Neuronal Entropy-Rate Feature of Entopeduncular Nucleus in Rat Model of Parkinson's Disease

The function of the nigro-striatal pathway on neuronal entropy in the basal ganglia (BG) output nucleus, i.e. the entopeduncular nucleus (EPN) was investigated in the unilaterally 6-hyroxydopamine (6-OHDA)-lesioned rat model of Parkinson's disease (PD). In both control subjects and subjects with 6-OHDA lesion of dopamine (DA) the nigro-striatal pathway, a histological hallmark for parkinsonism, neuronal entropy in EPN was maximal in neurons with firing rates ranging between 15 and 25 Hz. In 6-OHDA lesioned rats, neuronal entropy in the EPN was specifically higher in neurons with firing rates above 25 Hz. Our data establishes that the nigro-striatal pathway controls neuronal entropy in motor circuitry and that the parkinsonian condition is associated with abnormal relationship between firing rate and neuronal entropy in BG output nuclei. The neuronal firing rates and entropy relationship provide putative relevant electrophysiological information to investigate the sensory-motor processing in normal condition and conditions such as movement disorders.

[1]  Olivier Darbin,et al.  Nonlinear temporal organization of neuronal discharge in the basal ganglia of Parkinson's disease patients , 2010, Experimental Neurology.

[2]  Atsushi Nambu,et al.  Mechanism of parkinsonian neuronal oscillations in the primate basal ganglia: some considerations based on our recent work , 2014, Front. Syst. Neurosci..

[3]  Bin Deng,et al.  Closed-Loop Control of the thalamocortical Relay Neuron's Parkinsonian State Based on Slow Variable , 2013, Int. J. Neural Syst..

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

[5]  Satomi Chiken,et al.  Mechanism of DBS: Inhibition, Excitation, or Disruption? , 2015 .

[6]  A L Benabid,et al.  Unilateral lesion of the nigrostriatal pathway induces an increase of neuronal activity of the pedunculopontine nucleus, which is reversed by the lesion of the subthalamic nucleus in the rat , 2001, The European journal of neuroscience.

[7]  David Hansel,et al.  Late emergence of synchronized oscillatory activity in the pallidum during progressive parkinsonism , 2007, The European journal of neuroscience.

[8]  Olivier Darbin,et al.  Non-Linear Dynamics in Parkinsonism , 2013, Front. Neurol..

[9]  Thomas Wichmann,et al.  Pathophysiology of Parkinsonism , 2008, Clinical Neurophysiology.

[10]  D. Kooy,et al.  The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat , 1981, Brain Research.

[11]  J. A. Obeso,et al.  What basal ganglia changes underlie the parkinsonian state? The significance of neuronal oscillatory activity , 2013, Neurobiology of Disease.

[12]  Wei Yen Hsu,et al.  Application of Competitive Hopfield Neural Network to Brain-Computer Interface Systems , 2012, Int. J. Neural Syst..

[13]  J. Dostrovsky,et al.  Neuronal firing rates and patterns in the globus pallidus internus of patients with cervical dystonia differ from those with Parkinson's disease. , 2007, Journal of neurophysiology.

[14]  Dana Cohen,et al.  Electrophysiological characterization of entopeduncular nucleus neurons in anesthetized and freely moving rats , 2014, Front. Syst. Neurosci..

[15]  J. Obeso,et al.  Pathophysiology of the basal ganglia in Parkinson's disease , 2000, Trends in Neurosciences.

[16]  A. Benabid,et al.  Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat , 2000, Neuroscience.

[17]  Steven M. Pincus Approximate entropy as a measure of irregularity for psychiatric serial metrics. , 2006, Bipolar disorders.

[18]  Hitoshi Kita,et al.  Glutamatergic and Gabaergic Control of Pallidal Activity in Monkeys , 2005 .

[19]  J. J. Wright,et al.  Attractor Dynamics and Thermodynamic Analogies in the Cerebral Cortex: Synchronous Oscillation, the Background EEG, and the Regulation of Attention , 2011, Bulletin of mathematical biology.

[20]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[21]  Joachim K. Krauss,et al.  The rotenone-induced rat model of Parkinson's disease: Behavioral and electrophysiological findings , 2015, Behavioural Brain Research.

[22]  O. Darbin The aging striatal dopamine function. , 2012, Parkinsonism & related disorders.

[23]  J. Bouyer,et al.  Restraint in primate chair may cause unusual behaviour in baboons; electrocorticographic correlates and corrective effects of diazepam. , 1978, Electroencephalography and clinical neurophysiology.

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

[25]  Christoph Kayser,et al.  A role of the claustrum in auditory scene analysis by reflecting sensory change , 2014, Front. Syst. Neurosci..

[26]  J. Luthman,et al.  Sprouting of striatal serotonin nerve terminals following selective lesions of nigro-striatal dopamine neurons in neonatal rat , 1987, Brain Research Bulletin.

[27]  Ali Charara,et al.  Electrophysiological Interactions between Striatal Glutamatergic and Dopaminergic Systems , 2003, Annals of the New York Academy of Sciences.

[28]  Tiku T. Tanyimboh,et al.  Calculating Maximum Entropy Flows in Networks , 1993 .

[29]  R Stoop,et al.  Multiple-time-scale framework for understanding the progression of Parkinson's disease. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[30]  A. Nambu A new dynamic model of the cortico-basal ganglia loop. , 2004, Progress in brain research.

[31]  Atsushi Nambu,et al.  A new approach to understand the pathophysiology of Parkinson’s disease , 2005, Journal of neurology.

[32]  D Sapoznikov,et al.  Detection of regularities in heart rate variations by linear and non-linear analysis: power spectrum versus approximate entropy. , 1995, Computer methods and programs in biomedicine.

[33]  Stanley J. Watson,et al.  The rat brain in stereotaxic coordinates (2nd edn) by George Paxinos and Charles Watson, Academic Press, 1986. £40.00/$80.00 (264 pages) ISBN 012 547 6213 , 1987, Trends in Neurosciences.

[34]  D. A. Bergstrom,et al.  Nigrostriatal lesion and dopamine agonists affect firing patterns of rodent entopeduncular nucleus neurons. , 2002, Journal of neurophysiology.

[35]  S M Pincus,et al.  Approximate entropy as a measure of system complexity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Stephen B. Dunnett,et al.  The effect of additional noradrenergic and serotonergic depletion on a lateralised choice reaction time task in rats with nigral 6-OHDA lesions , 2014, Experimental Neurology.

[37]  Anton Bittner,et al.  Dopamine depletion induced up-regulation of HCN3 enhances rebound excitability of basal ganglia output neurons , 2009, Neurobiology of Disease.

[38]  M. W. Manning,et al.  GDNF Protection against 6-OHDA–Induced Reductions in Potassium-Evoked Overflow of Striatal Dopamine , 1999, The Journal of Neuroscience.

[39]  Daniela Sabrina Andres,et al.  Finite Dimensional Structure of the GPI discharge in Patients with Parkinson's Disease , 2011, Int. J. Neural Syst..

[40]  Daniela Sabrina Andres,et al.  Neuronal Entropy Depends on the Level of Alertness in the Parkinsonian Globus Pallidus in vivo , 2014, Front. Neurol..

[41]  H. Fibiger,et al.  Ascending catecholamine pathways and amphetamine-induced locomotor activity: Importance of dopamine and apparent non-involvement of norepinephrine , 1975, Brain Research.

[42]  Atsushi Nambu,et al.  Functional Circuitry of the Basal Ganglia , 2015 .

[43]  A. Nambu,et al.  Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway , 2002, Neuroscience Research.

[44]  C. Gerfen,et al.  Modulation of striatal projection systems by dopamine. , 2011, Annual review of neuroscience.

[45]  T. Wichmann,et al.  Apomorphine reduces subthalamic neuronal entropy in parkinsonian patients , 2010, Experimental Neurology.

[46]  Thomas Wichmann,et al.  Nonlinear analysis of discharge patterns in monkey basal ganglia , 2006, Brain Research.

[47]  J. Obeso,et al.  The basal ganglia in Parkinson's disease: Current concepts and unexplained observations , 2008, Annals of neurology.

[48]  A. Grace,et al.  The control of firing pattern in nigral dopamine neurons: burst firing , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  Reuben R. Shamir,et al.  Engineering the Next Generation of Clinical Deep Brain Stimulation Technology , 2015, Brain Stimulation.

[50]  J. Krauss,et al.  Effect of Deep Brain Stimulation on Levodopa-Induced Dyskinesias and Striatal Oscillatory Local Field Potentials in a Rat Model of Parkinson's Disease , 2014, Brain Stimulation.

[51]  J. P. Huston,et al.  The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments , 1996, Progress in Neurobiology.

[52]  Antoni Morro,et al.  Studying the Role of Synchronized and Chaotic Spiking Neural Ensembles in Neural Information Processing , 2014, Int. J. Neural Syst..

[53]  Rui Jiang,et al.  A Gray-Box Neural Network-Based Model Identification and Fault estimation Scheme for nonlinear Dynamic Systems , 2013, Int. J. Neural Syst..

[54]  S. Pincus Approximate entropy (ApEn) as a complexity measure. , 1995, Chaos.

[55]  Olivier Darbin,et al.  An Entropy-Based Model for Basal Ganglia Dysfunctions in Movement Disorders , 2013, BioMed research international.

[56]  P. Gatev,et al.  Oscillations in the basal ganglia under normal conditions and in movement disorders , 2006, Movement disorders : official journal of the Movement Disorder Society.

[57]  A. Nambu Seven problems on the basal ganglia , 2008, Current Opinion in Neurobiology.

[58]  Erwin B. Montgomery One View of the Current State of Understanding in Basal Ganglia Pathophysiology and What is Needed for the Future , 2011, Journal of movement disorders.