The Reward Circuit: Linking Primate Anatomy and Human Imaging

Although cells in many brain regions respond to reward, the cortical-basal ganglia circuit is at the heart of the reward system. The key structures in this network are the anterior cingulate cortex, the orbital prefrontal cortex, the ventral striatum, the ventral pallidum, and the midbrain dopamine neurons. In addition, other structures, including the dorsal prefrontal cortex, amygdala, hippocampus, thalamus, and lateral habenular nucleus, and specific brainstem structures such as the pedunculopontine nucleus, and the raphe nucleus, are key components in regulating the reward circuit. Connectivity between these areas forms a complex neural network that mediates different aspects of reward processing. Advances in neuroimaging techniques allow better spatial and temporal resolution. These studies now demonstrate that human functional and structural imaging results map increasingly close to primate anatomy.

[1]  Jelliffe Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[2]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[3]  Cytoarchitecture of the Human Brain Stem , 1954, Neurology.

[4]  James L Olds,et al.  Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. , 1954, Journal of comparative and physiological psychology.

[5]  J. Olszewski,et al.  Cytoarchitecture of the Human Brain Stem , 1955 .

[6]  P. Yakovlev,et al.  Organization of the projections of the anterior group of nuclei and of midline nuclei of thalamus to the cingulate gyrus, hippocampal rudiment and septal area in monkey. , 1960, Transactions of the American Neurological Association.

[7]  R A PATTON,et al.  Limbic nuclei of thalamus and connections of limbic cortex. , 1960, Archives of neurology.

[8]  W. Nauta,et al.  Projections of the lentiform nucleus in the monkey. , 1966, Brain research.

[9]  J. Rafols,et al.  The primate globus pallidus: a Golgi and electron microscopic study. , 1974, Journal fur Hirnforschung.

[10]  W. Nauta,et al.  Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber‐of‐passage problem , 1977, The Journal of comparative neurology.

[11]  L. Heimer The Olfactory Cortex and the Ventral Striatum , 1978 .

[12]  A. Phillips,et al.  The role of dopamine in maintaining intracranial self-stimulation in the ventral tegmentum, nucleus accumbens, and medial prefrontal cortex. , 1978, Canadian journal of psychology.

[13]  W. Nauta,et al.  Crossroads of Limbic and Striatal Circuitry: Hypothalamo-Nigral Connections , 1978 .

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

[15]  J. Szabo Strionigral and Nigrostriatal Connections , 1979 .

[16]  J. Szabo Strionigral and nigrostriatal connections. Anatomical studies. , 1979, Applied neurophysiology.

[17]  W. Nauta,et al.  Efferent connections of the habenular nuclei in the rat , 1979, The Journal of comparative neurology.

[18]  K. Akert,et al.  Relationships of precentral premotor and prefrontal cortex to the mediodorsal and intralaminar nuclei of the monkey thalamus. , 1980, Acta neurobiologiae experimentalis.

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

[20]  A. Parent,et al.  The origin of forebrain afferents to the habenula in rat, cat and monkey , 1981, Brain Research Bulletin.

[21]  P. Somogyi,et al.  Monosynaptic input from the nucleus accumbens-ventral striatum region to retrogradely labelled nigrostriatal neurones , 1981, Brain Research.

[22]  N. Aronin,et al.  Light and electron microscopic localization of immunoreactive Leu- enkephalin in the monkey basal ganglia , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  P. Bailey The neurobiology of the nucleus accumbens R. B. Chronister and J. F. de France (Eds). Haer Institute for Electrophysiological Research (1981). 388 pp , 1982, Neuroscience.

[24]  L. Heimer,et al.  Ventral striatum and ventral pallidum Components of the motor system? , 1982, Trends in Neurosciences.

[25]  D. Jacobowitz,et al.  A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[26]  N. White,et al.  Conditioned place preference from intra-accumbens but not intra-caudate amphetamine injections. , 1983, Life sciences.

[27]  M. Giguére,et al.  Comparative morphology of the substantia nigra and ventral tegmental area in the monkey, cat and rat , 1983, Brain Research Bulletin.

[28]  W. Nauta,et al.  Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry , 1983, Neuroscience.

[29]  L. Heimer,et al.  The ventral pallidal projection to the mediodorsal thalamus: a study with fluorescent retrograde tracers and immunohistofluorescence , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  A. Parent,et al.  The striatopallidal and striatonigral projections: two distinct fiber systems in primate , 1984, Brain Research.

[31]  Jérôme Yelnik,et al.  A histological atlas of the macaque (Macaca, mulatta) substantia nigra in ventricular coordinates , 1985, Brain Research Bulletin.

[32]  W. Nauta,et al.  Efferent connections of the ventral pallidum: Evidence of a dual striato pallidofugal pathway , 1985, The Journal of comparative neurology.

[33]  S. Haber,et al.  The comparative distribution of enkephalin, dynorphin and substance P in the human globus pallidus and basal forebrain , 1985, Neuroscience.

[34]  D. Amaral,et al.  The amygdalostriatal projections in the monkey. An anterograde tracing study , 1985, Brain Research.

[35]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  S. Bayer,et al.  Neurogenesis in the olfactory tubercle and islands of Calleja in the rat , 1985, International Journal of Developmental Neuroscience.

[37]  A. Hopf,et al.  Substance P in the human brain , 1986, Neuroscience.

[38]  G. Halliday,et al.  Comparative anatomy of the ventromedial mesencephalic tegmentum in the rat, cat, monkey and human , 1986, The Journal of comparative neurology.

[39]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[40]  S. Haber Anatomical relationship between the basal ganglia and the basal nucleus of Meynert in human and monkey forebrain. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[41]  T. Beach,et al.  Light microscopic evidence for a substance P-containing innervation of the human nucleus basalis of Meynert , 1987, Brain Research.

[42]  H. T. Chang,et al.  Enkephalinergic-cholinergic interaction in the rat globus pallidus: a pre-embedding double-labeling immunocytochemistry study , 1987, Brain Research.

[43]  L. Heimer,et al.  New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: The striatopallidal, amygdaloid, and corticopetal components of substantia innominata , 1988, Neuroscience.

[44]  H. Kimura,et al.  The efferent projections of the rat lateral habenular nucleus revealed by the PHA-L anterograde tracing method , 1988, Brain Research.

[45]  R. Villalba,et al.  Distribution of enkephalin-immunoreactive nerve fibres and terminals in the region of the nucleus basalis magnocellularis of the rat: a light and electron microscopic study , 1988, Journal of neurocytology.

[46]  T. Robbins,et al.  Interactions between the amygdala and ventral striatum in stimulus-reward associations: Studies using a second-order schedule of sexual reinforcement , 1989, Neuroscience.

[47]  G. Meyer,et al.  Aggregations of granule cells in the basal forebrain (islands of Calleja): Golgi and cytoarchitectonic study in different mammals, including man , 1989, The Journal of comparative neurology.

[48]  T. Robbins,et al.  Involvement of the amygdala in stimulus-reward associations: Interaction with the ventral striatum , 1989, Neuroscience.

[49]  H. Groenewegen,et al.  Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum , 1990, The Journal of comparative neurology.

[50]  S. Haber,et al.  Topographic organization of the ventral striatal efferent projections in the rhesus monkey: An anterograde tracing study , 1990, The Journal of comparative neurology.

[51]  S. Haber,et al.  The relationship between ventral striatal efferent fibers and the distribution of peptide-positive woolly fibers in the forebrain of the rhesus monkey , 1990, Neuroscience.

[52]  P. Goldman-Rakic,et al.  Topographic intermingling of striatonigral and striatopallidal neurons in the rhesus monkey , 1990, The Journal of comparative neurology.

[53]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[54]  L. Heimer,et al.  Piecing together the puzzle of basal forebrain anatomy. , 1991, Advances in experimental medicine and biology.

[55]  A. Parent,et al.  Dopaminergic neurons expressing calbindin in normal and parkinsonian monkeys. , 1991, Neuroreport.

[56]  J. Hedreen,et al.  Organization of striatopallidal, striatonigral, and nigrostriatal projections in the macaque , 1991, The Journal of comparative neurology.

[57]  P. Kalivas,et al.  The basal forebrain : anatomy to function , 1991 .

[58]  P. Goldman-Rakic,et al.  Distribution of dopaminergic receptors in the primate cerebral cortex: Quantitative autoradiographic analysis using [3H]raclopride, [3H]spiperone and [3H]SCH23390 , 1991, Neuroscience.

[59]  G. Percheron,et al.  Parallel processing in the basal ganglia: up to a point , 1991, Trends in Neurosciences.

[60]  A. Deutch,et al.  Topography and functional role of dopaminergic projections from the ventral mesencephalic tegmentum to the ventral pallidum , 1992, Neuroscience.

[61]  W. Cullinan,et al.  Projections from the nucleus accumbens to cholinergic neurons of the ventral pallidum: a correlated light and electron microscopic double-immunolabeling study in rat , 1992, Brain Research.

[62]  H. Barbas,et al.  Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. , 1992, Advances in neurology.

[63]  B. A. Brooks,et al.  Midbrain Dopaminergic Cell Loss in Parkinson's Disease and MPTP‐Induced Parkinsonism: Sparing of Calbindin‐D25k—Containing Cells a , 1992, Annals of the New York Academy of Sciences.

[64]  D. Lewis The catecholaminergic innervation of primate prefrontal cortex. , 1992, Journal of neural transmission. Supplementum.

[65]  W. Schultz,et al.  Neuronal activity in monkey ventral striatum related to the expectation of reward , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  J. Kaas,et al.  Topography and collateralization of the dopaminergic projections to motor and lateral prefrontal cortex in owl monkeys , 1992, The Journal of comparative neurology.

[67]  R. Huganir,et al.  AMPA glutamate receptor subunits are differentially distributed in rat brain , 1993, Neuroscience.

[68]  P. Goldman-Rakic,et al.  Characterization of the dopaminergic innervation of the primate frontal cortex using a dopamine-specific antibody. , 1993, Cerebral cortex.

[69]  A. Parent,et al.  The heterogeneity of the mesostriatal dopaminergic system as revealed in normal and parkinsonian monkeys. , 1993, Advances in neurology.

[70]  D. S. Zahm,et al.  Specificity in the efferent projections of the nucleus accumbens in the rat: Comparison of the rostral pole projection patterns with those of the core and shell , 1993, The Journal of comparative neurology.

[71]  G. Doucet,et al.  Ultrastructure and synaptic targets of the raphe-nigral projection in the rat , 1993, Neuroscience.

[72]  S. Haber,et al.  The organization of the descending ventral pallidal projections in the monkey , 1993, The Journal of comparative neurology.

[73]  J. Price,et al.  The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys , 1993, The Journal of comparative neurology.

[74]  M. Tohyama,et al.  The differential expression patterns of messenger RNAs encoding non-N-methyl-d-aspartate glutamate receptor subunits (GluR1–4) in the rat brain , 1993, Neuroscience.

[75]  A. Graybiel,et al.  Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  S. N. Haber,et al.  The organization of midbrain projections to the ventral striatum in the primate , 1994, Neuroscience.

[77]  M. Petrides Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

[78]  A. Parent,et al.  Pedunculopontine nucleus in the squirrel monkey: Projections to the basal ganglia as revealed by anterograde tract‐tracing methods , 1994, The Journal of comparative neurology.

[79]  S. Haber,et al.  Primate striatonigral projections: A comparison of the sensorimotor‐related striatum and the ventral striatum , 1994, The Journal of comparative neurology.

[80]  S. Haber,et al.  The organization of midbrain projections to the striatum in the primate: Sensorimotor-related striatum versus ventral striatum , 1994, Neuroscience.

[81]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[82]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[83]  D. Joel,et al.  The organization of the basal ganglia-thalamocortical circuits: Open interconnected rather than closed segregated , 1994, Neuroscience.

[84]  A. Parent,et al.  Pedunculopontine nucleus in the squirrel monkey: Cholinergic and glutamatergic projections to the substantia nigra , 1994, The Journal of comparative neurology.

[85]  S. Hersch,et al.  The dopamine transporter: immunochemical characterization and localization in brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[86]  S. Haber,et al.  Subsets of midbrain dopaminergic neurons in monkeys are distinguished by different levels of mRNA for the dopamine transporter: Comparison with the mRNA for the D2 receptor, tyrosine hydroxylase and calbindin immunoreactivity , 1995, The Journal of comparative neurology.

[87]  S de las Heras,et al.  Organization of thalamic projections to the ventral striatum in the primate , 1995, The Journal of comparative neurology.

[88]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[89]  G. Halliday,et al.  Calbindin D28k-containing neurons are restricted to the medial substantia nigra in humans , 1995, Neuroscience.

[90]  E. Lynd-Balta,et al.  The orbital and medial prefrontal circuit through the primate basal ganglia , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[91]  L. Porrino,et al.  Cocaine alters cerebral metabolism within the ventral striatum and limbic cortex of monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[92]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  A. D. Smith,et al.  The substantia nigra as a site of synaptic integration of functionally diverse information arising from the ventral pallidum and the globus pallidus in the rat , 1996, Neuroscience.

[94]  R. Wise,et al.  Rewarding Actions of Phencyclidine and Related Drugs in Nucleus Accumbens Shell and Frontal Cortex , 1996, The Journal of Neuroscience.

[95]  S. Haber,et al.  Ventral pallidostriatal pathway in the monkey: evidence for modulation of basal ganglia circuits. , 1996, The Journal of comparative neurology.

[96]  B. Richmond,et al.  Neural signals in the monkey ventral striatum related to motivation for juice and cocaine rewards. , 1996, Journal of neurophysiology.

[97]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[98]  S. Haber,et al.  Shell and core in monkey and human nucleus accumbens identified with antibodies to calbindin‐D28k , 1996, The Journal of comparative neurology.

[99]  R. Guillery,et al.  Functional organization of thalamocortical relays. , 1996, Journal of neurophysiology.

[100]  S. Augood,et al.  Dopamine transporter (Dat) and synaptic vesicle amine transporter (VMAT2) gene expression in the substantia nigra of control and Parkinson's disease. , 1996, Brain research. Molecular brain research.

[101]  C. Blaha,et al.  Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopontine tegmental nucleus-lesioned, and laterodorsal tegmental nucleus-lesioned rats , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[102]  Y. Smith,et al.  Efferent connections of the internal globus pallidus in the squirrel monkey: I. topography and synaptic organization of the pallidothalamic projection , 1997, The Journal of comparative neurology.

[103]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[104]  J. Bolam,et al.  Synaptic Integration of Functionally Diverse Pallidal Information in the Entopeduncular Nucleus and Subthalamic Nucleus in the Rat , 1997, The Journal of Neuroscience.

[105]  Suzanne N. Haber,et al.  Insular Cortical Projections to Functional Regions of the Striatum Correlate with Cortical Cytoarchitectonic Organization in the Primate , 1997, The Journal of Neuroscience.

[106]  R. J. Dolan,et al.  Differential neural response to positive and negative feedback in planning and guessing tasks , 1997, Neuropsychologia.

[107]  S. Hersch,et al.  Subcellular localization and molecular topology of the dopamine transporter in the striatum and substantia nigra , 1997, The Journal of comparative neurology.

[108]  A. Charara,et al.  The striatopallidal fiber system in primates. , 1997, Advances in neurology.

[109]  S. Hyman,et al.  Acute Effects of Cocaine on Human Brain Activity and Emotion , 1997, Neuron.

[110]  Gregor Thut,et al.  Activation of the human brain by monetary reward , 1997, Neuroreport.

[111]  C. Rampon,et al.  Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods , 1997, Neuroscience.

[112]  Masahiko Inase,et al.  Corticostriatal input zones from the supplementary motor area overlap those from the contra- rather than ipsilateral primary motor cortex , 1998, Brain Research.

[113]  J. Penney,et al.  Regional dopamine transporter gene expression in the substantia nigra from control and Parkinson’s disease brains , 1998, Journal of neurology, neurosurgery, and psychiatry.

[114]  L. Brown,et al.  Organizing principles of cortical integration in the rat neostriatum: Corticostriate map of the body surface is an ordered lattice of curved laminae and radial points , 1998, The Journal of comparative neurology.

[115]  D. Brooks,et al.  Evidence for striatal dopamine release during a video game , 1998, Nature.

[116]  R. Buckner,et al.  Human Brain Mapping 6:373–377(1998) � Event-Related fMRI and the Hemodynamic Response , 2022 .

[117]  C. Darian‐Smith,et al.  Comparing thalamocortical and corticothalamic microstructure and spatial reciprocity in the macaque ventral posterolateral nucleus (VPLc) and medial pulvinar , 1999, The Journal of comparative neurology.

[118]  A. Parent,et al.  The pallidofugal projection system in primates: evidence for neurons branching ipsilaterally and contralaterally to the thalamus and brainstem , 1999, Journal of Chemical Neuroanatomy.

[119]  P. Goldman-Rakic,et al.  The primate mesocortical dopamine system , 1999 .

[120]  Nikolaus R. McFarland,et al.  The Concept of the Ventral Striatum in Nonhuman Primates , 1999, Annals of the New York Academy of Sciences.

[121]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[122]  S. Haber,et al.  The distribution of dynorphinergic terminals in striatal target regions in comparison to the distribution of substance P-containing and enkephalinergic terminals in monkeys and humans , 1999, Neuroscience.

[123]  N. Volkow,et al.  Reinforcing effects of psychostimulants in humans are associated with increases in brain dopamine and occupancy of D(2) receptors. , 1999, The Journal of pharmacology and experimental therapeutics.

[124]  Carol A. Seger,et al.  Striatal activation during acquisition of a cognitive skill. , 1999, Neuropsychology.

[125]  S. Charpier,et al.  In vivo induction of striatal long-term potentiation by low-frequency stimulation of the cerebral cortex , 1999, Neuroscience.

[126]  T. Robbins,et al.  Choosing between Small, Likely Rewards and Large, Unlikely Rewards Activates Inferior and Orbital Prefrontal Cortex , 1999, The Journal of Neuroscience.

[127]  L. Heimer,et al.  Chapter II – The human basal forebrain. Part II , 1999 .

[128]  T. Robbins,et al.  Associative Processes in Addiction and Reward The Role of Amygdala‐Ventral Striatal Subsystems , 1999, Annals of the New York Academy of Sciences.

[129]  S. Haber,et al.  The central nucleus of the amygdala projection to dopamine subpopulations in primates , 2000, Neuroscience.

[130]  C. Rouillard,et al.  Dorsal raphe stimulation differentially modulates dopaminergic neurons in the ventral tegmental area and substantia nigra , 2000, Synapse.

[131]  K L Leenders,et al.  Reduced reward processing in the brains of Parkinsonian patients , 2000, Neuroreport.

[132]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[133]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[134]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[135]  B. Everitt,et al.  Limbic cortical-ventral striatal systems underlying appetitive conditioning. , 2000, Progress in brain research.

[136]  Brian Knutson,et al.  FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task , 2000, NeuroImage.

[137]  M. Merello,et al.  [Functional anatomy of the basal ganglia]. , 2000, Revista de neurologia.

[138]  J. Hollerman,et al.  Reward processing in primate orbitofrontal cortex and basal ganglia. , 2000, Cerebral cortex.

[139]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[140]  W. Schultz,et al.  Reward-related neuronal activity during go-nogo task performance in primate orbitofrontal cortex. , 2000, Journal of neurophysiology.

[141]  J. Price,et al.  Prefrontal cortical projections to the striatum in macaque monkeys: Evidence for an organization related to prefrontal networks , 2000, The Journal of comparative neurology.

[142]  Karl J. Friston,et al.  Dissociable Neural Responses in Human Reward Systems , 2000, The Journal of Neuroscience.

[143]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

[144]  W. Schultz Multiple reward signals in the brain , 2000, Nature Reviews Neuroscience.

[145]  Nikolaus R. McFarland,et al.  Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum , 2000, The Journal of Neuroscience.

[146]  L. Nystrom,et al.  Tracking the hemodynamic responses to reward and punishment in the striatum. , 2000, Journal of neurophysiology.

[147]  Nikolaus R. McFarland,et al.  Organization of thalamostriatal terminals from the ventral motor nuclei in the macaque , 2001, The Journal of comparative neurology.

[148]  Samuel M. McClure,et al.  Predictability Modulates Human Brain Response to Reward , 2001, The Journal of Neuroscience.

[149]  S. Haber,et al.  Bed nucleus of the stria terminalis and extended amygdala inputs to dopamine subpopulations in primates , 2001, Neuroscience.

[150]  D. Ariely,et al.  Beautiful Faces Have Variable Reward Value fMRI and Behavioral Evidence , 2001, Neuron.

[151]  D. Kahneman,et al.  Functional Imaging of Neural Responses to Expectancy and Experience of Monetary Gains and Losses tasks with monetary payoffs , 2001 .

[152]  J. Deniau,et al.  Segregation and Convergence of Information Flow through the Cortico-Subthalamic Pathways , 2001, The Journal of Neuroscience.

[153]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[154]  D. Kupfer,et al.  Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria , 2001, Biological Psychiatry.

[155]  Brian Knutson,et al.  Dissociation of reward anticipation and outcome with event-related fMRI , 2001, Neuroreport.

[156]  Alan C. Evans,et al.  Changes in brain activity related to eating chocolate: from pleasure to aversion. , 2001, Brain : a journal of neurology.

[157]  W. Schultz,et al.  Changes in brain activation associated with reward processing in smokers and nonsmokers , 2001, Experimental Brain Research.

[158]  Osama Mawlawi,et al.  Imaging Human Mesolimbic Dopamine Transmission with Positron Emission Tomography: I. Accuracy and Precision of D2 Receptor Parameter Measurements in Ventral Striatum , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[159]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[160]  A. Grace,et al.  Regulation of Limbic Information Outflow by the Subthalamic Nucleus: Excitatory Amino Acid Projections to the Ventral Pallidum , 2001, The Journal of Neuroscience.

[161]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[162]  R. Zatorre,et al.  Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[163]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[164]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[165]  Nikolaus R. McFarland,et al.  Thalamic Relay Nuclei of the Basal Ganglia Form Both Reciprocal and Nonreciprocal Cortical Connections, Linking Multiple Frontal Cortical Areas , 2002, The Journal of Neuroscience.

[166]  A. Dagher,et al.  Amphetamine-Induced Increases in Extracellular Dopamine, Drug Wanting, and Novelty Seeking: A PET/[11C]Raclopride Study in Healthy Men , 2002, Neuropsychopharmacology.

[167]  J. Yelnik Functional anatomy of the basal ganglia , 2002, Movement disorders : official journal of the Movement Disorder Society.

[168]  K. Berridge,et al.  The Neuroscience of Natural Rewards: Relevance to Addictive Drugs , 2002, The Journal of Neuroscience.

[169]  A. Syrota,et al.  In Vivo Detection of Striatal Dopamine Release during Reward: A PET Study with [11C]Raclopride and a Single Dynamic Scan Approach , 2002, NeuroImage.

[170]  S. Haber,et al.  Amygdaloid projections to ventromedial striatal subterritories in the primate , 2002, Neuroscience.

[171]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[172]  Klaas E. Stephan,et al.  The anatomical basis of functional localization in the cortex , 2002, Nature Reviews Neuroscience.

[173]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[174]  W. Schultz Getting Formal with Dopamine and Reward , 2002, Neuron.

[175]  J. O'Doherty,et al.  Appetitive and Aversive Olfactory Learning in Humans Studied Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[176]  M. Petrides,et al.  Differential activation of the human orbital, mid-ventrolateral, and mid-dorsolateral prefrontal cortex during the processing of visual stimuli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[177]  T. Napier,et al.  Mu and kappa opioid agonists modulate ventral tegmental area input to the ventral pallidum , 2002, The European journal of neuroscience.

[178]  Charles J. Wilson,et al.  Corticostriatal combinatorics: the implications of corticostriatal axonal arborizations. , 2002, Journal of neurophysiology.

[179]  Richard C Saunders,et al.  Comparison of hippocampal, amygdala, and perirhinal projections to the nucleus accumbens: Combined anterograde and retrograde tracing study in the Macaque brain , 2002, The Journal of comparative neurology.

[180]  R. Wise Brain Reward Circuitry Insights from Unsensed Incentives , 2002, Neuron.

[181]  J. Deniau,et al.  Synaptic Convergence of Motor and Somatosensory Cortical Afferents onto GABAergic Interneurons in the Rat Striatum , 2002, Journal of Neuroscience.

[182]  S. Kapur,et al.  Direct Activation of the Ventral Striatum in Anticipation of Aversive Stimuli , 2003, Neuron.

[183]  Brian Knutson,et al.  A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI , 2003, NeuroImage.

[184]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[185]  D. V. von Cramon,et al.  Error Monitoring Using External Feedback: Specific Roles of the Habenular Complex, the Reward System, and the Cingulate Motor Area Revealed by Functional Magnetic Resonance Imaging , 2003, The Journal of Neuroscience.

[186]  D. Zald The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[187]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[188]  A. Dagher,et al.  Alcohol promotes dopamine release in the human nucleus accumbens , 2003, Synapse.

[189]  M. Mesulam,et al.  Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation , 2003, Neuron.

[190]  E. Miller,et al.  Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task , 2003, The European journal of neuroscience.

[191]  Matthew F S Rushworth,et al.  Functional Specialization within Medial Frontal Cortex of the Anterior Cingulate for Evaluating Effort-Related Decisions , 2003, The Journal of Neuroscience.

[192]  E T Rolls,et al.  Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. , 2003, Cerebral cortex.

[193]  Samuel M. McClure,et al.  Temporal Prediction Errors in a Passive Learning Task Activate Human Striatum , 2003, Neuron.

[194]  Wolfram Schultz,et al.  Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. , 2003, Journal of neurophysiology.

[195]  Karl J. Friston,et al.  Temporal Difference Models and Reward-Related Learning in the Human Brain , 2003, Neuron.

[196]  J. O'Doherty,et al.  Dissociating Valence of Outcome from Behavioral Control in Human Orbital and Ventral Prefrontal Cortices , 2003, The Journal of Neuroscience.

[197]  M. Delgado,et al.  Dorsal striatum responses to reward and punishment: Effects of valence and magnitude manipulations , 2003, Cognitive, affective & behavioral neuroscience.

[198]  S. Haber,et al.  Imaging Human Mesolimbic Dopamine Transmission with Positron Emission Tomography. Part II: Amphetamine-Induced Dopamine Release in the Functional Subdivisions of the Striatum , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[199]  M. Greicius,et al.  Humor Modulates the Mesolimbic Reward Centers , 2003, Neuron.

[200]  Saori C. Tanaka,et al.  Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops , 2004, Nature Neuroscience.

[201]  Samuel M. McClure,et al.  The Neural Substrates of Reward Processing in Humans: The Modern Role of fMRI , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[202]  Karl J. Friston,et al.  Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning , 2004, Science.

[203]  Samuel M. McClure,et al.  Separate Neural Systems Value Immediate and Delayed Monetary Rewards , 2004, Science.

[204]  T. Matsuura,et al.  Light and electron microscopic immunohistochemical studies of serotonin nerve fibers in the substantia nigra of the rat, cat and monkey , 2004, Anatomy and Embryology.

[205]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[206]  T. Robbins,et al.  Differential control over cocaine-seeking behavior by nucleus accumbens core and shell , 2004, Nature Neuroscience.

[207]  F. McGlone,et al.  Dopamine Transmission in the Human Striatum during Monetary Reward Tasks , 2004, The Journal of Neuroscience.

[208]  H. Fibiger,et al.  Neurochemical heterogeneity of the primate nucleus accumbens , 2004, Experimental Brain Research.

[209]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[210]  N. Swindale,et al.  Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans , 2004, Annals of neurology.

[211]  R. E. Passingham,et al.  Prediction error for free monetary reward in the human prefrontal cortex , 2004, NeuroImage.

[212]  Michael A. Nader,et al.  Behavioral/systems/cognitive Cocaine Self-administration Produces a Progressive Involvement of Limbic, Association, and Sensorimotor Striatal Domains , 2022 .

[213]  M. Roesch,et al.  Neuronal Activity Related to Reward Value and Motivation in Primate Frontal Cortex , 2004, Science.

[214]  David A Lewis,et al.  Cortical connections of the lateral mediodorsal thalamus in cynomolgus monkeys , 2004, The Journal of comparative neurology.

[215]  H. Heinze,et al.  Reward-Related fMRI Activation of Dopaminergic Midbrain Is Associated with Enhanced Hippocampus- Dependent Long-Term Memory Formation , 2005, Neuron.

[216]  Daniel J. Levitin,et al.  The rewards of music listening: Response and physiological connectivity of the mesolimbic system , 2005, NeuroImage.

[217]  Matthew T. Kaufman,et al.  Distributed Neural Representation of Expected Value , 2005, The Journal of Neuroscience.

[218]  Helen E. Fisher,et al.  Reward, motivation, and emotion systems associated with early-stage intense romantic love. , 2005, Journal of neurophysiology.

[219]  Camelia M. Kuhnen,et al.  The Neural Basis of Financial Risk Taking , 2005, Neuron.

[220]  E. Miller,et al.  Different time courses of learning-related activity in the prefrontal cortex and striatum , 2005, Nature.

[221]  T. Robbins,et al.  Neural systems of reinforcement for drug addiction: from actions to habits to compulsion , 2005, Nature Neuroscience.

[222]  J. Doyon,et al.  Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[223]  B. Vogt,et al.  Architecture and neurocytology of monkey cingulate gyrus , 2005, The Journal of comparative neurology.

[224]  Stéphane Charpier,et al.  Feedforward Inhibition of Projection Neurons by Fast-Spiking GABA Interneurons in the Rat Striatum In Vivo , 2005, The Journal of Neuroscience.

[225]  J. Mayhew,et al.  How Visual Stimuli Activate Dopaminergic Neurons at Short Latency , 2005, Science.

[226]  Dirk J. Heslenfeld,et al.  Activity in human reward-sensitive brain areas is strongly context dependent , 2005, NeuroImage.

[227]  J. Bolam,et al.  THE PEDUNCULOPONTINE NUCLEUS : Towards a Functional Integration with the Basal Ganglia , 2005 .

[228]  S. Inati,et al.  An fMRI study of reward-related probability learning , 2005, NeuroImage.

[229]  O. Hikosaka,et al.  Immediate changes in anticipatory activity of caudate neurons associated with reversal of position-reward contingency. , 2005, Journal of neurophysiology.

[230]  R. Adolphs,et al.  Electrophysiological correlates of reward prediction error recorded in the human prefrontal cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[231]  N. Volkow,et al.  Unmanageable Motivation in Addiction: A Pathology in Prefrontal-Accumbens Glutamate Transmission , 2005, Neuron.

[232]  S. Haber,et al.  Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning , 2006, The Journal of Neuroscience.

[233]  J. Morton,et al.  Choosing the Lesser of Two Evils, the Better of Two Goods: Specifying the Roles of Ventromedial Prefrontal Cortex and Dorsal Anterior Cingulate in Object Choice , 2006, The Journal of Neuroscience.

[234]  K. Berman,et al.  Cerebral Cortex doi:10.1093/cercor/bhj004 Neural Coding of Distinct Statistical Properties of Reward Information in Humans , 2005 .

[235]  C. Padoa-Schioppa,et al.  Neurons in the orbitofrontal cortex encode economic value , 2006, Nature.

[236]  N. Volkow,et al.  Cocaine Cues and Dopamine in Dorsal Striatum: Mechanism of Craving in Cocaine Addiction , 2006, The Journal of Neuroscience.

[237]  B. Moghaddam,et al.  Rule Learning and Reward Contingency Are Associated with Dissociable Patterns of Dopamine Activation in the Rat Prefrontal Cortex, Nucleus Accumbens, and Dorsal Striatum , 2006, The Journal of Neuroscience.

[238]  J. O'Doherty,et al.  Is Avoiding an Aversive Outcome Rewarding? Neural Substrates of Avoidance Learning in the Human Brain , 2006, PLoS biology.

[239]  N. Bunzeck,et al.  Absolute Coding of Stimulus Novelty in the Human Substantia Nigra/VTA , 2006, Neuron.

[240]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[241]  H. Fields,et al.  Inhibitions of Nucleus Accumbens Neurons Encode a Gating Signal for Reward-Directed Behavior , 2006, The Journal of Neuroscience.

[242]  S. Quartz,et al.  Neural Differentiation of Expected Reward and Risk in Human Subcortical Structures , 2006, Neuron.

[243]  Brian Knutson,et al.  Reward-Motivated Learning: Mesolimbic Activation Precedes Memory Formation , 2006, Neuron.

[244]  Martin Parent,et al.  Single‐axon tracing study of corticostriatal projections arising from primary motor cortex in primates , 2006, The Journal of comparative neurology.

[245]  J. Gläscher,et al.  Dissociable Systems for Gain- and Loss-Related Value Predictions and Errors of Prediction in the Human Brain , 2006, The Journal of Neuroscience.

[246]  Henrik Walter,et al.  Prediction error as a linear function of reward probability is coded in human nucleus accumbens , 2006, NeuroImage.

[247]  Kyle S. Smith,et al.  Ventral pallidum firing codes hedonic reward: when a bad taste turns good. , 2006, Journal of neurophysiology.

[248]  S. Haber,et al.  Prefrontal Cortical Projections to the Midbrain in Primates: Evidence for a Sparse Connection , 2006, Neuropsychopharmacology.

[249]  James L. McClelland,et al.  Performance Feedback Drives Caudate Activation in a Phonological Learning Task , 2006, Journal of Cognitive Neuroscience.

[250]  J. O'Doherty,et al.  Reward Value Coding Distinct From Risk Attitude-Related Uncertainty Coding in Human Reward Systems , 2006, Journal of neurophysiology.

[251]  Samuel M. McClure,et al.  Time Discounting for Primary Rewards , 2007, The Journal of Neuroscience.

[252]  P. Shepard,et al.  Lateral Habenula Stimulation Inhibits Rat Midbrain Dopamine Neurons through a GABAA Receptor-Mediated Mechanism , 2007, The Journal of Neuroscience.

[253]  J. O'Doherty,et al.  Orbitofrontal Cortex Encodes Willingness to Pay in Everyday Economic Transactions , 2007, The Journal of Neuroscience.

[254]  J. O'Doherty,et al.  Neural coding of reward-prediction error signals during classical conditioning with attractive faces. , 2007, Journal of neurophysiology.

[255]  O. Hikosaka,et al.  Lateral habenula as a source of negative reward signals in dopamine neurons , 2007, Nature.

[256]  Kyle S. Smith,et al.  Opioid Limbic Circuit for Reward: Interaction between Hedonic Hotspots of Nucleus Accumbens and Ventral Pallidum , 2007, The Journal of Neuroscience.

[257]  Yasushi Kobayashi,et al.  Reward Prediction Error Computation in the Pedunculopontine Tegmental Nucleus Neurons , 2007, Annals of the New York Academy of Sciences.

[258]  Tobias Sommer,et al.  Subregions of the ventral striatum show preferential coding of reward magnitude and probability , 2007, NeuroImage.

[259]  E. Murray The amygdala, reward and emotion , 2007, Trends in Cognitive Sciences.

[260]  G. Loewenstein,et al.  Neural Predictors of Purchases , 2007, Neuron.

[261]  H. Barbas,et al.  Parallel Driving and Modulatory Pathways Link the Prefrontal Cortex and Thalamus , 2007, PloS one.

[262]  Kevin McCabe,et al.  Neural signature of fictive learning signals in a sequential investment task , 2007, Proceedings of the National Academy of Sciences.

[263]  D. R. Ramirez,et al.  Differential involvement of the basolateral amygdala, orbitofrontal cortex, and nucleus accumbens core in the acquisition and use of reward expectancies. , 2007, Behavioral neuroscience.

[264]  P. Glimcher,et al.  The neural correlates of subjective value during intertemporal choice , 2007, Nature Neuroscience.

[265]  S. Boye,et al.  Electrolytic lesions of the habenula attenuate brain stimulation reward , 2008, Behavioural Brain Research.

[266]  Kerstin Preuschoff,et al.  Investigating signal integration with canonical correlation analysis of fMRI brain activation data , 2008, NeuroImage.

[267]  George I. Christopoulos,et al.  Neuronal Distortions of Reward Probability without Choice , 2008, The Journal of Neuroscience.

[268]  Valeria Della-Maggiore,et al.  Functional integration across a gradient of corticostriatal channels controls UP state transitions in the dorsal striatum , 2008, Proceedings of the National Academy of Sciences.

[269]  Simon Hong,et al.  New Insights on the Subcortical Representation of Reward This Review Comes from a Themed Issue on Cognitive Neuroscience Edited Lateral Habenula Serotonin Neurons , 2022 .

[270]  Brian Knutson,et al.  Anticipatory affect: neural correlates and consequences for choice , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[271]  B. Everitt,et al.  Cocaine Seeking Habits Depend upon Dopamine-Dependent Serial Connectivity Linking the Ventral with the Dorsal Striatum , 2008, Neuron.

[272]  Kae Nakamura,et al.  Reward-Dependent Modulation of Neuronal Activity in the Primate Dorsal Raphe Nucleus , 2008, The Journal of Neuroscience.

[273]  Richard S. J. Frackowiak,et al.  Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia , 2008, The Journal of Neuroscience.

[274]  Brian Knutson,et al.  Valence and salience contribute to nucleus accumbens activation , 2008, NeuroImage.

[275]  Brian Knutson,et al.  Neural Responses to Monetary Incentives in Major Depression , 2008, Biological Psychiatry.

[276]  Bruno B. Averbeck,et al.  The Statistical Neuroanatomy of Frontal Networks in the Macaque , 2008, PLoS Comput. Biol..

[277]  Samuel M. McClure,et al.  BOLD Responses Reflecting Dopaminergic Signals in the Human Ventral Tegmental Area , 2008, Science.

[278]  J. Gläscher,et al.  Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. , 2009, Cerebral cortex.

[279]  S. Kennerley,et al.  Reward-Dependent Modulation of Working Memory in Lateral Prefrontal Cortex , 2009, The Journal of Neuroscience.

[280]  Sylvia M. L. Cox,et al.  Striatal Dopamine Responses to Intranasal Cocaine Self-Administration in Humans , 2009, Biological Psychiatry.

[281]  D. Kumaran,et al.  The Neurobiology of Reference-Dependent Value Computation , 2009, NeuroImage.

[282]  Brian Knutson,et al.  Dissociable neural representations of future reward magnitude and delay during temporal discounting , 2009, NeuroImage.

[283]  Joseph T. McGuire,et al.  Effort discounting in human nucleus accumbens , 2009, Cognitive, affective & behavioral neuroscience.

[284]  Michael X. Cohen,et al.  Connectivity-based segregation of the human striatum predicts personality characteristics , 2009, Nature Neuroscience.

[285]  Timothy Edward John Behrens,et al.  Effort-Based Cost–Benefit Valuation and the Human Brain , 2009, The Journal of Neuroscience.

[286]  Colin Camerer,et al.  Neural Response to Reward Anticipation under Risk Is Nonlinear in Probabilities , 2009, The Journal of Neuroscience.

[287]  Peter Redgrave,et al.  Tectonigral projections in the primate: a pathway for pre‐attentive sensory input to midbrain dopaminergic neurons , 2009, The European journal of neuroscience.

[288]  Michael X. Cohen,et al.  Neuroelectric Signatures of Reward Learning and Decision-Making in the Human Nucleus Accumbens , 2009, Neuropsychopharmacology.

[289]  P. Tobler,et al.  Functional imaging of the human dopaminergic midbrain , 2009, Trends in Neurosciences.