Asymmetric Dopaminergic Degeneration and Attentional Resources in Parkinson’s Disease

Background: Attention is crucial to voluntary perform actions in Parkinson’s disease (PD), allowing patients to bypass the impaired habitual motor control. The asymmetrical degeneration of the dopaminergic system could affect the attentional functions. Objective: To investigate the relationship between the asymmetric dopaminergic degeneration and the attentional resources in Parkinsonian patients with right-side (RPD) and left-side (LPD) motor symptoms predominance. Methods: 50 RPD, 50 LPD, and 34 healthy controls underwent visual (V), auditory (A), and multiple choices (MC) reaction time (RTs) tasks. For PD patients, these tasks were performed before and after a 4-week intensive, motor-cognitive rehabilitation treatment (MIRT). The effectiveness of treatment was evaluated assessing Unified Parkinson’s disease Rating Scale (UPDRS) III and Timed-up and Go Test (TUG). Results: RTs did not differ between PD patients and healthy controls. Before MIRT, no differences between LPD and RPD patients were observed in RTs (p = 0.20), UPDRS III (p = 0.60), and TUG (p = 0.38). No differences in dopaminergic medication were found between groups (p = 0.44 and p = 0.66 before and after MIRT, respectively). After MIRT, LPD patients showed a significant reduction in MC RTs (p = 0.05), V RTs (p = 0.02), and MC-V RTs. A significant association between changes in RTs and improvements in UPDRS III and TUG was observed in LPD patients. Conclusion: attention does not differ among RPD patients, LPD patients and healthy controls. Only LPD patients improved their performances on attentional tasks after MIRT. We argue that the increased early susceptibility of the left nigrostriatal system to degeneration affects differently the cognitive modifiability and the neuroplastic potential. Our results could provide insight into new therapeutic approaches, highlighting the importance to design different treatments for RPD patients and LPD patients.

[1]  M. Hoehn,et al.  Parkinsonism , 2020, Definitions.

[2]  Nir Giladi,et al.  Basal ganglia and beyond: The interplay between motor and cognitive aspects in Parkinson’s disease rehabilitation , 2018, Neuroscience & Biobehavioral Reviews.

[3]  M. Ghilardi,et al.  Efficacy of intensive multidisciplinary rehabilitation in Parkinson’s disease: a randomised controlled study , 2018, Journal of Neurology, Neurosurgery, and Psychiatry.

[4]  D. Qiao,et al.  Treadmill Exercise Improves Motor Dysfunction and Hyperactivity of the Corticostriatal Glutamatergic Pathway in Rats with 6-OHDA-Induced Parkinson's Disease , 2017, Neural plasticity.

[5]  Nir Giladi,et al.  Focused and Sustained Attention Is Modified by a Goal-Based Rehabilitation in Parkinsonian Patients , 2017, Front. Behav. Neurosci..

[6]  T. Wilson,et al.  The cortical signature of symptom laterality in Parkinson's disease , 2017, NeuroImage: Clinical.

[7]  B. Dawant,et al.  Cortical asymmetry in Parkinson's disease: early susceptibility of the left hemisphere , 2016, Brain and behavior.

[8]  M. Ghilardi,et al.  Intensive Rehabilitation Enhances Lymphocyte BDNF-TrkB Signaling in Patients With Parkinson’s Disease , 2016, Neurorehabilitation and neural repair.

[9]  Litia A. Carvalho,et al.  Neurotrophic factors in Parkinson's disease are regulated by exercise: Evidence-based practice , 2016, Journal of the Neurological Sciences.

[10]  S. Leurgans,et al.  Exercise improves cognition in Parkinson's disease: The PRET‐PD randomized, clinical trial , 2015, Movement disorders : official journal of the Movement Disorder Society.

[11]  C. Caltagirone,et al.  Neuropsychiatric and cognitive symptoms and body side of onset of parkinsonism in unmedicated Parkinson's disease patients. , 2015, Parkinsonism & related disorders.

[12]  R. Maestri,et al.  Differences in Muscle Strength in Parkinsonian Patients Affected on the Right and Left Side , 2015, PloS one.

[13]  Meir Plotnik,et al.  Working on asymmetry in Parkinson’s disease: randomized, controlled pilot study , 2015, Neurological Sciences.

[14]  Roberto Maestri,et al.  Intensive Rehabilitation Treatment in Early Parkinson’s Disease , 2015, Neurorehabilitation and neural repair.

[15]  S. Logue,et al.  The neural and genetic basis of executive function: Attention, cognitive flexibility, and response inhibition , 2014, Pharmacology Biochemistry and Behavior.

[16]  Gereon R. Fink,et al.  Dorsal and Ventral Attention Systems , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[17]  Roberto Maestri,et al.  Intensive Rehabilitation Increases BDNF Serum Levels in Parkinsonian Patients , 2014, Neurorehabilitation and neural repair.

[18]  D. Waldvogel,et al.  Body side and predominant motor features at the onset of Parkinson's disease are linked to motor and nonmotor progression , 2014, Movement disorders : official journal of the Movement Disorder Society.

[19]  B. Röder,et al.  Beneficial effects of physical exercise on neuroplasticity and cognition , 2013, Neuroscience & Biobehavioral Reviews.

[20]  S. McEwen,et al.  Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease , 2013, The Lancet Neurology.

[21]  Nin Bajaj,et al.  Clinical utility of dopamine transporter single photon emission CT (DaT-SPECT) with (123I) ioflupane in diagnosis of parkinsonian syndromes , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[22]  M. T. Pellecchia,et al.  Side of onset does not influence cognition in newly diagnosed untreated Parkinson's disease patients. , 2013, Parkinsonism & related disorders.

[23]  U. Bonuccelli,et al.  The relationship between motor symptom lateralization and cognitive performance in newly diagnosed drug-naïve patients with Parkinson's disease , 2013, Journal of clinical and experimental neuropsychology.

[24]  Klaus Seppi,et al.  Left hemispheric predominance of nigrostriatal dysfunction in Parkinson's disease. , 2012, Brain : a journal of neurology.

[25]  M. Posner,et al.  The attention system of the human brain: 20 years after. , 2012, Annual review of neuroscience.

[26]  B. D. de Jong,et al.  Handedness correlates with the dominant Parkinson side: A systematic review and meta‐analysis , 2012, Movement disorders : official journal of the Movement Disorder Society.

[27]  Pietro Balbi,et al.  Effectiveness of Intensive Inpatient Rehabilitation Treatment on Disease Progression in Parkinsonian Patients , 2012, Neurorehabilitation and neural repair.

[28]  Joy J. Geng,et al.  Contextual Knowledge Configures Attentional Control Networks , 2011, The Journal of Neuroscience.

[29]  G. Vingerhoets,et al.  Cognitive Differences Between Patients with Left-sided and Right-sided Parkinson’s Disease. A Review , 2011, Neuropsychology Review.

[30]  R. Ratcliff,et al.  Diffusion model for one-choice reaction-time tasks and the cognitive effects of sleep deprivation , 2011, Proceedings of the National Academy of Sciences.

[31]  P. Robert,et al.  Dysexecutive syndrome: Diagnostic criteria and validation study , 2010, Annals of neurology.

[32]  L. Schöls,et al.  CSF Aβ42 and tau in Parkinson's disease with cognitive impairment , 2010, Movement disorders : official journal of the Movement Disorder Society.

[33]  R. Helmich,et al.  Side of symptom onset affects motor dysfunction in Parkinson's disease , 2010, Neuroscience.

[34]  H. Vankova Mini Mental State , 2010 .

[35]  Meg E Morris,et al.  Striding Out With Parkinson Disease: Evidence-Based Physical Therapy for Gait Disorders , 2010, Physical Therapy.

[36]  Lynn Rochester,et al.  Motor learning in Parkinson's disease: limitations and potential for rehabilitation. , 2009, Parkinsonism & related disorders.

[37]  J. Aharon-Peretz,et al.  Dopamine asymmetry interacts with medication to affect cognition in Parkinson's disease , 2007, Neuropsychologia.

[38]  I. McNish Clocking the Mind: Mental Chronometry and Individual Differences , 2007 .

[39]  Meg E Morris,et al.  Locomotor Training in People With Parkinson Disease , 2006, Physical Therapy.

[40]  R. Djaldetti,et al.  The mystery of motor asymmetry in Parkinson's disease , 2006, The Lancet Neurology.

[41]  T. Robbins,et al.  Lateralisation of striatal function: evidence from 18F-dopa PET in Parkinson’s disease , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[42]  P. Nichelli,et al.  The Frontal Assessment Battery (FAB): normative values in an Italian population sample , 2005, Neurological Sciences.

[43]  Jeffrey M. Hausdorff,et al.  Is freezing of gait in Parkinson's disease related to asymmetric motor function? , 2005, Annals of neurology.

[44]  B. Fisher,et al.  Exercise‐induced behavioral recovery and neuroplasticity in the 1‐methyl‐4‐phenyl‐1,2,3,6‐tetrahydropyridine‐lesioned mouse basal ganglia , 2004, Journal of neuroscience research.

[45]  A. Nieoullon Dopamine and the regulation of cognition and attention , 2002, Progress in Neurobiology.

[46]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

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

[48]  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.

[49]  I Litvan,et al.  The FAB: A frontal assessment battery at bedside , 2000, Neurology.

[50]  M. Thaut,et al.  The connection between rhythmicity and brain function , 1999, IEEE Engineering in Medicine and Biology Magazine.

[51]  M. Sliwinski,et al.  Cognitive and affective functioning in Parkinson's disease patients with lateralized motor signs. , 1998, Journal of clinical and experimental neuropsychology.

[52]  Younglim Lee,et al.  A Primary Acoustic Startle Pathway: Obligatory Role of Cochlear Root Neurons and the Nucleus Reticularis Pontis Caudalis , 1996, The Journal of Neuroscience.

[53]  B. Mackenzie,et al.  The relationship between speed of information processing and cognitive ability , 1996 .

[54]  E Magni,et al.  Mini‐Mental State Examination: a normative study in Italian elderly population , 1996, European journal of neurology.

[55]  M. Viitanen,et al.  Association between presenting motor symptoms and the risk of cognitive impairment in Parkinson's disease. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[56]  R. Ratcliff Methods for dealing with reaction time outliers. , 1993, Psychological bulletin.

[57]  R. Cohen The Neuropsychology of Attention , 1993, Critical Issues in Neuropsychology.

[58]  J. Hughes,et al.  Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[59]  W. Weiner,et al.  Visuospatial impairment in Parkinson's disease , 1991, Neurology.

[60]  G. Paulson,et al.  Neuropsychological Similarities in Lateralized Parkinsonism , 1989, Cortex.

[61]  Stephen M. Rao,et al.  Effects of Intravenous Physostigmine and Lecithin on Memory Loss in Multiple Sclerosis: Report of a Pilot Study , 1988 .

[62]  S. Bentin,et al.  Asymmetrical Cognitive Deterioration in Demented and Parkinson Patients , 1981, Cortex.

[63]  S. Rossignol,et al.  Audio-spinal influence in man studied by the H-reflex and its possible role on rhythmic movements synchronized to sound. , 1976, Electroencephalography and clinical neurophysiology.

[64]  S. Folstein,et al.  “Mini-mental state”: A practical method for grading the cognitive state of patients for the clinician , 1975 .

[65]  M. Sanjak,et al.  Exercise-induced neuroplasticity in human Parkinson's disease: What is the evidence telling us? , 2016, Parkinsonism & related disorders.

[66]  Robert Iansek,et al.  Gait festination and freezing in Parkinson's disease: Pathogenesis and rehabilitation , 2008, Movement disorders : official journal of the Movement Disorder Society.

[67]  S. Gilman,et al.  Diagnostic criteria for Parkinson disease. , 1999, Archives of neurology.

[68]  J. Baron,et al.  PET imaging of neocortical monoaminergic terminals in Parkinson's disease , 1995, Journal of neural transmission. Parkinson's disease and dementia section.

[69]  Jessica A. Grahn,et al.  Neuroscience and Biobehavioral Reviews into the Groove: Can Rhythm Influence Parkinson's Disease? , 2022 .