Elsevier

Progress in Neurobiology

Volume 92, Issue 4, December 2010, Pages 533-557
Progress in Neurobiology

Nucleus accumbens and impulsivity

https://doi.org/10.1016/j.pneurobio.2010.08.007Get rights and content

Abstract

The multifaceted concept of impulsivity implies that different impulsivity aspects, mediated by different neural processes, influence behavior at different levels. The nucleus accumbens (NAc) is a key component of the neural processes regulating impulsivity. In this review, we discuss the findings of lesion studies in animals and functional imaging studies in humans focusing on the role of the NAc in impulsivity. Evidence supports that the extent and pattern of involvement of the NAc, and its subregions, the core and the shell, vary among different facets of impulsivity. Data from imaging studies reviewed in this article suggest the involvement of the ventral striatum/NAc in impulsive choice. Findings of animal studies indicate that lesions of the NAc core subregion facilitated impulsivity in tasks involving intertemporal choice, and promoted a risk-averse, less impulsive, tendency in tasks involving options with probability differences. Modification of neurotransmitter activity, especially of dopamine, which is proposed to underlie the changes observed in functional imaging studies, has been shown to influence afferent input pattern in the NAc and the generation of the behavioral output. Parameters of behavioral tasks reflecting response inhibition function are altered by neurochemical interventions and local electrical stimulation in both the core and the shell subregions. In toto, NAc's pattern of neuronal activity, either genetically determined or acquired, has a critical impact on the interindividual variation in the expression of impulsivity. Nevertheless, the NAc is not the only substrate responsible for impulsivity and it is not involved in each facet of impulsivity to the same extent.

Research highlights

▶ The nucleus accumbens (NAc) is a key component of the neural processes regulating impulsivity. ▶ The extent and pattern of involvement of the NAc, and its subregions, the core and the shell, vary among different facets of impulsivity. ▶ There is strong evidence supporting the involvement of the NAc core in impulsive choice, but only limited evidence supports its involvement in response inhibition.

Introduction

Making choices and acting accordingly are basic daily life activities for both humans and animals. The quality of these activities is critical for adaptation and survival. Impulsive features directly influence the quality of the decisions and actions (Zermatten et al., 2005; Franken et al., 2008). Impulsivity has been defined as the inability to wait, a tendency to act without forethought, insensitivity to consequences, preference for immediate over delayed gratification, inability to inhibit inappropriate behavior, the tendency to engage in risky behavior, and the desire to seek out novel sensations (Mitchell, 2004, Reynolds et al., 2006). Impulsivity has been a difficult term to define; part of this complexity arises from the fact that different areas of science (psychiatry, psychology and neuroscience), as well as lay people, have used it with a wide range of connotations (Evenden, 1999d). Impulsive acts often have deleterious consequences, although we all act impulsively with varying degree and frequency. Besides being part of healthy behavior, impulsivity is one of the core symptoms of various disruptive behaviors and psychiatric disorders such as drug abuse, attention deficit and hyperactivity disorder (ADHD), bipolar disorder, obsessive compulsive disorder, aggression, suicide, pathological gambling, trichotillomania, intermittent explosive disorder, self-injurious behavior, and kleptomania (Kisa et al., 2005, Swann et al., 2001).

Research on impulsivity, using a wide range of methods both in humans and animals, has attempted to define the main neuronal elements involved in the development and expression of impulsivity. The current concept of impulsivity emphasizes its multifaceted nature (Evenden, 1999d). This means that there are different cognitive and behavioral features covered by the term (Congdon and Canli, 2005, Evenden, 1999a, Reynolds et al., 2006). This conceptualization makes it unlikely that a single common biological mechanism underlies all features of impulsivity. In the last years, a growing amount of evidence support a frontostriatal regulation of impulsive behavior (Bechara and Van Der Linden, 2005, Chambers and Potenza, 2003, Dalley et al., 2008), and within this frontostriatal circuit, the nucleus accumbens (NAc) has been shown to be a key structure (Dalley et al., 2007). For instance, lesions of the NAc in rats produce profound changes in specific facets of impulsivity (Bezzina et al., 2007, Cardinal et al., 2001, Eagle and Robbins, 2003b, Pothuizen et al., 2005).

The NAc has been extensively studied with anatomical, electrophysiological, pharmacological and behavioral methods because of its possible role in the pathophysiology of psychiatric disorders (Mogenson et al., 1980, Stevens, 1973). The NAc receives information both from limbic structures, which are critical for affective processing, as well as motor structures which coordinate motor performance. Therefore, the NAc is proposed to be critical in integrating motivational information to modulate behavior. In the last decades, more and more data has become available on the involvement of the NAc in reward, motivation, and affective disorders (Nestler and Carlezon, 2006, Robbins and Everitt, 1996). The NAc has been implicated in the neurobiology of decision making; not only in motivation and salience attribution, but also in action selection (Berridge and Robinson, 1998, Ernst and Paulus, 2005, Nicola, 2007).

A multitude of behavioral measures and models of different features of impulsivity have been proposed (Monterosso and Ainslie, 1999, Winstanley et al., 2006). The elucidation of underlying neurobiological mechanisms regulating each impulsive feature, and application of the multifaceted conceptualization of impulsivity to models of psychopathology may improve strategies of intervention and treatment in impulsivity related disruptive behaviors and disorders.

Section snippets

Nucleus accumbens

Before reviewing the evidence on the involvement of the NAc in impulsive behavior, we will review some anatomical facts. Following a brief description of the regional anatomy, we will deal with the intrinsic organization and connections of the NAc.

Impulsivity

The definition and the structural components of impulsivity, as well as the methods of evaluating impulsivity have been extensively investigated. The most influential models of personality include impulsivity as a significant component, and frequently multiple dimensions of impulsivity were taken into consideration (Eysenck and Eysenck, 1977, Eysenck, 1985, Gray, 1981, Gray, 1987, Cloninger et al., 1993, Zuckerman et al., 1984, Dickman, 1990, McCrae and Costa, 1990). The research on human

Nucleus accumbens and impulsivity

Lesions due to various reasons (e.g. tumour, ischemia) have contributed significantly to our understanding of the function of various brain regions. However, this is not the case for the NAc. In animal models, a substantial amount of data has become available by experimental lesions, electrical stimulation and application of pharmacological agents. In humans, the role of the NAc in impulsivity has predominantly been investigated by neuroimaging studies. In this section, we will review and

Discussion: nucleus accumbens and impulsivity

Impulsive acts and decisions are related to individual differences in the neural representations of stimuli/events (Chambers and Potenza, 2003). The NAc plays an important regulatory role in the neural representation of response options, as shown by functional neuroimaging studies in healthy individuals. Although some studies showed the involvement of the NAc in salience or valence representation, recent findings support the recruitment of the NAc in coding of both salience and valence (Cooper

Conclusion

The afferent and efferent connections of the NAc and the rich interplay of major neurotransmitter systems within it, makes the NAc a major determinant of behavioral output. The NAc functions as a key element of cortico-striatal circuits regulating cognitive and behavioral processes. NAc's pattern of neuronal activity, either genetically determined or acquired, has a critical impact on the interindividual variation in the expression of impulsivity. Dopamine facilitates the implementation of

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