Chemistry of the adaptive mind

A failure to adapt to novel or changing environmental demands is a core feature of a wide variety of neuropsychiatric disorders as well as the normal states of stress and fatigue. We review the neurochemistry of cognitive control, which has been associated primarily with the prefrontal cortex. Many drugs affect the functioning of the prefrontal cortex, but the direction and extent of drug effects vary across individuals and tasks. Apparently paradoxical effects are often observed, where the same medication causes both cognitive enhancement as well as cognitive side effects. We review neurobiological research that is beginning to elucidate the nature of these contrasting effects and the factors underlying the large variability across individuals and behaviours. The work has considerable implications for the understanding of and treatment development for abnormalities such as Parkinson's disease, attention deficit hyperactivity disorder and drug addiction.

[1]  T. Robbins,et al.  A componential analysis of task-switching deficits associated with lesions of left and right frontal cortex. , 2004, Brain : a journal of neurology.

[2]  Paul M. Grasby,et al.  Systemic sulpiride modulates striatal blood flow: relationships to spatial working memory and planning , 2003, NeuroImage.

[3]  T. Robbins,et al.  Differential effects of 6-OHDA lesions of the frontal cortex and caudate nucleus on the ability to acquire an attentional set. , 2001, Cerebral cortex.

[4]  N. Kurzina,et al.  The effects of local application of D2 selective dopaminergic drugs into the medial prefrontal cortex of rats in a delayed spatial choice task , 2000, Behavioural Brain Research.

[5]  T. Robbins,et al.  “Paradoxical” effects of psychomotor stimulant drugs in hyperactive children from the standpoint of behavioural pharmacology , 1979, Neuropharmacology.

[6]  R. Knight,et al.  Human prefrontal lesions increase distractibility to irrelevant sensory inputs , 1995, Neuroreport.

[7]  J. Callicott,et al.  Neurophysiological correlates of age-related changes in human motor function , 2002, Neurology.

[8]  A. Diamond,et al.  Genetic and neurochemical modulation of prefrontal cognitive functions in children. , 2004, The American journal of psychiatry.

[9]  C. Marsden,et al.  l-Dopa withdrawal in Parkinson's disease selectively impairs cognitive performance in tests sensitive to frontal lobe dysfunction , 2005, Psychopharmacology.

[10]  T. Goldberg,et al.  Dopaminergic modulation of cortical function in patients with Parkinson's disease , 2002, Annals of neurology.

[11]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[12]  T. Robbins,et al.  Dopaminergic modulation of high-level cognition in Parkinson's disease: the role of the prefrontal cortex revealed by PET. , 2002, Brain : a journal of neurology.

[13]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

[14]  J. Wilder Paradoxic reactions to treatment. , 1957, New York state journal of medicine.

[15]  CR Yang,et al.  Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  B. Dubois,et al.  Procedural learning and striatofrontal dysfunction in Parkinson's disease , 2002, Movement disorders : official journal of the Movement Disorder Society.

[17]  M. Farah,et al.  Ventromedial frontal cortex mediates affective shifting in humans: evidence from a reversal learning paradigm. , 2003, Brain : a journal of neurology.

[18]  T. Robbins,et al.  The effects of intradimensional and extradimensional shifts on visual discrimination learning in humans and non-human primates , 1988, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[19]  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.

[20]  JaneR . Taylor,et al.  Supranormal Stimulation of D1 Dopamine Receptors in the Rodent Prefrontal Cortex Impairs Spatial Working Memory Performance , 1997, The Journal of Neuroscience.

[21]  D. Durstewitz,et al.  Bidirectional Dopamine Modulation of GABAergic Inhibition in Prefrontal Cortical Pyramidal Neurons , 2001, The Journal of Neuroscience.

[22]  T. Sejnowski,et al.  Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Robert M Bilder,et al.  Catechol O-methyltransferase Val158Met polymorphism in schizophrenia: differential effects of Val and Met alleles on cognitive stability and flexibility. , 2004, The American journal of psychiatry.

[24]  T. Robbins,et al.  Dissociating executive mechanisms of task control following frontal lobe damage and Parkinson's disease. , 1998, Brain : a journal of neurology.

[25]  P. Dews Studies on behavior. IV. Stimulant actions of methamphetamine. , 1958, The Journal of pharmacology and experimental therapeutics.

[26]  A C Roberts,et al.  6-Hydroxydopamine lesions of the prefrontal cortex in monkeys enhance performance on an analog of the Wisconsin Card Sort Test: possible interactions with subcortical dopamine , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  S. Kish,et al.  Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. , 1988, The New England journal of medicine.

[28]  Mitul A Mehta,et al.  Methylphenidate improves working memory and set-shifting in AD/HD: relationships to baseline memory capacity. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[29]  P. Goldman-Rakic,et al.  Modulation of memory fields by dopamine Dl receptors in prefrontal cortex , 1995, Nature.

[30]  Jonathan D. Cohen,et al.  Computational perspectives on dopamine function in prefrontal cortex , 2002, Current Opinion in Neurobiology.

[31]  R. Yerkes,et al.  The relation of strength of stimulus to rapidity of habit‐formation , 1908 .

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

[33]  T. Robbins,et al.  l-Dopa medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson’s disease , 2003, Neuropsychologia.

[34]  J. Palacios,et al.  Dopamine receptors in human brain: Autoradiographic distribution of D2 sites , 1989, Neuroscience.

[35]  H. E. Rosvold,et al.  Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. , 1979, Science.

[36]  T. Robbins,et al.  Impaired set-shifting and dissociable effects on tests of spatial working memory following the dopamine D2 receptor antagonist sulpiride in human volunteers , 2004, Psychopharmacology.

[37]  S. Floresco,et al.  Magnitude of Dopamine Release in Medial Prefrontal Cortex Predicts Accuracy of Memory on a Delayed Response Task , 2004, The Journal of Neuroscience.

[38]  A. Arnsten Catecholamine modulation of prefrontal cortical cognitive function , 1998, Trends in Cognitive Sciences.

[39]  H. E. Rosvold,et al.  Behavioral effects of selective ablation of the caudate nucleus. , 1967, Journal of comparative and physiological psychology.

[40]  Martin H. Teicher,et al.  Rate dependency revisited: understanding the effects of methylphenidate in children with attention deficit hyperactivity disorder. , 2003, Journal of child and adolescent psychopharmacology.

[41]  R. Depue,et al.  Facilitation of Working Memory in Humans by a D2 Dopamine Receptor Agonist , 1992, Journal of Cognitive Neuroscience.

[42]  S. Foote,et al.  Extrathalamic modulation of cortical function. , 1987, Annual review of neuroscience.

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

[44]  T. Robbins,et al.  Contrasting mechanisms of impaired attentional set-shifting in patients with frontal lobe damage or Parkinson's disease. , 1993, Brain : a journal of neurology.

[45]  C. Carter,et al.  Effect of lesion of cortical dopamine terminals on subcortical dopamine receptors in rats , 1980, Nature.

[46]  Y. Burnod,et al.  A Model of Prefrontal Cortex Dopaminergic Modulation during the Delayed Alternation Task , 2002, Journal of Cognitive Neuroscience.

[47]  M. Farah,et al.  Effects of bromocriptine on human subjects depend on working memory capacity , 1997, Neuroreport.

[48]  Giuseppe Esposito,et al.  Dextroamphetamine Enhances “Neural Network-Specific” Physiological Signals: A Positron-Emission Tomography rCBF Study , 1996, The Journal of Neuroscience.

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

[50]  H. S. Koelega Stimulant drugs and vigilance performance: a review , 2005, Psychopharmacology.

[51]  A. C. Roberts,et al.  Perseveration and Strategy in a Novel Spatial Self-Ordered Sequencing Task for Nonhuman Primates: Effects of Excitotoxic Lesions and Dopamine Depletions of the Prefrontal Cortex , 1998, Journal of Cognitive Neuroscience.

[52]  J. Wilder Recent developments in the law of initial values. , 1962, Experimental medicine and surgery.

[53]  S. Pollmann,et al.  D1- Versus D2-Receptor Modulation of Visuospatial Working Memory in Humans , 1998, The Journal of Neuroscience.

[54]  Trevor W. Robbins,et al.  Enhanced and Impaired Attentional Performance After Infusion of D1 Dopaminergic Receptor Agents into Rat Prefrontal Cortex , 2000, The Journal of Neuroscience.

[55]  M S Buchsbaum,et al.  Dextroamphetamine. Its cognitive and behavioral effects in normal and hyperactive boys and normal men. , 1980, Archives of general psychiatry.

[56]  M. D’Esposito,et al.  Isolating the neural mechanisms of age-related changes in human working memory , 2000, Nature Neuroscience.

[57]  V. Brown,et al.  Mechanisms underlying attentional set-shifting inParkinsons disease , 1999, Neuropsychologia.

[58]  S. Floresco,et al.  Delay-dependent modulation of memory retrieval by infusion of a dopamine D1 agonist into the rat medial prefrontal cortex. , 2001, Behavioral neuroscience.

[59]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[60]  T. Robbins,et al.  Probabilistic learning and reversal deficits in patients with Parkinson’s disease or frontal or temporal lobe lesions: possible adverse effects of dopaminergic medication , 2000, Neuropsychologia.

[61]  J D Cohen,et al.  A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. , 1990, Science.

[62]  T. Sawaguchi,et al.  Effects of dopamine antagonists on neuronal activity related to a delayed response task in monkey prefrontal cortex. , 1990, Journal of neurophysiology.

[63]  Adrian M. Owen,et al.  Methylphenidate Enhances Working Memory by Modulating Discrete Frontal and Parietal Lobe Regions in the Human Brain , 2000, The Journal of Neuroscience.

[64]  J. Fuster Prefrontal Cortex , 2018 .

[65]  Douglas W. Jones,et al.  The effect of amphetamine on regional cerebral blood flow during cognitive activation in schizophrenia , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  M. Gluck,et al.  Role of the basal ganglia in category learning: how do patients with Parkinson's disease learn? , 2004, Behavioral neuroscience.

[67]  D. Durstewitz,et al.  A Neurocomputational Theory of the Dopaminergic Modulation of Working Memory Functions , 1999, The Journal of Neuroscience.

[68]  Jonathan D. Cohen,et al.  Role of locus coeruleus in attention and behavioral flexibility , 1999, Biological Psychiatry.

[69]  M. Egan,et al.  Catechol O-methyltransferase val158-met genotype and individual variation in the brain response to amphetamine , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[70]  Sharon K. McDowell,et al.  Differential effect of a dopaminergic agonist on prefrontal function in traumatic brain injury patients. , 1998, Brain : a journal of neurology.

[71]  T. Robbins,et al.  Chemical neuromodulation of frontal-executive functions in humans and other animals , 2000, Experimental Brain Research.

[72]  C. Marsden,et al.  'Frontal' cognitive function in patients with Parkinson's disease 'on' and 'off' levodopa. , 1988, Brain : a journal of neurology.

[73]  T. Robbins,et al.  Enhanced or impaired cognitive function in Parkinson's disease as a function of dopaminergic medication and task demands. , 2001, Cerebral cortex.

[74]  T. Robbins,et al.  Defining the Neural Mechanisms of Probabilistic Reversal Learning Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[75]  P. Maruff,et al.  Executive function and attention deficit hyperactivity disorder: stimulant medication and better executive function performance in children , 1999, Psychological Medicine.

[76]  T. Robbins,et al.  Dissociation in prefrontal cortex of affective and attentional shifts , 1996, Nature.

[77]  M. Mishkin,et al.  Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity , 1970, Experimental Brain Research.

[78]  John R. Anderson,et al.  The role of prefrontal cortex and posterior parietal cortex in task switching. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[79]  J. Glowinski,et al.  Selective activation of the mesocortical DA system by stress , 1976, Nature.

[80]  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.

[81]  R. Elliott,et al.  Effects of methylphenidate on spatial working memory and planning in healthy young adults , 1997, Psychopharmacology.