Neuronal activity pattern defects in the striatum in awake mouse model of Parkinson’s disease

HighlightsBilateral DA depletion reduces MSNs firing rate and burst activity during movement.Uni and Bilateral DA depletion both decrease firing rate of FSIs during movement.Uni and Bilateral DA depletion change striatal LFP oscillations during movement. Abstract Previous studies showed the loss of dopaminergic neurons directly leads to both changes in firing rate and neuronal synchrony in the striatum by pharmacogenetic approach, but physiological observation of striatal neurons in awake animal is rare up to now due to the limitation of recording methods. We use multichannel in vivo recording system, to record the activity pattern of both medium spiny projecting neurons (MSNs) and fast spiking interneurons (FSIs) in awake mouse model of Parkinson’s disease (PD), created by injection of 6‐hydroxyl‐dopamine (6‐OHDA) into dorsolateral striatum bilaterally and unilaterally. The abnormal discharge of neurons, including oscillations, burst activity and firing rate were systematically observed, and we used these index together to comprehensively analyse the functional change of striatal neurons in PD mouse model. We found that PD mouse model exhibited elevated synchronized oscillatory activity in &bgr; frequency band and decreased firing rate of FSIs during movement. The firing rate and burst activity of MSNs clearly reduced during movement after bilateral dopamine depletion. The present study has novelly shown the firing pattern changes of the MSNs and FSIs in DL striatum in awake PD mouse model, by combination of electrophysiology with molecular biological technology. Our results may help to reveal a new circuitry mechanism of movement disorders in PD.

[1]  John F. Marshall,et al.  Dopamine manipulation alters immediate-early gene response of striatal parvalbumin interneurons to cortical stimulation , 2005, Brain Research.

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

[3]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[4]  J. Dostrovsky,et al.  Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson's disease. , 2006, Journal of neurophysiology.

[5]  M. Hoane,et al.  Incomplete nigrostriatal dopaminergic cell loss and partial reductions in striatal dopamine produce akinesia, rigidity, tremor and cognitive deficits in middle-aged rats , 1999, Behavioural Brain Research.

[6]  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.

[7]  A. Oliviero,et al.  Dopamine Dependency of Oscillations between Subthalamic Nucleus and Pallidum in Parkinson's Disease , 2001, The Journal of Neuroscience.

[8]  J A Obeso,et al.  Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. , 2006, Brain : a journal of neurology.

[9]  J. Tepper,et al.  Inhibitory control of neostriatal projection neurons by GABAergic interneurons , 1999, Nature Neuroscience.

[10]  A. Priori,et al.  Movement-related modulation of neural activity in human basal ganglia and its L-DOPA dependency: recordings from deep brain stimulation electrodes in patients with Parkinson's disease , 2002, Neurological Sciences.

[11]  Kim T Blackwell,et al.  Desynchronization of Fast-Spiking Interneurons Reduces β-Band Oscillations and Imbalance in Firing in the Dopamine-Depleted Striatum , 2015, The Journal of Neuroscience.

[12]  G. C. McConnell,et al.  Frequency-dependent, transient effects of subthalamic nucleus deep brain stimulation on methamphetamine-induced circling and neuronal activity in the hemiparkinsonian rat , 2017, Behavioural Brain Research.

[13]  Henrike Planert,et al.  Dynamics of Synaptic Transmission between Fast-Spiking Interneurons and Striatal Projection Neurons of the Direct and Indirect Pathways , 2010, The Journal of Neuroscience.

[14]  J. Walters,et al.  Oscillatory Activity in Basal Ganglia and Motor Cortex in an Awake Behaving Rodent Model of Parkinson's Disease. , 2014, Basal ganglia.

[15]  J. Walters,et al.  State-Dependent Spike and Local Field Synchronization between Motor Cortex and Substantia Nigra in Hemiparkinsonian Rats , 2012, The Journal of Neuroscience.

[16]  Yasuo Kawaguchi,et al.  Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin , 1987, Brain Research.

[17]  Anatol C. Kreitzer,et al.  Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry , 2010, Nature.

[18]  Donald J. Woodward,et al.  Neural responses in multiple basal ganglia regions following unilateral dopamine depletion in behaving rats performing a treadmill locomotion task , 2006, Experimental Brain Research.

[19]  Andrea A. Kühn,et al.  The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson's disease , 2005, Experimental Neurology.

[20]  Tsuyoshi Murata,et al.  {m , 1934, ACML.

[21]  A. Priori,et al.  Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease , 2004, Experimental Neurology.

[22]  Joseph P Huston,et al.  Behavioral phenotyping of the MPTP mouse model of Parkinson's disease , 2001, Behavioural Brain Research.

[23]  C. Luo,et al.  The effects of unilateral 6-OHDA lesion in medial forebrain bundle on the motor, cognitive dysfunctions and vulnerability of different striatal interneuron types in rats , 2014, Behavioural Brain Research.

[24]  Louise C. Parr-Brownlie,et al.  Beta frequency synchronization in basal ganglia output during rest and walk in a hemiparkinsonian rat , 2010, Experimental Neurology.

[25]  R. Romo,et al.  Effects of unilateral electrical stimulation of various thalamic nuclei on the release of dopamine from dendrites and nerve terminals of neurons of the two nigrostriatal dopaminergic pathways , 1983, Neuroscience.

[26]  Jozsef Csicsvari,et al.  Disrupted Dopamine Transmission and the Emergence of Exaggerated Beta Oscillations in Subthalamic Nucleus and Cerebral Cortex , 2008, The Journal of Neuroscience.

[27]  T. Cassano,et al.  Striatal 6-OHDA lesion in mice: Investigating early neurochemical changes underlying Parkinson's disease , 2010, Behavioural Brain Research.

[28]  M. Gernert,et al.  Deficit of Striatal Parvalbumin-Reactive GABAergic Interneurons and Decreased Basal Ganglia Output in a Genetic Rodent Model of Idiopathic Paroxysmal Dystonia , 2000, The Journal of Neuroscience.

[29]  Anatol C. Kreitzer,et al.  Selective Inhibition of Striatal Fast-Spiking Interneurons Causes Dyskinesias , 2011, The Journal of Neuroscience.

[30]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[31]  P. Jenner,et al.  The rationale for the use of dopamine agonists in Parkinson's disease , 1995, Neurology.

[32]  Fiona E. N. LeBeau,et al.  Recruitment of Parvalbumin-Positive Interneurons Determines Hippocampal Function and Associated Behavior , 2007, Neuron.

[33]  M. Nicolelis,et al.  Differential Corticostriatal Plasticity during Fast and Slow Motor Skill Learning in Mice , 2004, Current Biology.

[34]  Robert E. Gross,et al.  Human striatal recordings reveal abnormal discharge of projection neurons in Parkinson’s disease , 2016, Proceedings of the National Academy of Sciences.

[35]  Intrinsic and network mechanisms involved in balanced firing and striatal synchrony during dopamine depletion , 2013, BMC Neuroscience.

[36]  J. Krauss,et al.  Neuronal activity in the medial associative‐limbic and lateral motor part of the rat subthalamic nucleus and the effect of 6‐hydroxydopamine‐induced lesions of the dorsolateral striatum , 2013, The Journal of comparative neurology.

[37]  Antonio Oliviero,et al.  Effects of stimulation of the subthalamic area on oscillatory pallidal activity in Parkinson's disease , 2004, Experimental Neurology.

[38]  Jerald L Schnoor,et al.  What the h? , 2008, Environmental science & technology.

[39]  A. Sadikot,et al.  GABA promotes survival but not proliferation of parvalbumin-immunoreactive interneurons in rodent neostriatum: an in vivo study with stereology , 2001, Neuroscience.

[40]  Junxia Xie,et al.  High frequency stimulation of subthalamic nucleus results in behavioral recovery by increasing striatal dopamine release in 6-hydroxydopamine lesioned rat , 2014, Behavioural Brain Research.

[41]  G. Petzinger,et al.  The parkinsonian toxin 1‐methyl‐4‐phenyl‐1,2,3,6‐tetrahydropyridine (MPTP): a technical review of its utility and safety , 2001, Journal of neurochemistry.

[42]  G. Heit,et al.  Regular Article Intra-operative STN DBS attenuates the prominent beta rhythm in the STN in Parkinson's disease , 2006 .

[43]  B. Hyland,et al.  Bradykinesia Induced by Dopamine D2 Receptor Blockade Is Associated with Reduced Motor Cortex Activity in the Rat , 2005, The Journal of Neuroscience.

[44]  M. DiFiglia,et al.  Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[45]  B. Ferger,et al.  Neurochemical findings in the MPTP model of Parkinson's disease , 2001, Journal of neural transmission.

[46]  John B. Shoven,et al.  I , Edinburgh Medical and Surgical Journal.

[47]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[48]  P. Barnéoud,et al.  Effects of complete and partial lesions of the dopaminergic mesotelencephalic system on skilled forelimb use in the rat , 1995, Neuroscience.

[49]  J. Walters,et al.  Functional correlates of exaggerated oscillatory activity in basal ganglia output in hemiparkinsonian rats , 2014, Experimental Neurology.

[50]  Mandy Miller Koop,et al.  Intra-operative STN DBS attenuates the prominent beta rhythm in the STN in Parkinson's disease , 2006, Experimental Neurology.

[51]  P. Brown,et al.  Reduction in subthalamic 8–35 Hz oscillatory activity correlates with clinical improvement in Parkinson's disease , 2006, The European journal of neuroscience.

[52]  G. Halliday,et al.  Relationships between various behavioural abnormalities and nigrostriatal dopamine depletion in the unilateral 6-OHDA-lesioned rat , 2003, Behavioural Brain Research.

[53]  Hitoshi Kita,et al.  Role of Striatum in the Pause and Burst Generation in the Globus Pallidus of 6-OHDA-Treated Rats , 2011, Front. Syst. Neurosci..

[54]  A. Björklund,et al.  Studies on Neuroprotective and Regenerative Effects of GDNF in a Partial Lesion Model of Parkinson's Disease , 1997, Neurobiology of Disease.

[55]  Jae-Ick Kim,et al.  Functional Roles of Neurotransmitters and Neuromodulators in the Dorsal Striatum Circuits: Glutamatergic and Gabaergic Transmission Thalamostriatal Circuit Local Gabaergic Circuits: Parvalbumin-expressing Fast-spiking Interneurons and Neuropeptide-y Positive Low-threshold Spiking Interneurons Neurom , 2022 .

[56]  S. Dunnett,et al.  Unilateral nigrostriatal 6-hydroxydopamine lesions in mice I: Motor impairments identify extent of dopamine depletion at three different lesion sites , 2012, Behavioural Brain Research.

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

[58]  Rui M. Costa,et al.  Rapid Alterations in Corticostriatal Ensemble Coordination during Acute Dopamine-Dependent Motor Dysfunction , 2006, Neuron.

[59]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[60]  Greg A. Gerhardt,et al.  Multiple single-unit recordings in the striatum of freely moving animals: effects of apomorphine and d-amphetamine in normal and unilateral 6-hydroxydopamine-lesioned rats , 1999, Brain Research.

[61]  Y. Agid,et al.  Dopaminergic sprouting in the rat striatum after partial lesion of the substantia nigra , 1996, Brain Research.

[62]  P. Somogyi,et al.  Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons , 2000, Nature Neuroscience.

[63]  J. Cadet,et al.  Invited Review Free radicals and the pathobiology of brain dopamine systems , 1998, Neurochemistry International.

[64]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[65]  S. Epstein,et al.  Background gamma rhythmicity and attention in cortical local circuits: a computational study. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[66]  T. Robinson,et al.  Changes in striatal dopamine neurotransmission assessed with microdialysis following recovery from a bilateral 6-OHDA lesion: variation as a function of lesion size , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  J. Berke Uncoordinated Firing Rate Changes of Striatal Fast-Spiking Interneurons during Behavioral Task Performance , 2008, The Journal of Neuroscience.

[68]  Xin Jin,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience , 2022 .

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

[70]  D. Plenz When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function , 2003, Trends in Neurosciences.

[71]  A. Oliviero,et al.  Patterning of globus pallidus local field potentials differs between Parkinson's disease and dystonia. , 2003, Brain : a journal of neurology.

[72]  Anatol C. Kreitzer,et al.  Distinct Roles of GABAergic Interneurons in the Regulation of Striatal Output Pathways , 2010, The Journal of Neuroscience.

[73]  Mark D. Humphries,et al.  Dopamine-modulated dynamic cell assemblies generated by the GABAergic striatal microcircuit , 2009, Neural Networks.

[74]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[75]  Anatol C. Kreitzer,et al.  Striatal microcircuitry and movement disorders , 2012, Trends in Neurosciences.

[76]  G. Nikkhah,et al.  Comparison of unilateral and bilateral intrastriatal 6‐hydroxydopamine‐induced axon terminal lesions: Evidence for interhemispheric functional coupling of the two nigrostriatal pathways , 2001, The Journal of comparative neurology.

[77]  B. D. Bennett,et al.  Synaptic input and output of parvalbumin-immunoreactive neurons in the neostriatum of the rat , 1994, Neuroscience.