Dopamine modulation of emotional processing in cortical and subcortical neural circuits: evidence for a final common pathway in schizophrenia?

The neural regulation of emotional perception, learning, and memory is essential for normal behavioral and cognitive functioning. Many of the symptoms displayed by individuals with schizophrenia may arise from fundamental disturbances in the ability to accurately process emotionally salient sensory information. The neurotransmitter dopamine (DA) and its ability to modulate neural regions involved in emotional learning, perception, and memory formation has received considerable research attention as a potential final common pathway to account for the aberrant emotional regulation and psychosis present in the schizophrenic syndrome. Evidence from both human neuroimaging studies and animal-based research using neurodevelopmental, behavioral, and electrophysiological techniques have implicated the mesocorticolimbic DA circuit as a crucial system for the encoding and expression of emotionally salient learning and memory formation. While many theories have examined the cortical-subcortical interactions between prefrontal cortical regions and subcortical DA substrates, many questions remain as to how DA may control emotional perception and learning and how disturbances linked to DA abnormalities may underlie the disturbed emotional processing in schizophrenia. Beyond the mesolimbic DA system, increasing evidence points to the amygdala-prefrontal cortical circuit as an important processor of emotionally salient information and how neurodevelopmental perturbances within this circuitry may lead to dysregulation of DAergic modulation of emotional processing and learning along this cortical-subcortical emotional processing circuit.

[1]  Alexandra Horowitz,et al.  Smelling more or less: Investigating the olfactory experience of the domestic dog , 2013 .

[2]  P. Fletcher,et al.  A Sensitizing Regimen of Amphetamine Impairs Visual Attention in the 5-Choice Serial Reaction Time Test: Reversal by a D1 Receptor Agonist Injected into the Medial Prefrontal Cortex , 2007, Neuropsychopharmacology.

[3]  Christer Halldin,et al.  Dopamine D2 receptor binding in drug-naïve patients with schizophrenia examined with raclopride-C11 and positron emission tomography , 2006, Psychiatry Research: Neuroimaging.

[4]  Miriam C. Tepper Mind, Brain, and Schizophrenia , 2006 .

[5]  A. Grace,et al.  Cannabinoids Potentiate Emotional Learning Plasticity in Neurons of the Medial Prefrontal Cortex through Basolateral Amygdala Inputs , 2006, The Journal of Neuroscience.

[6]  A. Grace,et al.  The roles of cannabinoid and dopamine receptor systems in neural emotional learning circuits: implications for schizophrenia and addiction , 2006, Cellular and Molecular Life Sciences CMLS.

[7]  Hidehiko Takahashi,et al.  The Role of Extrastriatal Dopamine D2 Receptors in Schizophrenia , 2006, Biological Psychiatry.

[8]  Joseph E LeDoux,et al.  Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior , 2005, Neuron.

[9]  C. Fahim,et al.  Brain activity during emotionally negative pictures in schizophrenia with and without flat affect: An fMRI study , 2005, Psychiatry Research: Neuroimaging.

[10]  A. Grace,et al.  Prenatal Disruption of Neocortical Development Alters Prefrontal Cortical Neuron Responses to Dopamine in Adult Rats , 2005, Neuropsychopharmacology.

[11]  Anthony A Grace,et al.  A Subpopulation of Neurons in the Medial Prefrontal Cortex Encodes Emotional Learning with Burst and Frequency Codes through a Dopamine D4 Receptor-Dependent Basolateral Amygdala Input , 2005, The Journal of Neuroscience.

[12]  A. Grace,et al.  Dopamine modulates excitability of basolateral amygdala neurons in vitro. , 2005, Journal of neurophysiology.

[13]  J. Feldon,et al.  Mesolimbic dopaminergic pathways in fear conditioning , 2004, Progress in Neurobiology.

[14]  N. Volkow,et al.  Drug addiction: the neurobiology of behaviour gone awry , 2004, Nature Reviews Neuroscience.

[15]  D. Treit,et al.  Selective antagonism of medial prefrontal cortex D4 receptors decreases fear‐related behaviour in rats , 2004, The European journal of neuroscience.

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

[17]  N. Rajakumar,et al.  Altered neurotrophin receptor function in the developing prefrontal cortex leads to adult-onset dopaminergic hyperresponsivity and impaired prepulse inhibition of acoustic startle , 2004, Biological Psychiatry.

[18]  G. Quirk,et al.  Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. , 2004, Behavioral neuroscience.

[19]  Leanne M Williams,et al.  Dysregulation of arousal and amygdala-prefrontal systems in paranoid schizophrenia. , 2004, The American journal of psychiatry.

[20]  S. Henriksen,et al.  Opiate state controls bi-directional reward signaling via GABAA receptors in the ventral tegmental area , 2004, Nature Neuroscience.

[21]  A. Grace,et al.  The Prefrontal Cortex Regulates Lateral Amygdala Neuronal Plasticity and Responses to Previously Conditioned Stimuli , 2003, The Journal of Neuroscience.

[22]  Christer Halldin,et al.  Decreased thalamic D2/D3 receptor binding in drug-naive patients with schizophrenia: a PET study with [11C]FLB 457. , 2003, The international journal of neuropsychopharmacology.

[23]  S. Kapur,et al.  Half a century of antipsychotics and still a central role for dopamine D2 receptors , 2003, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[24]  S. Paradiso,et al.  Emotions in unmedicated patients with schizophrenia during evaluation with positron emission tomography. , 2003, The American journal of psychiatry.

[25]  P. Goldman-Rakic,et al.  Amphetamine sensitization of hallucinatory-like behaviors is dependent on prefrontal cortex in nonhuman primates , 2003, Biological Psychiatry.

[26]  Y. Humeau,et al.  Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition , 2003, Nature Neuroscience.

[27]  Anthony A Grace,et al.  Gating of Hippocampal-Evoked Activity in Prefrontal Cortical Neurons by Inputs from the Mediodorsal Thalamus and Ventral Tegmental Area , 2003, The Journal of Neuroscience.

[28]  G. Quirk,et al.  Neurons in medial prefrontal cortex signal memory for fear extinction , 2002, Nature.

[29]  B. Hyland,et al.  Firing modes of midbrain dopamine cells in the freely moving rat , 2002, Neuroscience.

[30]  Rita Z. Goldstein,et al.  Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. , 2002, The American journal of psychiatry.

[31]  D. Weinberger,et al.  Neonatal hippocampal damage alters electrophysiological properties of prefrontal cortical neurons in adult rats. , 2002, Cerebral cortex.

[32]  J. Holzer Frontal-Subcortical Circuits in Psychiatric and Neurological Disorders , 2002 .

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

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

[35]  K. Nader,et al.  Motivational state determines the functional role of the mesolimbic dopamine system in the mediation of opiate reward processes , 2002, Behavioural Brain Research.

[36]  Shigeru Watanabe,et al.  Enhancement of delayed release of dopamine in the amygdala induced by conditioned fear stress in methamphetamine-sensitized rats. , 2002, European journal of pharmacology.

[37]  Anthony A Grace,et al.  Cellular Mechanisms of Infralimbic and Prelimbic Prefrontal Cortical Inhibition and Dopaminergic Modulation of Basolateral Amygdala Neurons In Vivo , 2002, The Journal of Neuroscience.

[38]  H. Breiter,et al.  Reward Circuitry Activation by Noxious Thermal Stimuli , 2001, Neuron.

[39]  E. Gordon,et al.  Arousal Dissociates Amygdala and Hippocampal Fear Responses: Evidence from Simultaneous fMRI and Skin Conductance Recording , 2001, NeuroImage.

[40]  R. Straub,et al.  Effect of COMT Val108/158 Met genotype on frontal lobe function and risk for schizophrenia , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[41]  P. Pattison,et al.  Facial affect and affective prosody recognition in first-episode schizophrenia , 2001, Schizophrenia Research.

[42]  Peter G. Morris,et al.  The functional anatomy of auditory hallucinations in schizophrenia , 2000, Psychiatry Research: Neuroimaging.

[43]  R. Murray,et al.  Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. , 2000, Archives of general psychiatry.

[44]  K. Berridge,et al.  The psychology and neurobiology of addiction: an incentive-sensitization view. , 2000, Addiction.

[45]  J. Horvitz Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events , 2000, Neuroscience.

[46]  Michel Baudry,et al.  The amygdala modulates prefrontal cortex activity relative to conditioned fear , 1999, Nature.

[47]  J S Fowler,et al.  Regional brain metabolic activation during craving elicited by recall of previous drug experiences. , 1999, Life sciences.

[48]  R. Wise Drug-activation of brain reward pathways. , 1998, Drug and alcohol dependence.

[49]  Jeffrey A Lieberman,et al.  Neurochemical Sensitization in the Pathophysiology of Schizophrenia: Deficits and Dysfunction in Neuronal Regulation and Plasticity , 1997, Neuropsychopharmacology.

[50]  J. Joyce,et al.  Disrupted pattern of D2 dopamine receptors in the temporal lobe in schizophrenia. A postmortem study. , 1997, Archives of general psychiatry.

[51]  Mathias Schreckenberger,et al.  Correlation of positive symptoms exclusively to hyperperfusion or hypoperfusion of cerebral cortex in never-treated schizophrenics , 1997, The Lancet.

[52]  Edward Allan,et al.  Differential relationships between positive and negative symptoms and neuropsychological deficits in schizophrenia , 1997, Schizophrenia Research.

[53]  W. Schultz Dopamine neurons and their role in reward mechanisms , 1997, Current Opinion in Neurobiology.

[54]  A. Malhotra,et al.  Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[55]  M. Feenstra,et al.  Rapid sampling of extracellular dopamine in the rat prefrontal cortex during food consumption, handling and exposure to novelty , 1996, Brain Research.

[56]  R. Adolphs,et al.  Cortical Systems for the Recognition of Emotion in Facial Expressions , 1996, The Journal of Neuroscience.

[57]  J. Krystal,et al.  Single photon emission computerized tomography imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Karl J. Friston,et al.  Dopaminergic modulation of impaired cognitive activation in the anterior cingulate cortex in schizophrenia , 1995, Nature.

[59]  Richard S. J. Frackowiak,et al.  A functional neuroanatomy of hallucinations in schizophrenia , 1995, Nature.

[60]  A. Grace,et al.  The tonic/phasic model of dopamine system regulation: its relevance for understanding how stimulant abuse can alter basal ganglia function. , 1995, Drug and alcohol dependence.

[61]  J. Yeomans Role of Tegmental Cholinergic Neurons in Dopaminergic Activation, Antimuscarinic Psychosis and Schizophrenia , 1995, Neuropsychopharmacology.

[62]  R. Murray,et al.  Increased blood flow in Broca's area during auditory hallucinations in schizophrenia , 1993, The Lancet.

[63]  D. Weinberger,et al.  Postpubertal Emergence of Hyperresponsiveness to Stress and to Amphetamine after Neonatal Excitotoxic Hippocampal Damage: A Potential Animal Model of Schizophrenia , 1993, Neuropsychopharmacology.

[64]  S. Sesack,et al.  Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area , 1992, The Journal of comparative neurology.

[65]  D. Javitt,et al.  Recent advances in the phencyclidine model of schizophrenia. , 1991, The American journal of psychiatry.

[66]  T. Robinson,et al.  Enduring changes in brain and behavior produced by chronic amphetamine administration: A review and evaluation of animal models of amphetamine psychosis , 1986, Brain Research Reviews.

[67]  Barry L. Jacobs,et al.  Single unit response of noradrenergic, serotonergic and dopaminergic neurons in freely moving cats to simple sensory stimuli , 1986, Brain Research.

[68]  G. Reynolds Increased concentrations and lateral asymmetry of amygdala dopamine in schizophrenia , 1983, Nature.

[69]  M. Tohyama,et al.  Leucine-enkephalin-containing neuron system in the facial nucleus of the rat with special reference to its fine structure , 1983, Brain Research.

[70]  J. D. Miller,et al.  Mesencephalic dopaminergic unit activity in the behaviorally conditioned rat. , 1981, Life sciences.

[71]  Hervé Simon,et al.  Efferents and afferents of the ventral tegmental-A10 region studied after local injection of [3H]leucine and horseradish peroxidase , 1979, Brain Research.

[72]  D. Janowsky,et al.  Methylphenidate, dextroamphetamine, and levamfetamine. Effects on schizophrenic symptoms. , 1976, Archives of general psychiatry.

[73]  B. Angrist,et al.  The phenomenology of experimentally induced amphetamine psychosis--preliminary observations. , 1970, Biological psychiatry.

[74]  G. Rosenbaum,et al.  Model psychoses and schizophrenia. , 1962, The American journal of psychiatry.

[75]  J. Lieberman,et al.  Provocative tests with psychostimulant drugs in schizophrenia , 2004, Psychopharmacology.

[76]  J. Rotrosen,et al.  Responses to apomorphine, amphetamine, and neuroleptics in schizophrenic subjects , 2004, Psychopharmacology.

[77]  R. Wise Dopamine and food reward: back to the elements. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

[78]  D. Kooy,et al.  The neurobiology of nicotine addiction: bridging the gap from molecules to behaviour , 2004, Nature Reviews Neuroscience.

[79]  J. Cummings,et al.  Frontal-subcortical circuits in psychiatric and neurological disorders , 2001 .

[80]  R. Wise,et al.  Interactions between medial prefrontal cortex and meso-limbic components of brain reward circuitry. , 2000, Progress in brain research.

[81]  M. Feenstra,et al.  Dopamine and noradrenaline release in the prefrontal cortex in relation to unconditioned and conditioned stress and reward. , 2000, Progress in brain research.

[82]  John Patrick Aggleton,et al.  The Amygdala : a functional analysis , 2000 .

[83]  Joseph E LeDoux,et al.  The dopaminergic modulation of fear: quinpirole impairs the recall of emotional memories in rats. , 1999, Behavioral neuroscience.

[84]  S. R. Nash,et al.  Dopamine receptors: from structure to function. , 1998, Physiological reviews.

[85]  R. Roth,et al.  Dysregulation of mesoprefrontal dopamine neurons induced by acute and repeated phencyclidine administration in the nonhuman primate: implications for schizophrenia. , 1998, Advances in pharmacology.

[86]  M. Mandal,et al.  Facial expressions of emotions and schizophrenia: a review. , 1998, Schizophrenia bulletin.

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

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

[89]  M. Le Moal,et al.  Mesocorticolimbic dopaminergic network: functional and regulatory roles. , 1991, Physiological reviews.

[90]  K. Mueser,et al.  Deficits in facial-affect recognition and schizophrenia. , 1988, Schizophrenia bulletin.

[91]  P. Seeman,et al.  Dopamine receptors and the dopamine hypothesis of schizophrenia , 1987, Synapse.

[92]  S. Snyder,et al.  The dopamine hypothesis of schizophrenia: focus on the dopamine receptor. , 1976, The American journal of psychiatry.

[93]  S. Gershon,et al.  Amphetamine psychosis: behavioral and biochemical aspects. , 1974, Journal of psychiatric research.