Untangling Cortico-Striatal Connectivity and Cross-Frequency Coupling in L-DOPA-Induced Dyskinesia

We simultaneously recorded local field potentials (LFPs) in the primary motor cortex and sensorimotor striatum in awake, freely behaving, 6-OHDA lesioned hemi-parkinsonian rats in order to study the features directly related to pathological states such as parkinsonian state and levodopa-induced dyskinesia. We analyzed the spectral characteristics of the obtained signals and observed that during dyskinesia the most prominent feature was a relative power increase in the high gamma frequency range at around 80 Hz, while for the parkinsonian state it was in the beta frequency range. Here we show that during both pathological states effective connectivity in terms of Granger causality is bidirectional with an accent on the striatal influence on the cortex. In the case of dyskinesia, we also found a high increase in effective connectivity at 80 Hz. In order to further understand the 80-Hz phenomenon, we performed cross-frequency analysis and observed characteristic patterns in the case of dyskinesia but not in the case of the parkinsonian state or the control state. We noted a large decrease in the modulation of the amplitude at 80 Hz by the phase of low frequency oscillations (up to ~10 Hz) across both structures in the case of dyskinesia. This may suggest a lack of coupling between the low frequency activity of the recorded network and the group of neurons active at ~80 Hz.

[1]  Webster Ke Cortico-striate interrelations in the albino rat. , 1961 .

[2]  H. Eichenbaum,et al.  Oscillatory Entrainment of Striatal Neurons in Freely Moving Rats , 2004, Neuron.

[3]  Adriano B. L. Tort,et al.  Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task , 2008, Proceedings of the National Academy of Sciences.

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

[5]  C. Gerfen,et al.  Priming for l-dopa-induced dyskinesia in Parkinson’s disease: A feature inherent to the treatment or the disease? , 2009, Progress in Neurobiology.

[6]  A. Graybiel,et al.  Striosomes and mood dysfunction in Huntington's disease. , 2007, Brain : a journal of neurology.

[7]  H. Akaike A new look at the statistical model identification , 1974 .

[8]  A. Oliviero,et al.  Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. , 2002, Brain : a journal of neurology.

[9]  K. Miller,et al.  Exaggerated phase–amplitude coupling in the primary motor cortex in Parkinson disease , 2013, Proceedings of the National Academy of Sciences.

[10]  A. Pérez-Villalba Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[11]  Charles J. Wilson,et al.  Corticostriatal combinatorics: the implications of corticostriatal axonal arborizations. , 2002, Journal of neurophysiology.

[12]  J. Girault,et al.  What is the Degree of Segregation between Striatonigral and Striatopallidal Projections? , 2010, Front. Neuroanat..

[13]  Andreas Klaus,et al.  Mapping of Cortical Avalanches to the Striatum , 2015 .

[14]  S. Grillner,et al.  Mechanisms for selection of basic motor programs – roles for the striatum and pallidum , 2005, Trends in Neurosciences.

[15]  C. Tanner Epidemiology of Parkinson’s Disease , 1992, Neurologic Clinics.

[16]  J. Deniau,et al.  Synaptic Convergence of Motor and Somatosensory Cortical Afferents onto GABAergic Interneurons in the Rat Striatum , 2002, Journal of Neuroscience.

[17]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[18]  S. Bressler,et al.  Granger Causality: Basic Theory and Application to Neuroscience , 2006, q-bio/0608035.

[19]  Peter Brown,et al.  Oscillations in the Basal Ganglia: The good, the bad, and the unexpected , 2005 .

[20]  Zhentao Zhang,et al.  Impulsive and Compulsive Behaviors in Parkinson’s Disease , 2014, Front. Aging Neurosci..

[21]  Yvette E. Fisher,et al.  Differential Electrophysiological Changes in Striatal Output Neurons in Huntington's Disease , 2011, The Journal of Neuroscience.

[22]  A. Pisani,et al.  Levodopa-induced dyskinesia and striatal signaling pathways , 2009, Proceedings of the National Academy of Sciences.

[23]  Y. Smith,et al.  The thalamostriatal system: a highly specific network of the basal ganglia circuitry , 2004, Trends in Neurosciences.

[24]  John M. Beggs,et al.  Behavior Modulates Effective Connectivity between Cortex and Striatum , 2014, PloS one.

[25]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[26]  A. Aertsen,et al.  Representation of cooperative firing activity among simultaneously recorded neurons. , 1985, Journal of neurophysiology.

[27]  Matthijs A. A. van der Meer,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Low and High Gamma Oscillations in Rat Ventral Striatum Have Distinct Relationships to Behavior, Reward, and Spiking Activity on a Learned Spatial Decision Task , 2022 .

[28]  Charles J. Wilson,et al.  Connectivity and Convergence of Single Corticostriatal Axons , 1998, The Journal of Neuroscience.

[29]  M. Wibral,et al.  Untangling cross-frequency coupling in neuroscience , 2014, Current Opinion in Neurobiology.

[30]  Sarwant Singh,et al.  Connectivity and Convergence , 2012 .

[31]  Ian Q. Whishaw,et al.  Animal models of neurological deficits: how relevant is the rat? , 2002, Nature Reviews Neuroscience.

[32]  T. Shike,et al.  Animal models. , 2001, Contributions to nephrology.

[33]  A. Redish,et al.  Integrating Early Results on Ventral Striatal Gamma Oscillations in the Rat , 2010, Front. Neurosci..

[34]  Michael X. Cohen,et al.  Oscillatory Activity and Phase–Amplitude Coupling in the Human Medial Frontal Cortex during Decision Making , 2009, Journal of Cognitive Neuroscience.

[35]  B. Sabatini,et al.  Antagonistic but Not Symmetric Regulation of Primary Motor Cortex by Basal Ganglia Direct and Indirect Pathways , 2015, Neuron.

[36]  J. Jankovic,et al.  Impulse Control Disorders and Pathological Gambling in Patients With Parkinson Disease , 2008, The neurologist.

[37]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[38]  M. Boly,et al.  Granger Causality Analysis of Steady-State Electroencephalographic Signals during Propofol-Induced Anaesthesia , 2012, PloS one.

[39]  C. Konradi,et al.  Maladaptive striatal plasticity in L-DOPA-induced dyskinesia. , 2010, Progress in brain research.

[40]  T. Schreiber,et al.  Information transfer in continuous processes , 2002 .

[41]  E. Chee,et al.  Volumetric MRI changes in basal ganglia of children with Tourette's syndrome , 1993, Neurology.

[42]  Tom Robinson,et al.  Levodopa-induced dyskinesia in Parkinson’s disease: clinical features, pathogenesis, prevention and treatment , 2007, Postgraduate Medical Journal.

[43]  A. Seth,et al.  Granger Causality Analysis in Neuroscience and Neuroimaging , 2015, The Journal of Neuroscience.

[44]  M. Delong,et al.  Functional and pathophysiological models of the basal ganglia , 1996, Current Opinion in Neurobiology.

[45]  C. Goetz,et al.  Levodopa‐induced dyskinesias , 2007, Movement disorders : official journal of the Movement Disorder Society.

[46]  Joseph B. Martin Huntington's disease , 1984, Neurology.

[47]  J. Berke,et al.  Fast oscillations in cortical‐striatal networks switch frequency following rewarding events and stimulant drugs , 2009, The European journal of neuroscience.

[48]  Agid Yves Levodopa‐induced dyskinesia , 1992 .

[49]  P. Petersson,et al.  Mechanisms underlying cortical resonant states: implications for levodopa-induced dyskinesia , 2013, Reviews in the neurosciences.

[50]  K. Müller-Vahl,et al.  Tourette's syndrome. , 2009, Current topics in behavioral neurosciences.

[51]  P. Redgrave,et al.  The basal ganglia: a vertebrate solution to the selection problem? , 1999, Neuroscience.

[52]  Jeanette Hellgren Kotaleski,et al.  Behavior discrimination using a discrete wavelet based approach for feature extraction on local field potentials in the cortex and striatum , 2015, 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER).

[53]  Richard Mayeux,et al.  Epidemiology of neurodegeneration. , 2003, Annual review of neuroscience.

[54]  J. Geweke,et al.  Measurement of Linear Dependence and Feedback between Multiple Time Series , 1982 .

[55]  Erwan Bezard,et al.  Pathophysiology of levodopa-induced dyskinesia: Potential for new therapies , 2001, Nature Reviews Neuroscience.

[56]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[57]  P. Brown Oscillatory nature of human basal ganglia activity: Relationship to the pathophysiology of Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[58]  Cristina Tassorelli,et al.  Functional changes of the basal ganglia circuitry in Parkinson's disease , 2000, Progress in Neurobiology.

[59]  Anil K. Seth,et al.  A MATLAB toolbox for Granger causal connectivity analysis , 2010, Journal of Neuroscience Methods.

[60]  D. Oorschot Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: A stereological study using the cavalieri and optical disector methods , 1996, The Journal of comparative neurology.

[61]  Peter Brown,et al.  Directional analysis of coherent oscillatory field potentials in the cerebral cortex and basal ganglia of the rat , 2005, The Journal of physiology.

[62]  C. Granger Investigating causal relations by econometric models and cross-spectral methods , 1969 .

[63]  Michael Bloch,et al.  Recent advances in Tourette syndrome. , 2011, Current opinion in neurology.

[64]  C. Segebarth,et al.  Identifying Neural Drivers with Functional MRI: An Electrophysiological Validation , 2008, PLoS biology.

[65]  J. Mink,et al.  Recent advances in Tourette syndrome research , 2006, Trends in Neurosciences.

[66]  Anil K. Seth,et al.  The MVGC multivariate Granger causality toolbox: A new approach to Granger-causal inference , 2014, Journal of Neuroscience Methods.

[67]  H. Bergman,et al.  Pathological synchronization in Parkinson's disease: networks, models and treatments , 2007, Trends in Neurosciences.

[68]  Adriano B. L. Tort,et al.  Theta–gamma coupling increases during the learning of item–context associations , 2009, Proceedings of the National Academy of Sciences.

[69]  J. Walters,et al.  Effects of L-dopa priming on cortical high beta and high gamma oscillatory activity in a rodent model of Parkinson's disease , 2016, Neurobiology of Disease.

[70]  J. Brotchie,et al.  Levodopa-induced dyskinesia in Parkinson’s disease , 2005, Journal of neural transmission.

[71]  O. Jensen,et al.  Cross-frequency coupling between neuronal oscillations , 2007, Trends in Cognitive Sciences.

[72]  Nicole C. Swann,et al.  Therapeutic deep brain stimulation reduces cortical phase-amplitude coupling in Parkinson's disease , 2015, Nature Neuroscience.

[73]  E. Vaadia,et al.  Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates , 1998, Trends in Neurosciences.

[74]  P. Petersson,et al.  Levodopa-Induced Dyskinesia Is Strongly Associated with Resonant Cortical Oscillations , 2012, The Journal of Neuroscience.