The emerging role of norepinephrine in cognitive dysfunctions of Parkinson's disease

Parkinson's disease (PD) is the second most common neurodegenerative disorder, affecting 1% of the population over age 60. In those patients cognitive dysfunction is a persistent issue that impairs quality of life and productivity. Neuropathological studies demonstrate significant damage in brain regions outside the nigral dopamine (DA) system, including early degeneration of locus coeruleus norepinephrine (LC-NE) neurons, yet discussion of PD and treatment focus has remained dopaminergic-based. Motor symptoms benefit from DA replacement for many years, but other symptoms including several cognitive deficits continue unabated. Recent interest in non-DA substrates of PD highlights early involvement of LC-NE neurons and provides evidence for a prodromal phase, with cognitive disturbance, even in sporadic PD. We outline insights from basic research in LC-NE function to clinical and pathological evidence highlighting a role for NE in PD cognitive dysfunction. We propose that loss of LC-NE regulation, particularly in higher cortical regions, critically underlies certain cognitive dysfunctions in early PD. As a major unmet need for patients, research and use of NE drugs in PD may provide significant benefits for cognitive processing.

[1]  Elmer S. West From the U. S. A. , 1965 .

[2]  F. Biagioni,et al.  Abnormal involuntary movements (AIMs) following pulsatile dopaminergic stimulation: Severe deterioration and morphological correlates following the loss of locus coeruleus neurons , 2007, Brain Research.

[3]  T. Robbins,et al.  Functions of frontostriatal systems in cognition: Comparative neuropsychopharmacological studies in rats, monkeys and humans , 2006, Biological Psychology.

[4]  J. Jankovic Atomoxetine for freezing of gait in Parkinson disease , 2009, Journal of the Neurological Sciences.

[5]  Hansjürgen Bratzke,et al.  Stages in the development of Parkinson’s disease-related pathology , 2004, Cell and Tissue Research.

[6]  D. Weinshenker,et al.  Functional consequences of locus coeruleus degeneration in Alzheimer's disease. , 2008, Current Alzheimer research.

[7]  H. Eichenbaum,et al.  Noradrenergic, but not cholinergic, deafferentation of prefrontal cortex impairs attentional set-shifting , 2008, Neuroscience.

[8]  V. Chan‐Palay,et al.  Alterations in catecholamine neurons of the locus coeruleus in senile dementia of the Alzheimer type and in Parkinson's disease with and without dementia and depression , 1989, The Journal of comparative neurology.

[9]  Angie A. Kehagia,et al.  Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson's disease , 2010, The Lancet Neurology.

[10]  S. Sara,et al.  Reward expectation, orientation of attention and locus coeruleus‐medial frontal cortex interplay during learning , 2004, The European journal of neuroscience.

[11]  P. Calabresi,et al.  A convergent model for cognitive dysfunctions in Parkinson's disease: the critical dopamine–acetylcholine synaptic balance , 2006, The Lancet Neurology.

[12]  C. Waters,et al.  Current strategies in the treatment of Parkinson’s disease and a personalized approach to management , 2009, Expert review of neurotherapeutics.

[13]  V. Brown,et al.  Medial Frontal Cortex Mediates Perceptual Attentional Set Shifting in the Rat , 2000, The Journal of Neuroscience.

[14]  E. Wolters Non-motor extranigral signs and symptoms in Parkinson's disease. , 2009, Parkinsonism & related disorders.

[15]  Angie A. Kehagia,et al.  Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation , 2010, Current Opinion in Neurobiology.

[16]  T. Robbins,et al.  Lesions of the dorsal noradrenergic bundle impair attentional set‐shifting in the rat , 2007, The European journal of neuroscience.

[17]  I. McKeith,et al.  SIC Task Force appraisal of clinical diagnostic criteria for parkinsonian disorders , 2003, Movement disorders : official journal of the Movement Disorder Society.

[18]  H. Braak,et al.  A timeline for Parkinson's disease. , 2010, Parkinsonism & related disorders.

[19]  H. Braak,et al.  Staging of brain pathology related to sporadic Parkinson’s disease , 2003, Neurobiology of Aging.

[20]  Wade K. Smith,et al.  Disease‐specific patterns of locus coeruleus cell loss , 1992, Annals of neurology.

[21]  S. Floresco,et al.  Neural circuits subserving behavioral flexibility and their relevance to schizophrenia , 2009, Behavioural Brain Research.

[22]  C. Hawkes The prodromal phase of sporadic Parkinson's disease: Does it exist and if so how long is it? , 2008, Movement disorders : official journal of the Movement Disorder Society.

[23]  B. Jones Activity, modulation and role of basal forebrain cholinergic neurons innervating the cerebral cortex. , 2004, Progress in brain research.

[24]  A. C. Roberts,et al.  Impaired extra-dimensional shift performance in medicated and unmedicated Parkinson's disease: Evidence for a specific attentional dysfunction , 1989, Neuropsychologia.

[25]  F. Kirchhoff,et al.  Locus ceruleus controls Alzheimer's disease pathology by modulating microglial functions through norepinephrine , 2010, Proceedings of the National Academy of Sciences.

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

[27]  W. Schmidt,et al.  Potentiation of parkinsonian symptoms by depletion of locus coeruleus noradrenaline in 6‐hydroxydopamine‐induced partial degeneration of substantia nigra in rats , 2003, The European journal of neuroscience.

[28]  Dag Aarsland,et al.  Use of drugs with anticholinergic effect and impact on cognition in Parkinson's disease: a cohort study , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[29]  T. Robbins,et al.  Evolution of cognitive dysfunction in an incident Parkinson's disease cohort. , 2007, Brain : a journal of neurology.

[30]  Y. Agid,et al.  Idazoxan, an alpha‐2 antagonist, and L‐DOPA‐induced dyskinesias in patients with Parkinson's disease , 2001, Movement disorders : official journal of the Movement Disorder Society.

[31]  Hannah S. Locke,et al.  Flexible neural mechanisms of cognitive control within human prefrontal cortex , 2009, Proceedings of the National Academy of Sciences.

[32]  G. Miller,et al.  Norepinephrine loss produces more profound motor deficits than MPTP treatment in mice , 2007, Proceedings of the National Academy of Sciences.

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

[34]  C. Marsden,et al.  Fronto-striatal cognitive deficits at different stages of Parkinson's disease. , 1992, Brain : a journal of neurology.

[35]  Y. Agid,et al.  Attentional deficits in Parkinson's disease: partial reversibility with naphtoxazine (SDZ NVI-085), a selective noradrenergic alpha 1 agonist. , 1998, Clinical neuropharmacology.

[36]  D. Morilak,et al.  Chronic Treatment with Desipramine Improves Cognitive Performance of Rats in an Attentional Set-Shifting Test , 2007, Neuropsychopharmacology.

[37]  Jonathan D. Cohen,et al.  Phasic Activation of Monkey Locus Ceruleus Neurons by Simple Decisions in a Forced-Choice Task , 2004, The Journal of Neuroscience.

[38]  R. Bakay,et al.  Cognitive impairments in advanced PD without dementia , 2002, Neurology.

[39]  T. Montine,et al.  Cognitive impairment and dementia in patients with Parkinson disease. , 2009, Current topics in medicinal chemistry.

[40]  D. Goldstein,et al.  Catechols in post‐mortem brain of patients with Parkinson disease , 2011, European journal of neurology.

[41]  S. Floresco,et al.  Multiple Dopamine Receptor Subtypes in the Medial Prefrontal Cortex of the Rat Regulate Set-Shifting , 2006, Neuropsychopharmacology.

[42]  O. Monchi,et al.  Dopamine Depletion Impairs Frontostriatal Functional Connectivity during a Set-Shifting Task , 2008, The Journal of Neuroscience.

[43]  B D Waterhouse,et al.  New perspectives on the functional organization and postsynaptic influences of the locus ceruleus efferent projection system. , 1998, Advances in pharmacology.

[44]  J. Hedreen,et al.  The locus ceruleus and dementia in Parkinson's disease , 1993, Neurology.

[45]  Marcus C. Ferguson,et al.  Cortical serotonin and norepinephrine denervation in parkinsonism: preferential loss of the beaded serotonin innervation , 2009, The European journal of neuroscience.

[46]  D. Kirik,et al.  Ventral tegmental area dopamine neurons are resistant to human mutant alpha-synuclein overexpression , 2006, Neurobiology of Disease.

[47]  Y. Agid,et al.  Improvement of levodopa-induced dyskinesia by propranolol in Parkinson's disease , 1996, Neurology.

[48]  F. Bloom,et al.  Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  P. Barone,et al.  Neurotransmission in Parkinson’s disease: beyond dopamine , 2010, European journal of neurology.

[50]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[51]  S. Sara,et al.  Network reset: a simplified overarching theory of locus coeruleus noradrenaline function , 2005, Trends in Neurosciences.

[52]  N. Bohnen,et al.  Cortical cholinergic function is more severely affected in parkinsonian dementia than in Alzheimer disease: an in vivo positron emission tomographic study. , 2003, Archives of neurology.

[53]  A. Strafella,et al.  L-Dopa Medication in Parkinson's Disease Restores Activity in the Motor Cortico-Striatal Loop but Does Not Modify the Cognitive Network , 2009, PloS one.

[54]  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.

[55]  F. Bloom,et al.  Nucleus locus ceruleus: new evidence of anatomical and physiological specificity. , 1983, Physiological reviews.

[56]  S. Floresco,et al.  Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure , 2008, Behavioural Brain Research.

[57]  H. Braak,et al.  Critical appraisal of brain pathology staging related to presymptomatic and symptomatic cases of sporadic Parkinson's disease. , 2006, Journal of neural transmission. Supplementum.

[58]  M. Ragozzino,et al.  The effects of dopamine D(1) receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility. , 2002, Learning & memory.

[59]  D. Morilak,et al.  Noradrenergic modulation of cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability , 2006, Neuroscience.

[60]  J. McGaughy,et al.  Atomoxetine reverses attentional deficits produced by noradrenergic deafferentation of medial prefrontal cortex , 2008, Psychopharmacology.

[61]  T. Robbins,et al.  The effect of dopamine depletion from the caudate nucleus of the common marmoset (Callithrix jacchus) on tests of prefrontal cognitive function. , 2000, Behavioral neuroscience.

[62]  E. Tolosa,et al.  Response to 4-month treatment with reboxetine in Parkinson's disease patients with a major depressive episode. , 2006, General hospital psychiatry.

[63]  A. Lees,et al.  Cognitive deficits in the early stages of Parkinson's disease. , 1983, Brain : a journal of neurology.

[64]  K. Jellinger The morphological basis of mental dysfunction in Parkinson's disease , 2006, Journal of the Neurological Sciences.

[65]  E. Abercrombie,et al.  Relationship between locus coeruleus discharge rates and rates of norepinephrine release within neocortex as assessed by in vivo microdialysis , 1999, Neuroscience.

[66]  Melissa Gerstenhaber,et al.  Atomoxetine for the treatment of executive dysfunction in Parkinson's disease: A pilot open‐label study , 2009, Movement disorders : official journal of the Movement Disorder Society.

[67]  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.

[68]  R. Hilker,et al.  Dementia in Parkinson disease , 2005, Neurology.

[69]  C. Berridge,et al.  Organization of noradrenergic efferents to arousal‐related basal forebrain structures , 2006, The Journal of comparative neurology.

[70]  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.

[71]  Thomas Gasser,et al.  Neuropathological assessment of Parkinson's disease: refining the diagnostic criteria , 2009, The Lancet Neurology.

[72]  Y. Miyashita,et al.  The Wisconsin Card Sorting Test , 2022 .

[73]  C. Berridge,et al.  The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes , 2003, Brain Research Reviews.

[74]  M. Petrides,et al.  Neural Bases of Set-Shifting Deficits in Parkinson's Disease , 2004, The Journal of Neuroscience.

[75]  F. Colpaert,et al.  Effects of locus coeruleus lesions on parkinsonian signs, striatal dopamine and substantia nigra cell loss after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in monkeys: A possible role for the locus coeruleus in the progression of Parkinson's disease , 1991, Neuroscience.

[76]  T R Ten Have,et al.  Atomoxetine for depression and other neuropsychiatric symptoms in Parkinson disease , 2010, Neurology.

[77]  T. Robbins,et al.  The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. , 2009, Annual review of neuroscience.

[78]  M. Gluck,et al.  α-Synuclein gene duplication impairs reward learning , 2010, Proceedings of the National Academy of Sciences.

[79]  G. Aston-Jones,et al.  Light deprivation damages monoamine neurons and produces a depressive behavioral phenotype in rats , 2008, Proceedings of the National Academy of Sciences.

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

[81]  F. Cuetos,et al.  Cognitive impairment in Parkinson's disease without dementia , 2010, Movement disorders : official journal of the Movement Disorder Society.

[82]  A. Graybiel,et al.  Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease , 1988, Nature.

[83]  M. Hoehn,et al.  Parkinsonism , 1967, Neurology.

[84]  K. Rommelfanger,et al.  Norepinephrine: The redheaded stepchild of Parkinson's disease. , 2007, Biochemical pharmacology.

[85]  D J Woodward,et al.  Modulatory actions of norepinephrine in the central nervous system. , 1979, Federation proceedings.

[86]  S. Floresco,et al.  Pharmacological Enhancement of Memory and Executive Functioning in Laboratory Animals , 2011, Neuropsychopharmacology.

[87]  G. Halliday,et al.  The progression of pathology in longitudinally followed patients with Parkinson’s disease , 2008, Acta Neuropathologica.

[88]  Angela J. Yu,et al.  Phasic norepinephrine: A neural interrupt signal for unexpected events , 2006, Network.

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

[90]  F. Fornai,et al.  The role of the locus coeruleus in the development of Parkinson's disease , 2000, Neuroscience & Biobehavioral Reviews.

[91]  G. Aston-Jones,et al.  Enhanced norepinephrine release in prefrontal cortex with burst stimulation of the locus coeruleus , 1996, Brain Research.

[92]  G. Aston-Jones,et al.  Role of the locus coeruleus in emotional activation. , 1996, Progress in brain research.

[93]  F. Fornai,et al.  Noradrenaline in Parkinson's disease: from disease progression to current therapeutics. , 2007, Current medicinal chemistry.

[94]  J. Cohen,et al.  The role of locus coeruleus in the regulation of cognitive performance. , 1999, Science.

[95]  T. Robbins,et al.  Differential regulation of fronto-executive function by the monoamines and acetylcholine. , 2007, Cerebral cortex.