Altered Local Field Potential Relationship Between the Parafascicular Thalamic Nucleus and Dorsal Striatum in Hemiparkinsonian Rats
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摘要
The thalamostriatal pathway is implicated in Parkinson's disease(PD); however, PD-related changes in the relationship between oscillatory activity in the centromedian-parafascicular complex(CM/Pf, or the Pf in rodents) and the dorsal striatum(DS) remain unclear.Therefore, we simultaneously recorded local field potentials(LFPs) in both the Pf and DS of hemiparkinsonian and control rats during epochs of rest or treadmill walking. The dopamine-lesioned rats showed increased LFP power in the beta band(12 Hz–35 Hz) in the Pf and DS during both epochs, but decreased LFP power in the delta(0.5 Hz–3 Hz) band in the Pf during rest epochs and in the DS during both epochs, compared to control rats. In addition,exaggerated low gamma(35 Hz–70 Hz) oscillations after dopamine loss were restricted to the Pf regardless of the behavioral state. Furthermore, enhanced synchronization of LFP oscillations was found between the Pf and DS after the dopamine lesion. Significant increases occurred in the mean coherence in both theta(3 Hz–7 Hz) and beta bands,and a significant increase was also noted in the phase coherence in the beta band between the Pf and DS during rest epochs. During the treadmill walking epochs, significant increases were found in both the alpha(7 Hz–12 Hz)and beta bands for two coherence measures. Collectively,dramatic changes in the relative LFP power and coherence in the thalamostriatal pathway may underlie the dysfunction of the basal ganglia-thalamocortical network circuits in PD, contributing to some of the motor and non-motor symptoms of the disease.
The thalamostriatal pathway is implicated in Parkinson's disease(PD); however, PD-related changes in the relationship between oscillatory activity in the centromedian-parafascicular complex(CM/Pf, or the Pf in rodents) and the dorsal striatum(DS) remain unclear.Therefore, we simultaneously recorded local field potentials(LFPs) in both the Pf and DS of hemiparkinsonian and control rats during epochs of rest or treadmill walking. The dopamine-lesioned rats showed increased LFP power in the beta band(12 Hz–35 Hz) in the Pf and DS during both epochs, but decreased LFP power in the delta(0.5 Hz–3 Hz) band in the Pf during rest epochs and in the DS during both epochs, compared to control rats. In addition,exaggerated low gamma(35 Hz–70 Hz) oscillations after dopamine loss were restricted to the Pf regardless of the behavioral state. Furthermore, enhanced synchronization of LFP oscillations was found between the Pf and DS after the dopamine lesion. Significant increases occurred in the mean coherence in both theta(3 Hz–7 Hz) and beta bands,and a significant increase was also noted in the phase coherence in the beta band between the Pf and DS during rest epochs. During the treadmill walking epochs, significant increases were found in both the alpha(7 Hz–12 Hz)and beta bands for two coherence measures. Collectively,dramatic changes in the relative LFP power and coherence in the thalamostriatal pathway may underlie the dysfunction of the basal ganglia-thalamocortical network circuits in PD, contributing to some of the motor and non-motor symptoms of the disease.
The thalamostriatal pathway is implicated in Parkinson's disease(PD); however, PD-related changes in the relationship between oscillatory activity in the centromedian-parafascicular complex(CM/Pf, or the Pf in rodents) and the dorsal striatum(DS) remain unclear.Therefore, we simultaneously recorded local field potentials(LFPs) in both the Pf and DS of hemiparkinsonian and control rats during epochs of rest or treadmill walking. The dopamine-lesioned rats showed increased LFP power in the beta band(12 Hz–35 Hz) in the Pf and DS during both epochs, but decreased LFP power in the delta(0.5 Hz–3 Hz) band in the Pf during rest epochs and in the DS during both epochs, compared to control rats. In addition,exaggerated low gamma(35 Hz–70 Hz) oscillations after dopamine loss were restricted to the Pf regardless of the behavioral state. Furthermore, enhanced synchronization of LFP oscillations was found between the Pf and DS after the dopamine lesion. Significant increases occurred in the mean coherence in both theta(3 Hz–7 Hz) and beta bands,and a significant increase was also noted in the phase coherence in the beta band between the Pf and DS during rest epochs. During the treadmill walking epochs, significant increases were found in both the alpha(7 Hz–12 Hz)and beta bands for two coherence measures. Collectively,dramatic changes in the relative LFP power and coherence in the thalamostriatal pathway may underlie the dysfunction of the basal ganglia-thalamocortical network circuits in PD, contributing to some of the motor and non-motor symptoms of the disease.
引文
1.Thenganatt MA,Jankovic J.Parkinson disease subtypes.JAMANeurol 2014,71:499-504.
2.Klingelhoefer L,Reichmann H.Pathogenesis of Parkinson disease-the gut-brain axis and environmental factors.Nat Rev Neurol 2015,11:625-636.
3.Hornykiewicz O,Kish SJ.Biochemical pathophysiology of Parkinson’s disease.Adv Neurol 1987,45:19-34.
4.Li S,Le W.Biomarker discovery in Parkinson’s disease:present challenges and future opportunities.Neurosci Bull 2017,33:481-482.
5.Galvan A,Devergnas A,Wichmann T.Alterations in neuronal activity in basal ganglia-thalamocortical circuits in the parkinsonian state.Front Neuroanat 2015,9:5.
6.Singh A,Mewes K,Gross RE,DeLong MR,Obeso JA,Papa SM.Human striatal recordings reveal abnormal discharge of projection neurons in Parkinson’s disease.Proc Natl Acad Sci U S A2016,113:9629-9634.
7.Singh A,Liang L,Kaneoke Y,Cao X,Papa SM.Dopamine regulates distinctively the activity patterns of striatal output neurons in advanced parkinsonian primates.J Neurophysiol 2015,113:1533-1544.
8.Sharott A,Vinciati F,Nakamura KC,Magill PJ.A population of indirect pathway striatal projection neurons is selectively entrained to Parkinsonian beta oscillations.J Neurosci 2017,37:9977-9998.
9.Costa RM,Lin SC,Sotnikova TD,Cyr M,Gainetdinov RR,Caron MG,et al.Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction.Neuron 2006,52:359-369.
10.Burkhardt JM,Jin X,Costa RM.Dissociable effects of dopamine on neuronal firing rate and synchrony in the dorsal striatum.Front Integr Neurosci 2009,3:28.
11.Lemaire N,Hernandez LF,Hu D,Kubota Y,Howe MW,Graybiel AM.Effects of dopamine depletion on LFP oscillations in striatum are task-and learning-dependent and selectively reversed by L-DOPA.Proc Natl Acad Sci U S A 2012,109:18126-18131.
12.Smith Y,Galvan A,Ellender TJ,Doig N,Villalba RM,HuertaOcampo I,et al.The thalamostriatal system in normal and diseased states.Front Syst Neurosci 2014,8:5.
13.Henderson JM,Carpenter K,Cartwright H,Halliday GM.Degeneration of the centre median-parafascicular complex in Parkinson’s disease.Ann Neurol 2000,47:345-352.
14.Henderson JM,Carpenter K,Cartwright H,Halliday GM.Loss of thalamic intralaminar nuclei in progressive supranuclear palsy and Parkinson’s disease:clinical and therapeutic implications.Brain 2000,123:1410-1421.
15.Villalba RM,Wichmann T,Smith Y.Neuronal loss in the caudal intralaminar thalamic nuclei in a primate model of Parkinson’s disease.Brain Struct Funct 2014,219:381-394.
16.Parr-Brownlie LC,Poloskey SL,Bergstrom DA,Walters JR.Parafascicular thalamic nucleus activity in a rat model of Parkinson’s disease.Exp Neurol 2009,217:269-281.
17.Yan W,Zhang QJ,Liu J,Wang T,Wang S,Liu X,et al.The neuronal activity of thalamic parafascicular nucleus is conversely regulated by nigrostriatal pathway and pedunculopontine nucleus in the rat.Brain Res 2008,1240:204-212.
18.Ni ZG,Gao DM,Benabid AL,Benazzouz A.Unilateral lesion of the nigrostriatal pathway induces a transient decrease of firing rate with no change in the firing pattern of neurons of the parafascicular nucleus in the rat.Neuroscience 2000,101:993-999.
19.Kempf F,Brucke C,Salih F,Trottenberg T,Kupsch A,Schneider GH,et al.Gamma activity and reactivity in human thalamic local field potentials.Eur J Neurosci 2009,29:943-953.
20.Wang M,Qu QY,He TT,Li M,Song ZM,Chen FY,et al.Distinct temporal spike and local field potential activities in the thalamic parafascicular nucleus of Parkinsonian rats during rest and limb movement.Neuroscience 2016,330:57-71.
21.Aceves Buendia JJ,Tiroshi L,Chiu WH,Goldberg JA.Selective remodeling of glutamatergic transmission to striatal cholinergic interneurons after dopamine depletion.Eur J Neurosci 2017.https://doi.org/10.1111/ejn.13715.
22.Parker PR,Lalive AL,Kreitzer AC.Pathway-specific remodeling of thalamostriatal synapses in Parkinsonian mice.Neuron 2016,89:734-740.
23.Raju DV,Ahern TH,Shah DJ,Wright TM,Standaert DG,Hall RA,et al.Differential synaptic plasticity of the corticostriatal and thalamostriatal systems in an MPTP-treated monkey model of parkinsonism.Eur J Neurosci 2008,27:1647-1658.
24.Caparros-Lefebvre D,Blond S,Feltin MP,Pollak P,Benabid AL.Improvement of levodopa induced dyskinesias by thalamic deep brain stimulation is related to slight variation in electrode placement:possible involvement of the centre median and parafascicularis complex.J Neurol Neurosurg Psychiatry 1999,67:308-314.
25.Stefani A,Peppe A,Pierantozzi M,Galati S,Moschella V,Stanzione P,et al.Multi-target strategy for Parkinsonian patients:the role of deep brain stimulation in the centromedian-parafascicularis complex.Brain Res Bull 2009,78:113-118.
26.Kerkerian-Le Goff L,Bacci JJ,Jouve L,Melon C,Salin P.Impact of surgery targeting the caudal intralaminar thalamic nuclei on the pathophysiological functioning of basal ganglia in a rat model of Parkinson’s disease.Brain Res Bull 2009,78:80-84.
27.Peppe A,Gasbarra A,Stefani A,Chiavalon C,Pierantozzi M,Fermi E,et al.Deep brain stimulation of CM/PF of thalamus could be the new elective target for tremor in advanced Parkinson’s disease?Parkinsonism Relat Disord 2008,14:501-504.
28.Jouve L,Salin P,Melon C,Kerkerian-Le Goff L.Deep brain stimulation of the center median-parafascicular complex of the thalamus has efficient anti-parkinsonian action associated with widespread cellular responses in the basal ganglia network in a rat model of Parkinson’s disease.J Neurosci 2010,30:9919-9928.
29.Wang M,Li M,Geng XW,Song ZM,Albers HE,Yang MQ,et al.Altered neuronal activity in the primary motor cortex and globus pallidus after dopamine depletion in rats.J Neurol Sci2015,348:231-240.
30.Paxino.G,Watson C.The Rat Brain Atlas.San Diego,California:Academic Press,1986.
31.Womelsdorf T,Schoffelen JM,Oostenveld R,Singer W,Desimone R,Engel AK,et al.Modulation of neuronal interactions through neuronal synchronization.Science 2007,316:1609-1612.
32.Moran RJ,Mallet N,Litvak V,Dolan RJ,Magill PJ,Friston KJ,et al.Alterations in brain connectivity underlying beta oscillations in Parkinsonism.PLoS Comput Biol 2011,7:e1002124.
33.Stein E,Bar-Gad I.Beta oscillations in the cortico-basal ganglia loop during parkinsonism.Exp Neurol 2013,245:52-59.
34.Singh A.Oscillatory activity in the cortico-basal ganglia-thalamic neural circuits in Parkinson’s disease.Eur J Neurosci 2018,48:2869-2878.
35.Jenkinson N,Kuhn AA,Brown P.Gamma oscillations in the human basal ganglia.Exp Neurol 2013,245:72-76.
36.Weinberger M,Hutchison WD,Lozano AM,Hodaie M,Dostrovsky JO.Increased gamma oscillatory activity in the subthalamic nucleus during tremor in Parkinson’s disease patients.J Neurophysiol 2009,101:789-802.
37.Rubin JE,McIntyre CC,Turner RS,Wichmann T.Basal ganglia activity patterns in parkinsonism and computational modeling of their downstream effects.Eur J Neurosci 2012,36:2213-2228.
38.Brazhnik E,Novikov N,McCoy AJ,Cruz AV,Walters JR.Functional correlates of exaggerated oscillatory activity in basal ganglia output in hemiparkinsonian rats.Exp Neurol 2014,261:563-577.
39.Kondabolu K,Roberts EA,Bucklin M,McCarthy MM,Kopell N,Han X.Striatal cholinergic interneurons generate beta and gamma oscillations in the corticostriatal circuit and produce motor deficits.Proc Natl Acad Sci U S A 2016,113:E3159-3168.
2.Klingelhoefer L,Reichmann H.Pathogenesis of Parkinson disease-the gut-brain axis and environmental factors.Nat Rev Neurol 2015,11:625-636.
3.Hornykiewicz O,Kish SJ.Biochemical pathophysiology of Parkinson’s disease.Adv Neurol 1987,45:19-34.
4.Li S,Le W.Biomarker discovery in Parkinson’s disease:present challenges and future opportunities.Neurosci Bull 2017,33:481-482.
5.Galvan A,Devergnas A,Wichmann T.Alterations in neuronal activity in basal ganglia-thalamocortical circuits in the parkinsonian state.Front Neuroanat 2015,9:5.
6.Singh A,Mewes K,Gross RE,DeLong MR,Obeso JA,Papa SM.Human striatal recordings reveal abnormal discharge of projection neurons in Parkinson’s disease.Proc Natl Acad Sci U S A2016,113:9629-9634.
7.Singh A,Liang L,Kaneoke Y,Cao X,Papa SM.Dopamine regulates distinctively the activity patterns of striatal output neurons in advanced parkinsonian primates.J Neurophysiol 2015,113:1533-1544.
8.Sharott A,Vinciati F,Nakamura KC,Magill PJ.A population of indirect pathway striatal projection neurons is selectively entrained to Parkinsonian beta oscillations.J Neurosci 2017,37:9977-9998.
9.Costa RM,Lin SC,Sotnikova TD,Cyr M,Gainetdinov RR,Caron MG,et al.Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction.Neuron 2006,52:359-369.
10.Burkhardt JM,Jin X,Costa RM.Dissociable effects of dopamine on neuronal firing rate and synchrony in the dorsal striatum.Front Integr Neurosci 2009,3:28.
11.Lemaire N,Hernandez LF,Hu D,Kubota Y,Howe MW,Graybiel AM.Effects of dopamine depletion on LFP oscillations in striatum are task-and learning-dependent and selectively reversed by L-DOPA.Proc Natl Acad Sci U S A 2012,109:18126-18131.
12.Smith Y,Galvan A,Ellender TJ,Doig N,Villalba RM,HuertaOcampo I,et al.The thalamostriatal system in normal and diseased states.Front Syst Neurosci 2014,8:5.
13.Henderson JM,Carpenter K,Cartwright H,Halliday GM.Degeneration of the centre median-parafascicular complex in Parkinson’s disease.Ann Neurol 2000,47:345-352.
14.Henderson JM,Carpenter K,Cartwright H,Halliday GM.Loss of thalamic intralaminar nuclei in progressive supranuclear palsy and Parkinson’s disease:clinical and therapeutic implications.Brain 2000,123:1410-1421.
15.Villalba RM,Wichmann T,Smith Y.Neuronal loss in the caudal intralaminar thalamic nuclei in a primate model of Parkinson’s disease.Brain Struct Funct 2014,219:381-394.
16.Parr-Brownlie LC,Poloskey SL,Bergstrom DA,Walters JR.Parafascicular thalamic nucleus activity in a rat model of Parkinson’s disease.Exp Neurol 2009,217:269-281.
17.Yan W,Zhang QJ,Liu J,Wang T,Wang S,Liu X,et al.The neuronal activity of thalamic parafascicular nucleus is conversely regulated by nigrostriatal pathway and pedunculopontine nucleus in the rat.Brain Res 2008,1240:204-212.
18.Ni ZG,Gao DM,Benabid AL,Benazzouz A.Unilateral lesion of the nigrostriatal pathway induces a transient decrease of firing rate with no change in the firing pattern of neurons of the parafascicular nucleus in the rat.Neuroscience 2000,101:993-999.
19.Kempf F,Brucke C,Salih F,Trottenberg T,Kupsch A,Schneider GH,et al.Gamma activity and reactivity in human thalamic local field potentials.Eur J Neurosci 2009,29:943-953.
20.Wang M,Qu QY,He TT,Li M,Song ZM,Chen FY,et al.Distinct temporal spike and local field potential activities in the thalamic parafascicular nucleus of Parkinsonian rats during rest and limb movement.Neuroscience 2016,330:57-71.
21.Aceves Buendia JJ,Tiroshi L,Chiu WH,Goldberg JA.Selective remodeling of glutamatergic transmission to striatal cholinergic interneurons after dopamine depletion.Eur J Neurosci 2017.https://doi.org/10.1111/ejn.13715.
22.Parker PR,Lalive AL,Kreitzer AC.Pathway-specific remodeling of thalamostriatal synapses in Parkinsonian mice.Neuron 2016,89:734-740.
23.Raju DV,Ahern TH,Shah DJ,Wright TM,Standaert DG,Hall RA,et al.Differential synaptic plasticity of the corticostriatal and thalamostriatal systems in an MPTP-treated monkey model of parkinsonism.Eur J Neurosci 2008,27:1647-1658.
24.Caparros-Lefebvre D,Blond S,Feltin MP,Pollak P,Benabid AL.Improvement of levodopa induced dyskinesias by thalamic deep brain stimulation is related to slight variation in electrode placement:possible involvement of the centre median and parafascicularis complex.J Neurol Neurosurg Psychiatry 1999,67:308-314.
25.Stefani A,Peppe A,Pierantozzi M,Galati S,Moschella V,Stanzione P,et al.Multi-target strategy for Parkinsonian patients:the role of deep brain stimulation in the centromedian-parafascicularis complex.Brain Res Bull 2009,78:113-118.
26.Kerkerian-Le Goff L,Bacci JJ,Jouve L,Melon C,Salin P.Impact of surgery targeting the caudal intralaminar thalamic nuclei on the pathophysiological functioning of basal ganglia in a rat model of Parkinson’s disease.Brain Res Bull 2009,78:80-84.
27.Peppe A,Gasbarra A,Stefani A,Chiavalon C,Pierantozzi M,Fermi E,et al.Deep brain stimulation of CM/PF of thalamus could be the new elective target for tremor in advanced Parkinson’s disease?Parkinsonism Relat Disord 2008,14:501-504.
28.Jouve L,Salin P,Melon C,Kerkerian-Le Goff L.Deep brain stimulation of the center median-parafascicular complex of the thalamus has efficient anti-parkinsonian action associated with widespread cellular responses in the basal ganglia network in a rat model of Parkinson’s disease.J Neurosci 2010,30:9919-9928.
29.Wang M,Li M,Geng XW,Song ZM,Albers HE,Yang MQ,et al.Altered neuronal activity in the primary motor cortex and globus pallidus after dopamine depletion in rats.J Neurol Sci2015,348:231-240.
30.Paxino.G,Watson C.The Rat Brain Atlas.San Diego,California:Academic Press,1986.
31.Womelsdorf T,Schoffelen JM,Oostenveld R,Singer W,Desimone R,Engel AK,et al.Modulation of neuronal interactions through neuronal synchronization.Science 2007,316:1609-1612.
32.Moran RJ,Mallet N,Litvak V,Dolan RJ,Magill PJ,Friston KJ,et al.Alterations in brain connectivity underlying beta oscillations in Parkinsonism.PLoS Comput Biol 2011,7:e1002124.
33.Stein E,Bar-Gad I.Beta oscillations in the cortico-basal ganglia loop during parkinsonism.Exp Neurol 2013,245:52-59.
34.Singh A.Oscillatory activity in the cortico-basal ganglia-thalamic neural circuits in Parkinson’s disease.Eur J Neurosci 2018,48:2869-2878.
35.Jenkinson N,Kuhn AA,Brown P.Gamma oscillations in the human basal ganglia.Exp Neurol 2013,245:72-76.
36.Weinberger M,Hutchison WD,Lozano AM,Hodaie M,Dostrovsky JO.Increased gamma oscillatory activity in the subthalamic nucleus during tremor in Parkinson’s disease patients.J Neurophysiol 2009,101:789-802.
37.Rubin JE,McIntyre CC,Turner RS,Wichmann T.Basal ganglia activity patterns in parkinsonism and computational modeling of their downstream effects.Eur J Neurosci 2012,36:2213-2228.
38.Brazhnik E,Novikov N,McCoy AJ,Cruz AV,Walters JR.Functional correlates of exaggerated oscillatory activity in basal ganglia output in hemiparkinsonian rats.Exp Neurol 2014,261:563-577.
39.Kondabolu K,Roberts EA,Bucklin M,McCarthy MM,Kopell N,Han X.Striatal cholinergic interneurons generate beta and gamma oscillations in the corticostriatal circuit and produce motor deficits.Proc Natl Acad Sci U S A 2016,113:E3159-3168.