Integrative Networks Across Basal Ganglia Circuits

Publisher Summary This chapter reviews the basic circuitry that underlies parallel processing. It outlines the anatomical basis for integration across different cortico-basal ganglia circuits; and also discusses functional data that support integrative processing through the basal ganglia. The basal ganglia (BG) work in concert with the frontal cortex to orchestrate and execute motivated, planned behaviors requiring limbic, cognitive, and motor control systems. The basal ganglia are traditionally considered to process this information in parallel and segregated functional streams consisting of reward, associative, and motor control circuits. It reviews that frontal cortex contains divisions associated with specific functions; expressed behaviors are the result of a combination of complex information processing that involves all of frontal cortex. Indeed, appropriate responses to environmental stimuli require continual updating, and learning to adjust behaviors according to new data. This necessitates coordination between limbic, cognitive, and motor systems, to form smoothly executed, goal-directed behaviors. Parallel processing of functional information through different basal ganglia circuits does not address how information flows between circuits, thereby developing new, or adapting to previously, learned behaviors. While the anatomical pathways appear to be generally topographic from cortex through BG circuits, and there are some physiological correlates to the functional domains of the striatum, a large growing body of evidence supports a duel processing system. Thus, information is not only processed in parallel streams, but also through integrative mechanisms through which information can be transferred between functional circuits.

[1]  A. Graybiel,et al.  Chapter III Chemical architecture of the basal ganglia , 1999 .

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

[3]  H. Kuo,et al.  Ventral pallido‐striatal pathway in the rat brain: A light and electron microscopic study , 1992, The Journal of comparative neurology.

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

[5]  W. Schultz,et al.  Responses to reward in monkey dorsal and ventral striatum , 2004, Experimental Brain Research.

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

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

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

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

[10]  M. Kimura The role of primate putamen neurons in the association of sensory stimuli with movement , 1986, Neuroscience Research.

[11]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

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

[13]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

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

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

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

[17]  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.

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

[19]  J W Aldridge,et al.  Sensory-motor processing in the caudate nucleus and globus pallidus: a single-unit study in behaving primates. , 1980, Canadian journal of physiology and pharmacology.

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

[21]  P. Strick,et al.  Motor areas on the medial wall of the hemisphere. , 1998, Novartis Foundation symposium.

[22]  E. Welker,et al.  Organization of the projections from barrel cortex to thalamus in mice studied with Phaseolus vulgaris-leucoagglutinin and HRP , 2004, Experimental Brain Research.

[23]  T. Robbins,et al.  Differential Responses in Human Striatum and Prefrontal Cortex to Changes in Object and Rule Relevance , 2004, The Journal of Neuroscience.

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

[25]  A. Graybiel,et al.  Functions of the Cortico-Basal Ganglia Loop , 1995, Springer Japan.

[26]  M. Herkenham,et al.  New Perspectives on the Organization and Evolution of Nonspecific Thalamocortical Projections , 1986 .

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

[28]  D. R. Snyder,et al.  Alterations in aversive and aggressive behaviors following orbital frontal lesions in rhesus monkeys. , 1972, Acta neurobiologiae experimentalis.

[29]  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.

[30]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[32]  G. M. Peterson,et al.  Anterograde and retrograde axonal transport of Phaseolus vulgaris leucoagglutinin (PHA-L) from the globus pallidus to the striatum of the rat , 1988, Journal of Neuroscience Methods.

[33]  M. Filion,et al.  Pallidofugal projections to thalamus and midbrain: A quantitative antidromic activation study in monkeys and cats , 2004, Experimental Brain Research.

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

[35]  H. Fibiger,et al.  Demonstration of a pallidostriatal pathway by retrograde transport of HRP-labeled lectin , 1981, Brain Research.

[36]  Shiro Nakagawa,et al.  Topographical projections from the thalamus, subthalamic nucleus and pedunculopontine tegmental nucleus to the striatum in the Japanese monkey, Macaca fuscata , 1990, Brain Research.

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

[38]  H. Künzle Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study inMacaca fascicularis , 1975, Brain Research.

[39]  R. Elliott,et al.  Differential Response Patterns in the Striatum and Orbitofrontal Cortex to Financial Reward in Humans: A Parametric Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

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

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

[42]  W. Schultz,et al.  Influence of expectation of different rewards on behavior-related neuronal activity in the striatum. , 2001, Journal of neurophysiology.

[43]  C. Ranganath,et al.  Dorsolateral Prefrontal Cortex Promotes Long-Term Memory Formation through Its Role in Working Memory Organization , 2006, The Journal of Neuroscience.

[44]  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.

[45]  A. Dickinson,et al.  Prediction Error during Retrospective Revaluation of Causal Associations in Humans fMRI Evidence in Favor of an Associative Model of Learning , 2004, Neuron.

[46]  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.

[47]  Yu-Shin Ding,et al.  Behavioral / Systems / Cognitive Activation of Orbital and Medial Prefrontal Cortex by Methylphenidate in Cocaine-Addicted Subjects But Not in Controls : Relevance to Addiction , 2005 .

[48]  Martin Deschênes,et al.  The organization of corticothalamic projections: reciprocity versus parity , 1998, Brain Research Reviews.

[49]  L. Tremblay,et al.  The pallidosubthalamic projection: An anatomical substrate for nonmotor functions of the subthalamic nucleus in primates , 2005, Movement disorders : official journal of the Movement Disorder Society.

[50]  M. E. Anderson,et al.  An autoradiographic study of efferent connections of the globus pallidus in Macaca mulatta , 2004, Experimental Brain Research.

[51]  A. Parent,et al.  Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA‐L anterograde tracing method , 1990, The Journal of comparative neurology.

[52]  S. Haber,et al.  Organization of the output of the ventral striatopallidal system in the rat: Ventral pallidal efferents , 1993, Neuroscience.

[53]  M. Carpenter,et al.  Organization of pallidothalamic projections in the rhesus monkey , 1973, The Journal of comparative neurology.

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

[55]  J. Yelnik,et al.  Subthalamic neurons in primates: A quantitative and comparative analysis , 1979, Neuroscience.

[56]  E. Jones Chapter I - The thalamus of primates , 1998 .

[57]  K. Akert,et al.  Efferent connections of cortical, area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique , 1977, The Journal of comparative neurology.

[58]  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.

[59]  R. Elliott,et al.  Differential Neural Responses during Performance of Matching and Nonmatching to Sample Tasks at Two Delay Intervals , 1999, The Journal of Neuroscience.

[60]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[61]  A. Graybiel,et al.  Role of [corrected] nigrostriatal dopamine system in learning to perform sequential motor tasks in a predictive manner. , 1999, Journal of neurophysiology.

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

[63]  Philippe Mailly,et al.  Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: an anatomical substrate for cognition to action , 2007, The European journal of neuroscience.

[64]  R. Chipkin D2 receptor genes-the cause or consequence of substance abuse? , 1994, Trends in Neurosciences.

[65]  R. Wise Dopamine, learning and motivation , 2004, Nature Reviews Neuroscience.

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

[67]  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.

[68]  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.

[69]  O. Hikosaka,et al.  Differential Roles of the Frontal Cortex, Basal Ganglia, and Cerebellum in Visuomotor Sequence Learning , 1998, Neurobiology of Learning and Memory.

[70]  P. Somogyi,et al.  Projection of neostriatal spiny neurons to the substantia nigra. Application of a combined golgi-staining and horse-radish peroxidase transport procedure at both light and electron microscopic levels , 1979, Brain Research.

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

[72]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[73]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

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

[75]  Y. Smith,et al.  The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey , 1996, Neuroscience.

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

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

[78]  C. W. Ragsdale,et al.  A simple ordering of neocortical areas established by the compartmental organization of their striatal projections. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[81]  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.

[82]  J Tanji,et al.  Comparison of neuronal activity in the supplementary motor area and primary motor cortex. , 1996, Brain research. Cognitive brain research.

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

[84]  Jonathan D. Wallis,et al.  A Comparison of Abstract Rules in the Prefrontal Cortex, Premotor Cortex, Inferior Temporal Cortex, and Striatum , 2006, Journal of Cognitive Neuroscience.

[85]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

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

[89]  H. Kuypers,et al.  Differential laminar distribution of corticothalamic neurons projecting to the VL and the center median. An HRP study in the cynomolgus monkey , 1978, Brain Research.

[90]  Edward E. Smith,et al.  Working Memory: A View from Neuroimaging , 1997, Cognitive Psychology.

[91]  K. Hikosaka,et al.  Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. , 2000, Cerebral cortex.

[92]  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.

[93]  A. Parent,et al.  The subcortical afferents to caudate nucleus and putamen in primate: A fluorescence retrograde double labeling study , 1983, Neuroscience.

[94]  K. Akert,et al.  Projections of precentral and premotor cortex to the red nucleus and other midbrain areas in macaca fascicularis , 1979, Experimental Brain Research.

[95]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[96]  G. Paxinos,et al.  THE HUMAN NERVOUS SYSTEM , 1975 .

[97]  K. Berridge,et al.  What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? , 1998, Brain Research Reviews.

[98]  C. I. Connolly,et al.  Building neural representations of habits. , 1999, Science.

[99]  Robert M. Beckstead,et al.  A pallidostriatal projection in the cat and monkey , 1983, Brain Research Bulletin.

[100]  Masahiko Inase,et al.  Corticosubthalamic input zones from forelimb representations of the dorsal and ventral divisions of the premotor cortex in the macaque monkey: comparison with the input zones from the primary motor cortex and the supplementary motor area , 1997, Neuroscience Letters.

[101]  S. Carmichael,et al.  Networks related to the orbital and medial prefrontal cortex; a substrate for emotional behavior? , 1996, Progress in brain research.

[102]  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.

[103]  O. Hikosaka,et al.  Neural Correlates of Rewarded and Unrewarded Eye Movements in the Primate Caudate Nucleus , 2003, The Journal of Neuroscience.

[104]  S. Rauch,et al.  The Role of the Orbitofrontal Cortex in Anxiety Disorders , 2007, Annals of the New York Academy of Sciences.

[105]  P. Goldman-Rakic,et al.  Organization of the nigrothalamocortical system in the rhesus monkey , 1985, The Journal of comparative neurology.

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

[107]  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.

[108]  Trevor W. Robbins,et al.  High Impulsivity Predicts the Switch to Compulsive Cocaine-Taking , 2008, Science.

[109]  H. Groenewegen,et al.  The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei , 1994, Trends in Neurosciences.

[110]  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.

[111]  Michael A. Nader,et al.  The effects of cocaine: A shifting target over the course of addiction , 2007, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[112]  G. E. Alexander,et al.  Microstimulation of the primate neostriatum. II. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties. , 1985, Journal of neurophysiology.

[113]  A. Graybiel,et al.  Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. , 1994, Science.

[114]  P. Strick,et al.  Basal Ganglia ‘Loops’ with the Cerebral Cortex , 1995 .

[115]  J. Doyon,et al.  Role of the Striatum, Cerebellum, and Frontal Lobes in the Learning of a Visuomotor Sequence , 1997, Brain and Cognition.

[116]  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.

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

[118]  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.

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

[120]  J. Yelnik,et al.  Topographic distribution of the neurons of the central complex (centre médian-parafascicular complex) and of other thalamic neurons projecting to the striatum in macaques , 1991, Neuroscience.

[121]  M. Wiesendanger,et al.  The thalamic connections with medial area 6 (supplementary motor cortex) in the monkey (macaca fascicularis) , 2004, Experimental Brain Research.

[122]  Katsuyuki Sakai,et al.  The prefrontal cortex and working memory: physiology and brain imaging , 2004, Current Opinion in Neurobiology.

[123]  A. Parent,et al.  Anatomical aspects of information processing in primate basal ganglia , 1993, Trends in Neurosciences.

[124]  P. Goldman-Rakic,et al.  Differential Activation of the Caudate Nucleus in Primates Performing Spatial and Nonspatial Working Memory Tasks , 1997, The Journal of Neuroscience.

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

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

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

[128]  J. Bolam,et al.  Neurons projecting from the entopeduncular nucleus to the thalamus receive convergent synaptic inputs from the subthalamic nucleus and the neostriatum in the rat , 1994, Brain Research.

[129]  D. Coon The Human Nervous System 2nd ed , 1975 .

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

[131]  Nikolaus R. McFarland,et al.  Convergent Inputs from Thalamic Motor Nuclei and Frontal Cortical Areas to the Dorsal Striatum in the Primate , 2000, The Journal of Neuroscience.

[132]  M. Inase,et al.  Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[133]  Bruce Fischl,et al.  Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[134]  S. Haber,et al.  The Basal Ganglia , 2012 .

[135]  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.

[136]  M. Mishkin,et al.  Comparison of the effects of frontal and caudate lesions on delayed response and alternation in monkeys. , 1960, Journal of comparative and physiological psychology.

[137]  C. Gerfen,et al.  The frontal cortex-basal ganglia system in primates. , 1996, Critical reviews in neurobiology.

[138]  L. Parsons,et al.  Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. , 1999, The American journal of psychiatry.

[139]  H. Bergman,et al.  Information processing, dimensionality reduction and reinforcement learning in the basal ganglia , 2003, Progress in Neurobiology.

[140]  P. Strick,et al.  Cingulate Motor Areas , 1993 .

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

[142]  E. Ruppin,et al.  Reinforcement-Driven Dimensionality Reduction - A Model for Information Processing in the Basal Ganglia , 2000, Journal of basic and clinical physiology and pharmacology.

[143]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

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

[145]  H. Künzle,et al.  Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey , 1977, Experimental Brain Research.

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

[147]  P S Goldman-Rakic,et al.  Mediodorsal nucleus: Areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys , 1988, The Journal of comparative neurology.

[148]  A. Parent,et al.  Topography of the projection from the central complex of the thalamus to the sensorimotor striatal territory in monkeys , 1991, The Journal of comparative neurology.

[149]  Anders Björklund,et al.  The primate nervous system , 1997 .

[150]  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.

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

[152]  J. Fuster,et al.  Prefrontal neurons in networks of executive memory , 2000, Brain Research Bulletin.

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

[154]  P. Strick,et al.  Basal-ganglia 'projections' to the prefrontal cortex of the primate. , 2002, Cerebral cortex.

[155]  C. Seva,et al.  Growth-promoting effects of glycine-extended progastrin. , 1994, Science.

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

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

[158]  P. Somogyi,et al.  An approach to tracing neuron networks in the cerebral cortex and basal ganglia. Combination of golgi staining, retrograde transport of horseradish peroxidase and anterograde degeneration of synaptic boutons in the same material , 1979, Neuroscience.

[159]  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.

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

[161]  A. D. Smith,et al.  Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium‐size spiny neurons in the rat neostriatum , 1988, The Journal of comparative neurology.

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

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

[164]  P. Goldman-Rakic,et al.  The primate mediodorsal (MD) nucleus and its projection to the frontal lobe , 1985, The Journal of comparative neurology.

[165]  A. Parent,et al.  Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: A PHA‐L study of subcortical projections , 1992, The Journal of comparative neurology.

[166]  A. Flaherty,et al.  Input-output organization of the sensorimotor striatum in the squirrel monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[167]  O. Hikosaka,et al.  Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons. , 2002, Journal of neurophysiology.

[168]  Giuseppe Luppino,et al.  Thalamic input to mesial and superior area 6 in the macaque monkey , 1996, The Journal of comparative neurology.

[169]  S. Rauch,et al.  Recall of Fear Extinction in Humans Activates the Ventromedial Prefrontal Cortex and Hippocampus in Concert , 2007, Biological Psychiatry.

[170]  S. Haber,et al.  Ventral pallidostriatal pathway in the monkey: Evidence for modulation of basal ganglia circuits , 1996 .

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

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

[173]  M. Carpenter,et al.  Projections of the globus pallidus and adjacent structures: An autoradiographic study in the monkey , 1976, The Journal of comparative neurology.