Dopaminergic regulation of limbic-striatal interplay.

Neurochemical, electrophysiological and behavioural evidence indicates that certain forms of goal-directed behaviours are mediated by complex and reciprocal interactions between limbic and dopamine (DA) inputs in the nucleus accumbens (NAc). Mesoaccumbens DA transmission appears to be compartmentalized; synaptic DA transmission is mediated by phasic burst firing of DA neurons, whereas extrasynaptic tonic DA levels are regulated by DA neuron population activity and limbic glutamatergic inputs to the NAc. DA release facilitated by limbic inputs and acting on D1 receptors can either potentiate or suppress neural activity driven by separate limbic inputs converging on the same postsynaptic NAc neurons. In turn, D1 receptors in the NAc mediate accuracy of search behaviour regulated by hippocampal-ventral striatal circuitries; D2 receptors appear to mediate motivational aspects of task performance. These findings suggest that dopaminergic modulation of limbic afferents to the NAc may be a cellular mechanism for input selection that governs the smooth coordination of behaviour by permitting information processed by one limbic region to temporarily exert control over the type and intensity of adaptive behavioural responses.

[1]  D. Schacter,et al.  The Evolution of Multiple Memory Systems , 1987 .

[2]  P. O’Donnell Ensemble coding in the nucleus accumbens , 1999, Psychobiology.

[3]  B. Everitt,et al.  Effects of medial dorsal thalamic and ventral pallidal lesions on the acquisition of a conditioned place preference: Further evidence for the involvement of the ventral striatopallidal system in reward-related processes , 1993, Neuroscience.

[4]  G. Mogenson,et al.  Disruption of food hoarding by injections of procaine into mediodorsal thalamus, GABA into subpallidal region and haloperidol into accumbens , 1988, Brain Research Bulletin.

[5]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[6]  A. Phillips,et al.  Glutamate Receptor-Dependent Modulation of Dopamine Efflux in the Nucleus Accumbens by Basolateral, But Not Central, Nucleus of the Amygdala in Rats , 2002, The Journal of Neuroscience.

[7]  S. Floresco,et al.  Stimulation of the Ventral Subiculum of the Hippocampus Evokes Glutamate Receptor‐mediated Changes in Dopamine Efflux in the Rat Nucleus Accumbens , 1997, The European journal of neuroscience.

[8]  M. Witter,et al.  Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin , 1987, Neuroscience.

[9]  A. Grace,et al.  Interconnected Parallel Circuits between Rat Nucleus Accumbens and Thalamus Revealed by Retrograde Transynaptic Transport of Pseudorabies Virus , 1997, The Journal of Neuroscience.

[10]  J. Seamans,et al.  Selective Roles for Hippocampal, Prefrontal Cortical, and Ventral Striatal Circuits in Radial-Arm Maze Tasks With or Without a Delay , 1997, The Journal of Neuroscience.

[11]  J. Seamans,et al.  Selective memory impairments produced by transient lidocaine-induced lesions of the nucleus accumbens in rats. , 1994, Behavioral neuroscience.

[12]  C. Pennartz,et al.  The nucleus accumbens as a complex of functionally distinct neuronal ensembles: An integration of behavioural, electrophysiological and anatomical data , 1994, Progress in Neurobiology.

[13]  N. Mizuno,et al.  Topographic organization of collateral projections from the basolateral amygdaloid nucleus to both the prefrontal cortex and nucleus accumbens in the rat , 1994, Neuroscience.

[14]  R. Steinberg,et al.  2-Chloro-N-[(S)-phenyl [(2S)-piperidin-2-yl] methyl]-3-trifluoromethyl benzamide, monohydrochloride, an inhibitor of the glycine transporter type 1, increases evoked-dopamine release in the rat nucleus accumbens in vivo via an enhanced glutamatergic neurotransmission , 2006, Neuroscience.

[15]  A comparison of the effects of electrical stimulation of the amygdala and hippocampus on subpallidal output neurons to the pedunculopontine nucleus , 1989, Brain Research.

[16]  G. Mogenson,et al.  Electrical and chemical activation of the mesencephalic and subthalamic locomotor regions in freely moving rats , 1988, Brain Research.

[17]  G. P. Smith,et al.  Efferent connections and nigral afferents of the nucleus accumbens septi in the rat , 1978, Neuroscience.

[18]  F. H. Lopes da Silva,et al.  Electrophysiology of the Hippocampal and Amygdaloid Projections to the Nucleus Accumbens of the Rat: Convergence, Segregation, and Interaction of Inputs , 1998, The Journal of Neuroscience.

[19]  Joseph E LeDoux Emotion: clues from the brain. , 1995, Annual review of psychology.

[20]  R. Chronister,et al.  Dopamine action in the nucleus accumbens. , 1985, Journal of neurophysiology.

[21]  G. Mogenson,et al.  Electrophysiological responses of neurones in the nucleus accumbens to hippocampal stimulation and the attenuation of the excitatory responses by the mesolimbic dopaminergic system , 1984, Brain Research.

[22]  G. Rebec,et al.  Dopaminergic modulation of glutamate-induced excitations of neurons in the neostriatum and nucleus accumbens of awake, unrestrained rats. , 1996, Journal of neurophysiology.

[23]  C. Cepeda,et al.  Dopamine and N-Methyl-D- Aspartate Receptor Interactions in the Neostriatum , 1998, Developmental Neuroscience.

[24]  X.-T. Hu,et al.  Comparison of effects of D-1 and D-2 dopamine receptor agonists on neurons in the rat caudate putamen: an electrophysiological study , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  V. Pickel,et al.  Ultrastructural immunocytochemical localization of the N-methyl-d-aspartate receptor and tyrosine hydroxylase in the shell of the rat nucleus accumbens , 1996, Brain Research.

[26]  Douglas L. Jones,et al.  From motivation to action: Functional interface between the limbic system and the motor system , 1980, Progress in Neurobiology.

[27]  D. S. Zahm,et al.  Evidence for the coexistence of glutamate decar☐ylase and Met-enkephalin immunoreactivities in axon terminals of rat ventral pallidum , 1985, Brain Research.

[28]  D. S. Zahm,et al.  The patterns of afferent innervation of the core and shell in the “Accumbens” part of the rat ventral striatum: Immunohistochemical detection of retrogradely transported fluoro‐gold , 1993, The Journal of comparative neurology.

[29]  L. Heimer,et al.  Ventral striatopallidal parts of the basal ganglia in the rat: I. Neurochemical compartmentation as reflected by the distributions of neurotensin and substance P immunoreactivity , 1988, The Journal of comparative neurology.

[30]  J. Wickens,et al.  Dopamine reverses the depression of rat corticostriatal synapses which normally follows high-frequency stimulation of cortex In vitro , 1996, Neuroscience.

[31]  T. Ono,et al.  Effects of reward anticipation, reward presentation, and spatial parameters on the firing of single neurons recorded in the subiculum and nucleus accumbens of freely moving rats , 2000, Behavioural Brain Research.

[32]  C. Y. Yim,et al.  Response of nucleus accumbens neurons to amygdala stimulation and its modification by dopamine , 1982, Brain Research.

[33]  F. Fonnum,et al.  The distribution and origin of glutamate decar☐ylase and choline acetyltransferase in ventral pallidum and other basal forebrain regions , 1979, Brain Research.

[34]  L. W. Swanson,et al.  Evidence for a projection from the lateral preoptic area and substantia innominata to the ‘mesencephalic locomotor region’ in the rat , 1984, Brain Research.

[35]  S. Floresco,et al.  Dopamine D1 and NMDA Receptors Mediate Potentiation of Basolateral Amygdala-Evoked Firing of Nucleus Accumbens Neurons , 2001, The Journal of Neuroscience.

[36]  S. Henriksen,et al.  Distribution of amygdala input to the nucleus accumbens septi: An electrophysiological investigation , 2005, Journal of Neural Transmission / General Section JNT.

[37]  A. Grace,et al.  Modulation of Cell Firing in the Nucleus Accumbens , 1999, Annals of the New York Academy of Sciences.

[38]  T. Robbins,et al.  The basolateral amygdala-ventral striatal system and conditioned place preference: Further evidence of limbic-striatal interactions underlying reward-related processes , 1991, Neuroscience.

[39]  F. J. White,et al.  Dopamine D(2) receptor modulation of K(+) channel activity regulates excitability of nucleus accumbens neurons at different membrane potentials. , 2006, Journal of neurophysiology.

[40]  A. Grace,et al.  Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  A. Grace,et al.  Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior , 2005, Nature Neuroscience.

[42]  G. Mogenson,et al.  Nucleus accumbens to globus pallidus GABA projection: Electrophysiological and iontophoretic investigations , 1980, Brain Research.

[43]  J. Salamone,et al.  Behavioral functions of nucleus accumbens dopamine: Empirical and conceptual problems with the anhedonia hypothesis , 1997, Neuroscience & Biobehavioral Reviews.

[44]  G. Mogenson,et al.  Hippocampal signal transmission to the pedunculopontine nucleus and its regulation by dopamine D2 receptors in the nucleus accumbens: An electrophysiological and behavioural study , 1987, Neuroscience.

[45]  S. Sesack,et al.  In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other , 1990, Brain Research.

[46]  K. Chergui,et al.  Modulation by dopamine D1-like receptors of synaptic transmission and NMDA receptors in rat nucleus accumbens is attenuated by the protein kinase C inhibitor Ro 32-0432 , 1999, Neuropharmacology.

[47]  S. Ikemoto,et al.  The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking , 1999, Brain Research Reviews.

[48]  S. Floresco,et al.  Involvement of the Ventral Pallidum in Working Memory Tasks With or Without a Delay , 1999, Annals of the New York Academy of Sciences.

[49]  T. Robbins,et al.  Effects of lesions to amygdala, ventral subiculum, medial prefrontal cortex, and nucleus accumbens on the reaction to novelty: implication for limbic-striatal interactions. , 1996, Behavioral neuroscience.

[50]  G. Mogenson,et al.  Dopamine enhances terminal excitability of hippocampal-accumbens neurons via D2 receptor: role of dopamine in presynaptic inhibition , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  R. Malenka,et al.  Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. , 2000, Annual review of neuroscience.

[52]  F. H. Lopes da Silva,et al.  Presynaptic dopamine D1 receptors attenuate excitatory and inhibitory limbic inputs to the shell region of the rat nucleus accumbens studied in vitro. , 1992, Journal of neurophysiology.

[53]  T. Robbins,et al.  Differential Roles of Dopamine D1 and D2 Receptors in the Nucleus Accumbens in Attentional Performance on the Five-Choice Serial Reaction Time Task , 2007, Neuropsychopharmacology.

[54]  A. Grace,et al.  Glutamatergic Afferents from the Hippocampus to the Nucleus Accumbens Regulate Activity of Ventral Tegmental Area Dopamine Neurons , 2001, The Journal of Neuroscience.

[55]  R. Oades The role of noradrenaline in tuning and dopamine in switching between signals in the CNS , 1985, Neuroscience & Biobehavioral Reviews.

[56]  Trevor W. Robbins,et al.  Time-limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[57]  S. Floresco,et al.  Dopamine and hippocampal input to the nucleus accumbens play an essential role in the search for food in an unpredictable environment , 1999, Psychobiology.

[58]  A. Cools,et al.  Evidence that dopamine in the nucleus accumbens is involved in the ability of rats to switch to cue-directed behaviours , 1991, Behavioural Brain Research.

[59]  H. Higashi,et al.  Hyperpolarizing and depolarizing actions of dopamine via D-1 and D-2 receptors on nucleus accumbens neurons , 1986, Brain Research.

[60]  S. Smith‐Roe,et al.  Coincident Activation of NMDA and Dopamine D1Receptors within the Nucleus Accumbens Core Is Required for Appetitive Instrumental Learning , 2000, The Journal of Neuroscience.

[61]  A. D. Smith,et al.  Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. , 1989, Journal of chemical neuroanatomy.

[62]  J. Salamone,et al.  D1 or D2 antagonism in nucleus accumbens core or dorsomedial shell suppresses lever pressing for food but leads to compensatory increases in chow consumption , 2001, Pharmacology Biochemistry and Behavior.

[63]  L. Sorkin,et al.  Systemic gabapentin and S(+)-3-isobutyl-γ-aminobutyric acid block secondary hyperalgesia , 1998, Brain Research.

[64]  S. Totterdell,et al.  Individual nucleus accumbens-projection neurons receive both basolateral amygdala and ventral subicular afferents in rats , 2003, Neuroscience.

[65]  S. Floresco,et al.  Modulation of Hippocampal and Amygdalar-Evoked Activity of Nucleus Accumbens Neurons by Dopamine: Cellular Mechanisms of Input Selection , 2001, The Journal of Neuroscience.

[66]  Cyriel M. A. Pennartz,et al.  Hippocampal and amygdaloid interactions in the nucleus accumbens , 1999, Psychobiology.

[67]  A. Phillips,et al.  Electrical stimulation of the hippocampus disrupts prepulse inhibition in rats: frequency- and site-dependent effects , 2004, Behavioural Brain Research.

[68]  A. Grace,et al.  Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission , 2003, Nature Neuroscience.

[69]  Robert J. McDonald,et al.  Acquisition of a spatial conditioned place preference is impaired by amygdala lesions and improved by fornix lesions , 1993, Behavioural Brain Research.

[70]  S. Floresco,et al.  Association Basolateral amygdala stimulation evokes glutamate receptor‐dependent dopamine efflux in the nucleus accumbens of the anaesthetized rat , 1998, The European journal of neuroscience.

[71]  D. S. Zahm,et al.  Two transpallidal pathways originating in the rat nucleus accumbens , 1990, The Journal of comparative neurology.

[72]  S. Mizumori,et al.  Characteristics of basolateral amygdala neuronal firing on a spatial memory task involving differential reward. , 1998, Behavioral neuroscience.

[73]  E. D. Leonibus,et al.  Co-activation of glutamate and dopamine receptors within the nucleus accumbens is required for spatial memory consolidation in mice , 2005, Psychopharmacology.

[74]  Hisao Nishijo,et al.  Amygdala role in conditioned associative learning , 1995, Progress in Neurobiology.

[75]  F. Gonon,et al.  Excitatory effects of dopamine released by impulse flow in the rat nucleus accumbens in vivo , 1996, Neuroscience.

[76]  S. Totterdell,et al.  Input from the amygdala to the rat nucleus accumbens: Its relationship with tyrosine hydroxylase immunoreactivity and identified neurons , 1994, Neuroscience.

[77]  P. Winn,et al.  Examination of the role of the pedunculopontine tegmental nucleus in radial maze tasks with or without a delay , 2002, Neuroscience.

[78]  S. Nicola The nucleus accumbens as part of a basal ganglia action selection circuit , 2007, Psychopharmacology.

[79]  A. Dickinson,et al.  Neuronal coding of prediction errors. , 2000, Annual review of neuroscience.

[80]  P. Redgrave,et al.  Is the short-latency dopamine response too short to signal reward error? , 1999, Trends in Neurosciences.

[81]  J. Harvey,et al.  A Postsynaptic Interaction between Dopamine D1 and NMDA Receptors Promotes Presynaptic Inhibition in the Rat Nucleus Accumbens via Adenosine Release , 1997, The Journal of Neuroscience.

[82]  L. Heimer,et al.  Cholecystokinin innervation of the ventral striatum: A morphological and radioimmunological study , 1985, Neuroscience.

[83]  S. Floresco,et al.  Dissociable Roles for the Nucleus Accumbens Core and Shell in Regulating Set Shifting , 2006, The Journal of Neuroscience.

[84]  R. Wise,et al.  Chemical Stimulation of the Ventral Hippocampus Elevates Nucleus Accumbens Dopamine by Activating Dopaminergic Neurons of the Ventral Tegmental Area , 2000, The Journal of Neuroscience.

[85]  D. Surmeier,et al.  D1 and D2 dopamine receptor modulation of sodium and potassium currents in rat neostriatal neurons. , 1993, Progress in brain research.

[86]  S. Floresco,et al.  Cerebral Cortex doi:10.1093/cercor/bhl073 Thalamic--Prefrontal Cortical--Ventral Striatal Circuitry Mediates Dissociable Components of Strategy Set Shifting , 2006 .

[87]  S. Floresco,et al.  Hyperlocomotion and increased dopamine efflux in the rat nucleus accumbens evoked by electrical stimulation of the ventral subiculum: role of ionotropic glutamate and dopamine D1 receptors , 2000, Psychopharmacology.

[88]  J. O. Schenk,et al.  D2 Receptors May Modulate the Function of the Striatal Transporter for Dopamine: Kinetic Evidence from Studies In Vitro and In Vivo , 1993, Journal of neurochemistry.

[89]  R. Wise,et al.  Injections of N‐methyl‐D‐aspartate into the ventral hippocampus increase extracellular dopamine in the ventral tegmental area and nucleus accumbens , 1999, Synapse.

[90]  A. Grace,et al.  Dopaminergic Reduction of Excitability in Nucleus Accumbens Neurons Recorded in Vitro , 1996, Neuropsychopharmacology.

[91]  J. Bargas,et al.  D1 Receptor Activation Enhances Evoked Discharge in Neostriatal Medium Spiny Neurons by Modulating an L-Type Ca2+ Conductance , 1997, The Journal of Neuroscience.