–1910) inhibition [Lat. inhibere, to restrain] is “… not an occasional accident; it is an essential and unremitting element of our cerebral life” (James, 1890; Vol. II, p. 583). Scientists and philosophers have long been interested in the nature of inhibitory processes at the psychological, neurophysiological and cognitive level. Plato's allegory of the human soul viewed as a charioteer driving a chariot pulled by two horses

Failure of the inhibitory processes: impulsivity

“If the centres of inhibition, and thereby the faculty of attention, are weak, or present impulses unusually strong, volition is impulsive rather than deliberate”. (Ferrier, 1876, p. 287).

Impulsivity [or impulsiveness] is generally regarded as a consequence of impaired executive functioning. More specifically, an impulsive action is determined by the co-occurrence of dysfunctional inhibitory processes and strong ‘impulsions’ (or impulses), plus being triggered and modulated by dispositional and

Neural substrates of response inhibition

“The centres of inhibition being thus the essential factor of attention, constitute the organic basis of all the higher intellectual faculties. And in proportion to their development we should expect a corresponding intellectual power”. (Ferrier, 1876, p. 287)

The investigation of the neural substrates of response inhibition has been pursued using a variety of techniques and approaches. Animal models offer the possibility of testing the effects of drugs and discrete brain lesions on impulsive

Comparison with choice impulsivity and reversal learning

“Whenever choice appears in any form – as rivalry between appetites which cannot be simultaneously satisfied, as a perceived meaning attached to an ambiguous stimulus, as a planned decision between two courses of action, as a symbolic fulfillment of an unsuspected wish – it always involves an element of inhibition”. (Diamond et al., 1963; p. 145)

As previously discussed, two other families of behavioral tasks have been used to measure behavioral inhibition in clinical and preclinical settings:

Summary, conclusions and future perspectives

“I have nothing to say on the nature of the inhibitory process. I would urge, however, that here, as in all other cases, we should distinguish between the psychical and the physical; we cannot legitimately speak of any mental states as inhibitory of any physical processes, any more than we can speak of them as producing movements. I have long urged that controlling as well as directive action is displayed throughout the nervous system.” (Jackson, 1931b, p. 481)

The aim of the first part of the

Acknowledgments

The authors would like to thankfully acknowledge the work of two anonymous reviewers for their valuable comments. AB was supported by an MRC U.K. Studentship. The review was completed within the Behavioural and Clinical Neuroscience Institute, supported by a joint award from the MRC and Wellcome Trust. Dedicated to the memory of our friend and colleague Daina Economidou.

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