Striatal Cholinergic Interneurons Control Motor Behavior and Basal Ganglia Function in Experimental Parkinsonism

Cell Reports

Volumn 13, Issue 4, 2015, Pages 657-666

  Maurice, Nicolas ^a   Liberge, Martine ^b   Jaouen, Florence ^a   Ztaou, Samira ^b   Hanini, Marwa ^a   Camon, Jeremy ^b   Deisseroth, Karl ^c   Amalric, Marianne ^b   Kerkerian Le Goff, Lydia ^a   Beurrier, Corinne ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN ASYMMETRY; BRAIN FUNCTION; CATECHOLAMINE DEPLETION; CHOLINERGIC NERVE; CONTROLLED STUDY; DIRECT PATHWAY; EXPERIMENTAL PARKINSONISM; INDIRECT PATHWAY; INTERNEURON; LOCOMOTION; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NERVE CONDUCTION; NERVE EXCITABILITY; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROANATOMY; NEUROMODULATION; NEUROPATHOLOGY; NEUROTRANSMISSION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; STRIATE CORTEX; SYNAPTIC MEMBRANE; ANIMAL; CORPUS STRIATUM; CYTOLOGY; DISEASE MODEL; METABOLISM; PARKINSONISM; PHYSIOLOGY;

ANIMALS; BASAL GANGLIA; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; INTERNEURONS; MICE; PARKINSONIAN DISORDERS;

EID: 84945548465     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.09.034     Document Type: Article

References (39)

1. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
2. Aosaki T., Graybiel A.M., Kimura M. Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 1994, 265:412-415.
3. Barbeau A. The pathogenesis of Parkinson's disease: a new hypothesis. Can. Med. Assoc. J. 1962, 87:802-807.
4. Brown P. Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson's disease. Mov. Disord. 2003, 18:357-363.
5. Calabresi P., Picconi B., Tozzi A., Ghiglieri V., Di Filippo M. Direct and indirect pathways of basal ganglia: a critical reappraisal. Nat. Neurosci. 2014, 17:1022-1030.
6. Cui G., Jun S.B., Jin X., Pham M.D., Vogel S.S., Lovinger D.M., Costa R.M. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 2013, 494:238-242.
7. Dautan D., Huerta-Ocampo I., Witten I.B., Deisseroth K., Bolam J.P., Gerdjikov T., Mena-Segovia J. A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem. J. Neurosci. 2014, 34:4509-4518.
8. Day M., Wang Z., Ding J., An X., Ingham C.A., Shering A.F., Wokosin D., Ilijic E., Sun Z., Sampson A.R., et al. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat. Neurosci. 2006, 9:251-259.
9. Degos B., Deniau J.M., Thierry A.M., Glowinski J., Pezard L., Maurice N. Neuroleptic-induced catalepsy: electrophysiological mechanisms of functional recovery induced by high-frequency stimulation of the subthalamic nucleus. J. Neurosci. 2005, 25:7687-7696.
10. Ding J., Guzman J.N., Tkatch T., Chen S., Goldberg J.A., Ebert P.J., Levitt P., Wilson C.J., Hamm H.E., Surmeier D.J. RGS4-dependent attenuation of M4 autoreceptor function in striatal cholinergic interneurons following dopamine depletion. Nat. Neurosci. 2006, 9:832-842.
11. English D.F., Ibanez-Sandoval O., Stark E., Tecuapetla F., Buzsáki G., Deisseroth K., Tepper J.M., Koos T. GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nat. Neurosci. 2011, 15:123-130.
12. Eusebio A., Thevathasan W., Doyle Gaynor L., Pogosyan A., Bye E., Foltynie T., Zrinzo L., Ashkan K., Aziz T., Brown P. Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. J. Neurol. Neurosurg. Psychiatry 2011, 82:569-573.
13. Fieblinger T., Graves S.M., Sebel L.E., Alcacer C., Plotkin J.L., Gertler T.S., Chan C.S., Heiman M., Greengard P., Cenci M.A., Surmeier D.J. Cell type-specific plasticity of striatal projection neurons in parkinsonism and L-DOPA-induced dyskinesia. Nat. Commun. 2014, 5:5316.
14. Galarraga E., Hernández-López S., Reyes A., Miranda I., Bermudez-Rattoni F., Vilchis C., Bargas J. Cholinergic modulation of neostriatal output: a functional antagonism between different types of muscarinic receptors. J. Neurosci. 1999, 19:3629-3638.
15. Gertler T.S., Chan C.S., Surmeier D.J. Dichotomous anatomical properties of adult striatal medium spiny neurons. J. Neurosci. 2008, 28:10814-10824.
16. Goldberg J.A., Ding J.B., Surmeier D.J. Muscarinic modulation of striatal function and circuitry. Handb. Exp. Pharmacol. 2012, 208:223-241.
17. Hernández-Echeagaray E., Galarraga E., Bargas J. 3-Alpha-chloro-imperialine, a potent blocker of cholinergic presynaptic modulation of glutamatergic afferents in the rat neostriatum. Neuropharmacology 1998, 37:1493-1502.
18. Higley M.J., Gittis A.H., Oldenburg I.A., Balthasar N., Seal R.P., Edwards R.H., Lowell B.B., Kreitzer A.C., Sabatini B.L. Cholinergic interneurons mediate fast VGluT3-dependent glutamatergic transmission in the striatum. PLoS ONE 2011, 6:e19155.
19. Kravitz A.V., Freeze B.S., Parker P.R., Kay K., Thwin M.T., Deisseroth K., Kreitzer A.C. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010, 466:622-626.
20. Kreitzer A.C., Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 2007, 445:643-647.
21. Lobb C. Abnormal Bursting as a Pathophysiological Mechanism in Parkinson's Disease. Basal Ganglia 2014, 3:187-195.
22. Malenka R.C., Kocsis J.D. Presynaptic actions of carbachol and adenosine on corticostriatal synaptic transmission studied in vitro. J. Neurosci. 1988, 8:3750-3756.
23. Mallet N., Ballion B., Le Moine C., Gonon F. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J. Neurosci. 2006, 26:3875-3884.
24. Maurice N., Deniau J.M., Glowinski J., Thierry A.M. Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the cortico-nigral circuits. J. Neurosci. 1999, 19:4674-4681.
25. Nelson A.B., Hammack N., Yang C.F., Shah N.M., Seal R.P., Kreitzer A.C. Striatal cholinergic interneurons Drive GABA release from dopamine terminals. Neuron 2014, 82:63-70.
26. Pakhotin P., Bracci E. Cholinergic interneurons control the excitatory input to the striatum. J. Neurosci. 2007, 27:391-400.
27. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, San Diego. Second Edition.
28. Phelps P.E., Houser C.R., Vaughn J.E. Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: a correlated light and electron microscopic study of cholinergic neurons and synapses. J. Comp. Neurol. 1985, 238:286-307.
29. Pisani A., Bernardi G., Ding J., Surmeier D.J. Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci. 2007, 30:545-553.
30. Rivlin-Etzion M., Marmor O., Heimer G., Raz A., Nini A., Bergman H. Basal ganglia oscillations and pathophysiology of movement disorders. Curr. Opin. Neurobiol. 2006, 16:629-637.
31. Ryan L.J., Sanders D.J. Subthalamic nucleus and globus pallidus lesions alter activity in nigrothalamic neurons in rats. Brain Res. Bull. 1994, 34:19-26.
32. Sano H., Chiken S., Hikida T., Kobayashi K., Nambu A. Signals through the striatopallidal indirect pathway stop movements by phasic excitation in the substantia nigra. J. Neurosci. 2013, 33:7583-7594.
33. Shen W., Tian X., Day M., Ulrich S., Tkatch T., Nathanson N.M., Surmeier D.J. Cholinergic modulation of Kir2 channels selectively elevates dendritic excitability in striatopallidal neurons. Nat. Neurosci. 2007, 10:1458-1466.
34. Smith Y., Bevan M.D., Shink E., Bolam J.P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 1998, 86:353-387.
35. Tachibana Y., Kita H., Chiken S., Takada M., Nambu A. Motor cortical control of internal pallidal activity through glutamatergic and GABAergic inputs in awake monkeys. Eur. J. Neurosci. 2008, 27:238-253.
36. Threlfell S., Lalic T., Platt N.J., Jennings K.A., Deisseroth K., Cragg S.J. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 2012, 75:58-64.
37. Tritsch N.X., Oh W.J., Gu C., Sabatini B.L. Midbrain dopamine neurons sustain inhibitory transmission using plasma membrane uptake of GABA, not synthesis. eLife 2014, 3:e01936.
38. Wichmann T., Bergman H., Starr P.A., Subramanian T., Watts R.L., DeLong M.R. Comparison of MPTP-induced changes in spontaneous neuronal discharge in the internal pallidal segment and in the substantia nigra pars reticulata in primates. Exp. Brain Res. 1999, 125:397-409.
39. Witten I.B., Lin S.-C., Brodsky M., Prakash R., Diester I., Anikeeva P., Gradinaru V., Ramakrishnan C., Deisseroth K. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 2010, 330:1677-1681.