A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP

According to the Hebb rule, the change in the strength of a synapse depends only on the local interaction of presynaptic and postsynaptic events. Studies at many types of synapses indicate that the early phase of long-term potentiation (LTP) has Hebbian properties. However, it is now clear that the Hebb rule does not account for late LTP; this requires an additional signal that is non-local. For novel information and motivational events such as rewards this signal at hippocampal CA1 synapses is mediated by the neuromodulator, dopamine. In this Review we discuss recent experimental findings that support the view that this 'neoHebbian' framework can account for memory behavior in a variety of learning situations.

[1]  F. Craik,et al.  Depth of processing and the retention of words , 1975 .

[2]  D. Kumaran,et al.  An Unexpected Sequence of Events: Mismatch Detection in the Human Hippocampus , 2006, PLoS biology.

[3]  W. Schultz,et al.  Responses of monkey dopamine neurons during learning of behavioral reactions. , 1992, Journal of neurophysiology.

[4]  Paolo Calabresi,et al.  Dopamine-mediated regulation of corticostriatal synaptic plasticity , 2007, Trends in Neurosciences.

[5]  S. Mizumori,et al.  Conjunctive encoding of movement and reward by ventral tegmental area neurons in the freely navigating rodent. , 2010, Behavioral neuroscience.

[6]  A. Grace,et al.  Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  U. Frey,et al.  Synaptic tagging and long-term potentiation , 1997, Nature.

[8]  M M Mesulam,et al.  Human reticular formation: Cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons , 1989, The Journal of comparative neurology.

[9]  J. Hodges,et al.  Spectrum of memory dysfunction in degenerative disease , 1996, Current opinion in neurology.

[10]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[11]  R. Dolan,et al.  Contextual Novelty Changes Reward Representations in the Striatum , 2010, The Journal of Neuroscience.

[12]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[13]  Michael X. Cohen,et al.  Intracranial EEG Correlates of Expectancy and Memory Formation in the Human Hippocampus and Nucleus Accumbens , 2010, Neuron.

[14]  R. Morris,et al.  Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory , 2010, Proceedings of the National Academy of Sciences.

[15]  G. Aghajanian,et al.  Antidromic identification of dopaminergic and other output neurons of the rat substantia nigra , 1978, Brain Research.

[16]  H. Heinze,et al.  Reward-related fMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation , 2005 .

[17]  D. Sagi,et al.  Dynamics of Memory Representations in Networks with Novelty-Facilitated Synaptic Plasticity , 2006, Neuron.

[18]  F. Bermúdez-Rattoni,et al.  Off‐line concomitant release of dopamine and glutamate involvement in taste memory consolidation , 2010, Journal of neurochemistry.

[19]  J. Lisman,et al.  D1/D5 Dopamine Receptor Activation Increases the Magnitude of Early Long-Term Potentiation at CA1 Hippocampal Synapses , 1996, The Journal of Neuroscience.

[20]  A. Grace,et al.  Aberrant striatal plasticity is specifically associated with dyskinesia following levodopa treatment , 2010, Movement disorders : official journal of the Movement Disorder Society.

[21]  A. Grace,et al.  Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning , 2002, Nature.

[22]  J. Lisman,et al.  Dopamine Selectively Inhibits the Direct Cortical Pathway to the CA1 Hippocampal Region , 1999, The Journal of Neuroscience.

[23]  V. Bolshakov,et al.  Emotional enhancement of memory: how norepinephrine enables synaptic plasticity , 2010, Molecular Brain.

[24]  J. O’Neill,et al.  Play it again: reactivation of waking experience and memory , 2010, Trends in Neurosciences.

[25]  G. Mogenson,et al.  Response of ventral pallidal neurons to amygdala stimulation and its modulation by dopamine projections to nucleus accumbens. , 1983, Journal of neurophysiology.

[26]  M. A. De Luca,et al.  Differential Expression of Motivational Stimulus Properties by Dopamine in Nucleus Accumbens Shell versus Core and Prefrontal Cortex , 2002, The Journal of Neuroscience.

[27]  H. Heinze,et al.  The Dopaminergic Midbrain Participates in Human Episodic Memory Formation: Evidence from Genetic Imaging , 2006, The Journal of Neuroscience.

[28]  R. Palmiter,et al.  Vesicular Glutamate Transport Promotes Dopamine Storage and Glutamate Corelease In Vivo , 2010, Neuron.

[29]  Susumu Tonegawa,et al.  The Dendritic Branch Is the Preferred Integrative Unit for Protein Synthesis-Dependent LTP , 2011, Neuron.

[30]  T. Robbins,et al.  Review Personality, Addiction, Dopamine: Insights from Parkinson's Disease Table 1. Possible Site of Striatal Dopamine Dysfunction Causing Different Motor and Cognitive Symptoms in Parkinson's Disease , 2022 .

[31]  S. MacDonald,et al.  Simulating Neurocognitive Aging: Effects of a Dopaminergic Antagonist on Brain Activity During Working Memory , 2010, Biological Psychiatry.

[32]  R. Morris,et al.  Making memories last: the synaptic tagging and capture hypothesis , 2010, Nature Reviews Neuroscience.

[33]  W. B. Smith,et al.  Dopaminergic Stimulation of Local Protein Synthesis Enhances Surface Expression of GluR1 and Synaptic Transmission in Hippocampal Neurons , 2005, Neuron.

[34]  A. Grace,et al.  Aversive Stimuli Alter Ventral Tegmental Area Dopamine Neuron Activity via a Common Action in the Ventral Hippocampus , 2011, The Journal of Neuroscience.

[35]  Ethan S. Bromberg-Martin,et al.  Dopamine in Motivational Control: Rewarding, Aversive, and Alerting , 2010, Neuron.

[36]  R. Morris,et al.  Dopamine and Memory: Modulation of the Persistence of Memory for Novel Hippocampal NMDA Receptor-Dependent Paired Associates , 2010, The Journal of Neuroscience.

[37]  W. Pan,et al.  Pedunculopontine Tegmental Nucleus Controls Conditioned Responses of Midbrain Dopamine Neurons in Behaving Rats , 2005, The Journal of Neuroscience.

[38]  E. Düzel,et al.  Personality Traits Are Differentially Associated with Patterns of Reward and Novelty Processing in the Human Substantia Nigra/Ventral Tegmental Area , 2009, Biological Psychiatry.

[39]  D. Shohamy,et al.  Integrating Memories in the Human Brain: Hippocampal-Midbrain Encoding of Overlapping Events , 2008, Neuron.

[40]  M. W. Brown,et al.  Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe , 1998, Neuropharmacology.

[41]  Robert M. Kessler,et al.  Midbrain Dopamine Receptor Availability Is Inversely Associated with Novelty-Seeking Traits in Humans , 2008, The Journal of Neuroscience.

[42]  R. Palmiter,et al.  Morphine reward in dopamine-deficient mice , 2005, Nature.

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

[44]  W. Nauta,et al.  Efferent connections of the substantia nigra and ventral tegmental area in the rat , 1979, Brain Research.

[45]  M. Frank,et al.  Neurogenetics and Pharmacology of Learning, Motivation, and Cognition , 2011, Neuropsychopharmacology.

[46]  J. Ihalainen,et al.  Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis , 1999, Neuroscience Letters.

[47]  Stefano Puglisi-Allegra,et al.  Repeated stressful experiences differently affect the time-dependent responses of the mesolimbic dopamine system to the stressor , 1993, Brain Research.

[48]  Michael E. Hasselmo,et al.  Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection , 2005, Brain Research Reviews.

[49]  J. Frey,et al.  'Synaptic tagging' and 'cross-tagging' and related associative reinforcement processes of functional plasticity as the cellular basis for memory formation. , 2008, Progress in brain research.

[50]  U. Frey,et al.  Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices , 1990, Brain Research.

[51]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[52]  A. Grace,et al.  The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[54]  E. Kandel,et al.  D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Brian J Eastwood,et al.  Dopamine D1/5 receptor modulation of firing rate and bidirectional theta burst firing in medial septal/vertical limb of diagonal band neurons in vivo. , 2006, Journal of neurophysiology.

[56]  A. Grace,et al.  Regulation of firing of dopaminergic neurons and control of goal-directed behaviors , 2007, Trends in Neurosciences.

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

[58]  M. Ungless,et al.  Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli , 2009, Proceedings of the National Academy of Sciences.

[59]  A. Grace,et al.  Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—3. Evidence for electrotonic coupling , 1983, Neuroscience.

[60]  Emrah Düzel,et al.  Behavioral specifications of reward-associated long-term memory enhancement in humans. , 2011, Learning & memory.

[61]  K. Christian,et al.  BDNF: A key regulator for protein synthesis-dependent LTP and long-term memory? , 2008, Neurobiology of Learning and Memory.

[62]  E. Shimizu,et al.  NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. , 2000, Science.

[63]  M. Min,et al.  Change in bi‐directional plasticity at CA1 synapses in hippocampal slices taken from 6‐hydroxydopamine‐treated rats: the role of endogenous norepinephrine , 2002, The European journal of neuroscience.

[64]  E. Ringelstein,et al.  Levodopa: Faster and better word learning in normal humans , 2004, Annals of neurology.

[65]  M. Guitart-Masip,et al.  NOvelty-related Motivation of Anticipation and exploration by Dopamine (NOMAD): Implications for healthy aging , 2010, Neuroscience & Biobehavioral Reviews.

[66]  R. Habib,et al.  Activation of midbrain structures by associative novelty and the formation of explicit memory in humans. , 2004, Learning & memory.

[67]  A. Cools,et al.  Distinct kinds of novelty processing differentially increase extracellular dopamine in different brain regions , 2006, The European journal of neuroscience.

[68]  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.

[69]  Hans-Jochen Heinze,et al.  Novel Scenes Improve Recollection and Recall of Words , 2008, Journal of Cognitive Neuroscience.

[70]  J. Bolam,et al.  Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat , 2008, Neuroscience.

[71]  E. Kandel,et al.  Increased Attention to Spatial Context Increases Both Place Field Stability and Spatial Memory , 2004, Neuron.

[72]  J. Wagner,et al.  Postsynaptic dopamine D3 receptor modulation of evoked IPSCs via GABAA receptor endocytosis in rat hippocampus , 2008, Hippocampus.

[73]  Anthony A Grace,et al.  The Hippocampus Modulates Dopamine Neuron Responsivity by Regulating the Intensity of Phasic Neuron Activation , 2006, Neuropsychopharmacology.

[74]  D. Moncada,et al.  Induction of Long-Term Memory by Exposure to Novelty Requires Protein Synthesis: Evidence for a Behavioral Tagging , 2007, The Journal of Neuroscience.

[75]  P. O’Donnell,et al.  Dopamine gating of forebrain neural ensembles , 2003, The European journal of neuroscience.

[76]  Nico Bunzeck,et al.  Contextual interaction between novelty and reward processing within the mesolimbic system , 2011, Human brain mapping.

[77]  R. Palmiter,et al.  Dopamine Is Necessary for Cue-Dependent Fear Conditioning , 2009, The Journal of Neuroscience.

[78]  W. Abraham,et al.  A double dissociation within the hippocampus of dopamine D1/D5 receptor and β-adrenergic receptor contributions to the persistence of long-term potentiation , 1999, Neuroscience.

[79]  I. Izquierdo,et al.  Dopamine Controls Persistence of Long-Term Memory Storage , 2009, Science.

[80]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[81]  Angus C Nairn,et al.  Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[82]  Mark G. Baxter,et al.  The Rostromedial Tegmental Nucleus (RMTg), a GABAergic Afferent to Midbrain Dopamine Neurons, Encodes Aversive Stimuli and Inhibits Motor Responses , 2009, Neuron.

[83]  A. Grace,et al.  Nigral dopamine neurons: intracellular recording and identification with L-dopa injection and histofluorescence. , 1980, Science.

[84]  T. Mäntylä,et al.  Rewarded remembering: dissociations between self-rated motivation and memory performance. , 2005, Scandinavian journal of psychology.

[85]  Frank Neugebauer,et al.  Modulation of extracellular monoamine transmitter concentrations in the hippocampus after weak and strong tetanization of the perforant path in freely moving rats , 2009, Brain Research.

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

[87]  P. Dayan,et al.  A common mechanism for adaptive scaling of reward and novelty , 2010, Human brain mapping.

[88]  Mehdi Khamassi,et al.  Coherent Theta Oscillations and Reorganization of Spike Timing in the Hippocampal- Prefrontal Network upon Learning , 2010, Neuron.

[89]  S. Sesack,et al.  Anatomical Substrates for Glutamate‐Dopamine Interactions , 2003 .

[90]  D. Shohamy,et al.  Dopamine and adaptive memory , 2010, Trends in Cognitive Sciences.

[91]  H. Eichenbaum,et al.  Towards a functional organization of the medial temporal lobe memory system: Role of the parahippocampal and medial entorhinal cortical areas , 2008, Hippocampus.

[92]  W. Schultz.  Multiple dopamine functions at different time courses. , 2007, Annual review of neuroscience.

[93]  J. Tsien,et al.  Convergent Processing of Both Positive and Negative Motivational Signals by the VTA Dopamine Neuronal Populations , 2011, PloS one.

[94]  B. Kolachana,et al.  Variation in dopamine genes influences responsivity of the human reward system , 2009, Proceedings of the National Academy of Sciences.

[95]  A. Grace,et al.  Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—1. Identification and characterization , 1983, Neuroscience.

[96]  G. Rebec.  Real-time assessments of dopamine function during behavior: single-unit recording, iontophoresis, and fast-scan cyclic voltammetry in awake, unrestrained rats. , 1998, Alcoholism, clinical and experimental research.

[97]  M. Krug,et al.  Dopamine D1‐deficient mutant mice do not express the late phase of hippocampal long‐term potentiation , 1997, Neuroreport.

[98]  J. Lisman,et al.  The molecular basis of CaMKII function in synaptic and behavioural memory , 2002, Nature Reviews Neuroscience.

[99]  K. Fuxe,et al.  EVIDENCE FOR THE EXISTENCE OF MONOAMINE-CONTAINING NEURONS IN THE CENTRAL NERVOUS SYSTEM. I. DEMONSTRATION OF MONOAMINES IN THE CELL BODIES OF BRAIN STEM NEURONS. , 1964, Acta physiologica Scandinavica. Supplementum.

[100]  R. Morris,et al.  Heterosynaptic co-activation of glutamatergic and dopaminergic afferents is required to induce persistent long-term potentiation , 2004, Neuropharmacology.

[101]  F. Ballarini,et al.  Behavioral tagging is a general mechanism of long-term memory formation , 2009, Proceedings of the National Academy of Sciences.

[102]  J. Lisman,et al.  The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory , 2005, Neuron.

[103]  C. Harley,et al.  Locus Ceruleus Activation Initiates Delayed Synaptic Potentiation of Perforant Path Input to the Dentate Gyrus in Awake Rats: A Novel β-Adrenergic- and Protein Synthesis-Dependent Mammalian Plasticity Mechanism , 2004, The Journal of Neuroscience.

[104]  Jeffrey D. Karpicke,et al.  The Critical Importance of Retrieval for Learning , 2008, Science.

[105]  T. Sacktor,et al.  Protein synthesis-dependent formation of protein kinase Mzeta in long- term potentiation , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[106]  A. Grace,et al.  Dopamine-Dependent Interactions between Limbic and Prefrontal Cortical Plasticity in the Nucleus Accumbens: Disruption by Cocaine Sensitization , 2005, Neuron.

[107]  P. Dayan,et al.  Behavioral/systems/cognitive Action Dominates Valence in Anticipatory Representations in the Human Striatum and Dopaminergic Midbrain , 2010 .

[108]  Dorothy Tse,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles , 2022 .

[109]  A. Grace,et al.  Limbic and cortical information processing in the nucleus accumbens , 2008, Trends in Neurosciences.

[110]  James L McGaugh,et al.  The consolidation of object and context recognition memory involve different regions of the temporal lobe. , 2008, Learning & memory.

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

[112]  Anthony A. Grace,et al.  Dopamine System Dysregulation by the Ventral Subiculum as the Common Pathophysiological Basis for Schizophrenia Psychosis, Psychostimulant Abuse, and Stress , 2010, Neurotoxicity Research.

[113]  H. Wigström,et al.  Postsynaptic control of hippocampal long-term potentiation. , 1986, Journal de physiologie.

[114]  W. Schultz,et al.  Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli , 1996, Nature.

[115]  M. Constantine‐Paton,et al.  Postsynaptic BDNF‐TrkB signaling in synapse maturation, plasticity, and disease , 2010, Developmental neurobiology.

[116]  M. Le Moal,et al.  The role of stress in drug self-administration. , 1998, Trends in pharmacological sciences.

[117]  E. Portiansky,et al.  Dopaminergic mesencephalic systems and behavioral performance in very old rats , 2008, Neuroscience.

[118]  J. Bolam,et al.  Activity of Neurochemically Heterogeneous Dopaminergic Neurons in the Substantia Nigra during Spontaneous and Driven Changes in Brain State , 2009, The Journal of Neuroscience.

[119]  R. Liao,et al.  Dopamine receptor antagonists impair place conditioning after acute stress in rats , 2010, Behavioural pharmacology.

[120]  H. Condé,et al.  The role of the pedunculopontine tegmental nucleus in relation to conditioned motor performance in the cat I. Context-dependent and reinforcement-related single unit activity , 1998, Experimental Brain Research.

[121]  K. Deisseroth,et al.  Phasic Firing in Dopaminergic Neurons Is Sufficient for Behavioral Conditioning , 2009, Science.

[122]  G. Ellis‐Davies,et al.  Structural basis of long-term potentiation in single dendritic spines , 2004, Nature.

[123]  Peter Dayan,et al.  Dopamine: generalization and bonuses , 2002, Neural Networks.

[124]  Richard G M Morris,et al.  Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory. , 2006, Learning & memory.

[125]  E. Kandel,et al.  Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. , 1993, Science.

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

[127]  Nicolas Schweighofer,et al.  Positive and negative modulation of word learning by reward anticipation , 2008, Human brain mapping.

[128]  C J CLEMEDSON,et al.  DYNAMIC RESPONSE OF CHEST WALL AND LUNG INJURIES IN RABBITS EXPOSED TO AIR SHOCK WAVES OF SHORT DURATION. , 1964, Acta physiologica Scandinavica. Supplementum.

[129]  Eduardo D. Martín,et al.  D1 but not D5 dopamine receptors are critical for LTP, spatial learning, and LTP-Induced arc and zif268 expression in the hippocampus. , 2008, Cerebral cortex.

[130]  José María Delgado-García,et al.  Associative Learning and CA3–CA1 Synaptic Plasticity Are Impaired in D1R Null, Drd1a−/− Mice and in Hippocampal siRNA Silenced Drd1a Mice , 2010, The Journal of Neuroscience.

[131]  L. Nyberg,et al.  Linking cognitive aging to alterations in dopamine neurotransmitter functioning: Recent data and future avenues , 2010, Neuroscience & Biobehavioral Reviews.

[132]  Raymond J. Dolan,et al.  Anticipation of novelty recruits reward system and hippocampus while promoting recollection , 2007, NeuroImage.

[133]  E. Tulving.  Memory and consciousness. , 1985 .

[134]  P. O’Donnell,et al.  Prefrontal cortical up states are synchronized with ventral tegmental area activity , 2004, Synapse.

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

[136]  R. Cools.  Dopaminergic modulation of cognitive function-implications for l-DOPA treatment in Parkinson's disease , 2006, Neuroscience & Biobehavioral Reviews.

[137]  R. Malinow,et al.  Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation , 1986, Nature.

[138]  S. Sesack,et al.  Anatomical substrates for glutamate-dopamine interactions: evidence for specificity of connections and extrasynaptic actions. , 2003, Annals of the New York Academy of Sciences.

[139]  T. Robinson,et al.  A selective role for dopamine in reward learning , 2010, Nature.

[140]  R. Palmiter,et al.  Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior , 2009, Proceedings of the National Academy of Sciences.

[141]  Hyejin Kang,et al.  Translational Control by MAPK Signaling in Long-Term Synaptic Plasticity and Memory , 2004, Cell.

[142]  Hans-Jochen Heinze,et al.  Mesolimbic novelty processing in older adults. , 2007, Cerebral cortex.

[143]  O. Hikosaka,et al.  Two types of dopamine neuron distinctly convey positive and negative motivational signals , 2009, Nature.

[144]  M. Kahana,et al.  Human Substantia Nigra Neurons Encode Unexpected Financial Rewards , 2009, Science.

[145]  A. Lees,et al.  Ageing and Parkinson's disease: substantia nigra regional selectivity. , 1991, Brain : a journal of neurology.

[146]  S. Sajikumar,et al.  Synergistic requirements for the induction of dopaminergic D1/D5-receptor-mediated LTP in hippocampal slices of rat CA1 in vitro , 2007, Neuropharmacology.

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