Trends in Neurosciences
Volume 31, Issue 11, November 2008, Pages 552-558
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Limbic and cortical information processing in the nucleus accumbens

https://doi.org/10.1016/j.tins.2008.08.002Get rights and content

The nucleus accumbens regulates goal-directed behaviors by integrating information from limbic structures and the prefrontal cortex. Here, we review recent studies in an attempt to provide an integrated view of the control of information processing in the nucleus accumbens in terms of the regulation of goal-directed behaviors and how disruption of these functions might underlie the pathological states in drug addiction and other psychiatric disorders. We propose a model that could account for the results of several studies investigating limbic-system interactions in the nucleus accumbens and their modulation by dopamine and provide testable hypotheses for how these might relate to the pathophysiology of major psychiatric disorders.

Introduction

The nucleus accumbens (NAcc) is a central component of the limbic system of the brain. This is based on its innervation by limbic structures, including excitatory afferents from the ventral hippocampus and the basolateral amygdala, and the medial prefrontal cortex (PFC) [1]. The NAcc integrates these limbic and cortical inputs and, in turn, projects to other basal ganglia nuclei including the ventral pallidum (VP) [1], which, in turn, sends feedback projections into the PFC via the mediodorsal nucleus of the thalamus [2]. This anatomical organization places the NAcc as a site for integration of emotional salience and contextual constraints processed in the amygdala and hippocampus, respectively, and executive/motor plans from the PFC, with the output positioned toward controlling goal-directed behavior [3]. Here, we discuss the mechanisms of limbic and cortical input integration in the NAcc and their modulation by dopamine (DA) in the regulation of goal-directed behavior, and how disruptions in these systems could underlie psychiatric disorders.

Section snippets

Involvement of the NAcc in diverse brain functions

The NAcc is thought to facilitate goal-directed behaviors by integrating information related to limbic drive and motor planning [3]. Nevertheless, the exact process by which the NAcc achieves this function is not yet clear, given that studies have revealed that the NAcc is involved in multiple distinct aspects of behavior. NAcc lesions cause disruptions of an array of cognitive and affective processes, including operant and emotional learning, response inhibition and behavioral flexibility 4, 5

DA-system modulation of the NAcc

The NAcc receives a substantial DA innervation that arises from the ventral tegmental area (VTA) [22]. This mesolimbic DA input is essential for NAcc function, and compromises within this system are believed to underlie several psychiatric disorders 3, 23, 24. The primary role of DA seems to be to modulate excitatory glutamatergic transmission [25], with a configuration of glutamatergic and DA terminals at close proximity on the top and neck of dendritic spines, respectively [26]. An intact DA

Implications for psychiatric disorders

Disruptions of the DA system in the NAcc have been implicated in several psychiatric disorders. The involvement of the DA system in drug abuse has been a topic of substantial investigation. In addition, disruptions of the NAcc have also been suggested to occur in other psychiatric disorders such as schizophrenia [3], obsessive compulsive disorders [23] and attention deficit hyperactivity disorder [24].

Concluding remarks

Electrophysiological, neurochemical and behavioral studies in the NAcc have uncovered some important aspects of NAcc information processing because it relates to goal-directed behaviors. These studies have provided important insights into the mechanisms of information processing and associated behavioral functions within the NAcc and the unique role of the DA system in maintaining a balance between limbic and cortical drive within this region. Adaptive modifications in this balance are

Acknowledgements

This work was supported by National Alliance for Research in Schizophrenia and Depression (www.narsad.org) Young Investigator Award (Y.G.) and United States Public Health Service (www.usphs.gov) MH57440 (A.A.G.). We thank Marco Leyton for comments on the manuscript.

References (59)

  • W. Schultz

    Getting formal with dopamine and reward

    Neuron

    (2002)
  • F.G. Gonon

    Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry

    Neuroscience

    (1988)
  • Z.H. Cheung

    Synaptic roles of Cdk5: implications in higher cognitive functions and neurodegenerative diseases

    Neuron

    (2006)
  • M. Laruelle

    Increased dopamine transmission in schizophrenia: relationship to illness phases

    Biol. Psychiatry

    (1999)
  • S. Jazbec

    Intra-dimensional/extra-dimensional set-shifting performance in schizophrenia: impact of distractors

    Schizophr. Res.

    (2007)
  • R. Corcoran et al.

    A role for the hippocampus in card sorting?

    Cortex

    (1993)
  • S. Corkin

    Beware of frontal lobe deficits in hippocampal clothing

    Trends Cogn. Sci.

    (2001)
  • R.E. Strecker et al.

    Electrical stimulation of the kindled hippocampus briefly increases extracellular dopamine in the nucleus accumbens

    Neurosci. Lett.

    (1994)
  • B.K. Lipska et al.

    To model a psychiatric disorder in animals: schizophrenia as a reality test

    Neuropsychopharmacology

    (2000)
  • N.R. Swerdlow

    Lesion size and amphetamine hyperlocomotion after neonatal ventral hippocampal lesions: more is less

    Brain Res. Bull.

    (2001)
  • H.J. Groenewegen

    Convergence and segregation of ventral striatal inputs and outputs

    Ann. N. Y. Acad. Sci.

    (1999)
  • P. O’Donnell

    Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transynaptic transport of pseudorabies virus

    J. Neurosci.

    (1997)
  • R.N. Cardinal

    Impulsive choice induced in rats by lesions of the nucleus accumbens core

    Science

    (2001)
  • C.S. Lansink

    Preferential reactivation of motivationally relevant information in the ventral striatum

    J. Neurosci.

    (2008)
  • A. Ishikawa

    Dorsomedial prefrontal cortex contribution to behavioral and nucleus accumbens neuronal responses to incentive cues

    J. Neurosci.

    (2008)
  • G. Buzsaki

    Large-scale recording of neuronal ensembles

    Nat. Neurosci.

    (2004)
  • P. O’Donnell et al.

    Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input

    J. Neurosci.

    (1995)
  • S.J. French et al.

    Hippocampal and prefrontal cortical inputs monosynaptically converge with individual projection neurons of the nucleus accumbens

    J. Comp. Neurol.

    (2002)
  • Y. Goto et al.

    Network synchrony in the nucleus accumbens in vivo

    J. Neurosci.

    (2001)
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