Globus Pallidus Externus Neurons Expressing parvalbumin Interconnect the Subthalamic Nucleus and Striatal Interneurons

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Saunders, Arpiar ^a   Huang, Kee Wui ^a   Sabatini, Bernardo Luis ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN NERVE CELL; BRAIN SLICE; CONTROLLED STUDY; CORPUS STRIATUM; FAST FIRING SPONTANEOUS ACTIVITY; FEMALE; GLOBUS PALLIDUS; GLOBUS PALLIDUS EXTERNUS; INTERNEURON; MALE; MOUSE; NERVE CELL NETWORK; NERVE FIBER; NERVE TRACT; NONHUMAN; OPTOGENETICS; PALLIDOSTRIATAL AXON; PROTEIN EXPRESSION; SPINY PROJECTION NEURON; SUBSTANTIA NIGRA PARS COMPACTA; SUBSTANTIA NIGRA PARS RETICULATA; SUBTHALAMIC NUCLEUS; THALAMUS; TRANSGENIC MOUSE; VIRUS RECOMBINANT; ANIMAL; AXON; BIOSYNTHESIS; BRAIN MAPPING; CYTOLOGY; GENETICS; METABOLISM; SYNAPSE;

ANIMALS; AXONS; BRAIN MAPPING; GLOBUS PALLIDUS; MICE; MICE, TRANSGENIC; PARVALBUMINS; SUBTHALAMIC NUCLEUS; SYNAPSES;

EID: 84960968618     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0149798     Document Type: Article

References (58)

1. Tepper JM, Bolam JP. Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol. 2004; 14: 685-692. PMID: 15582369
2. Chang HT, Wilson CJ, Kitai ST. Single neostriatal efferent axons in the globus pallidus: A light and electron microscopic study. Science. 1981; 213: 915-918. PMID: 7256286
3. Gertler TS, Chan CS, Surmeier DJ. Dichotomous Anatomical Properties of Adult Striatal Medium Spiny Neurons. J Neurosci. 2008; 28: 10814-10824. doi: 10.1523/JNEUROSCI.2660-08.2008 PMID: 18945889
4. Gerfen CR. The neostriatal mosaic: Multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci. 1992; 15: 285-320. PMID: 1575444
5. Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989; 12: 366-375. PMID: 2479133
6. Smith Y, Bevan MD, Shink E, Bolam JP. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience. 1998; 86: 353-387. PMID: 9881853
7. Cazorla M, De Carvalho FD, Chohan MO, Shegda M, Chuhma N, Rayport S, et al. Dopamine D2 Receptors Regulate the Anatomical and Functional Balance of Basal Ganglia Circuitry. Neuron. 2014; 81: 153-164. doi: 10.1016/j.neuron.2013.10.041 PMID: 24411738
8. Taverna S, Ilijic E, Surmeier DJ. Recurrent Collateral Connections of Striatal Medium Spiny Neurons Are Disrupted in Models of Parkinson's Disease. J Neurosci. 2008; 28: 5504-5512. doi: 10.1523/JNEUROSCI.5493-07.2008 PMID: 18495884
9. Cui G, Jun SB, Jin X, Pham MD, Vogel SS, Lovinger DM, et al. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature. 2014; 494: 238-242.
10. Jin X, Tecuapetla F, Costa RM. Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences. Nat Neuro. 2014; 17: 423-430.
11. Oldenburg IA, Sabatini BL. Antagonistic but Not Symmetric Regulation of Primary Motor Cortex by Basal Ganglia Direct and Indirect Pathways. Neuron. 2015; 86: 1174-1181. doi: 10.1016/j.neuron. 2015.05.008 PMID: 26050037
12. Kravitz AV, Freeze BS, Parker PRL, Kay K, Thwin MT, Deisseroth K, et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature. 2010; 466: 622-626. doi: 10. 1038/nature09159 PMID: 20613723
13. Kozorovitskiy Y, Saunders A, Johnson CA, Lowell BB, Sabatini BL. Recurrent network activity drives striatal synaptogenesis. Nature. 2012; 485: 646-650. doi: 10.1038/nature11052 PMID: 22660328
14. Alexi T, Borlongan CV, Faull RL, Williams CE, Clark RG, Gluckman PD, et al. Neuroprotective strategies for basal ganglia degeneration: Parkinson's and Huntington's diseases. Prog Neurobiol. 2000; 60: 409-470. PMID: 10697073
15. Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature. 2012; 489: 391-399. doi: 10.1038/nature11405 PMID: 22996553
16. Smith Y, Parent A, Seguela P, Descarries L. Distribution of GABA-immunoreactive neurons in the basal ganglia of the squirrel monkey (Saimiri sciureus). J Comp Neurol. 1987; 259: 50-64. PMID: 3294929
17. Sadek AR, Magill PJ, Bolam JP. A single-cell analysis of intrinsic connectivity in the rat globus pallidus. J Neurosci. 2007; 27: 6352-6362. PMID: 17567796
18. Falls WM, Park MR, Kitai ST. An intracellular HRP study of the rat globus pallidus. II. Fine structural characteristics and synaptic connections of medially located large GP neurons. J Comp Neurology. 1983; 221: 229-245.
19. Chan CS, Shigemoto R, Mercer JN, Surmeier DJ. HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J Neurosci. 2004; 24: 9921-9932. PMID: 15525777
20. DeLong MR. Activity of pallidal neurons during movement. J Neurophysiol. 1971; 34: 414-427. PMID: 4997823
21. Sato F, Lavallée P, Lévesque M, Parent A. Single-axon tracing study of neurons of the external segment of the globus pallidus in primate. J Comp Neurology. 2000; 417: 17-31.
22. Smith Y, Bolam JP. The output neurones and the dopaminergic neurones of the substantia nigra receive a GABA-containing input from the globus pallidus in the rat. J Comp Neurol. 1990; 296: 47-64. PMID: 1694189
23. Cornwall J, Cooper JD, Phillipson OT. Projections to the rostral reticular thalamic nucleus in the rat. Exp Brain Res. 1990; 80: 157-171. PMID: 2358025
24. Gasca-Martinez D, Hernandez A, Sierra A, Valdiosera R, Anaya-Martinez V, Floran B, et al. Dopamine inhibits GABA transmission from the globus pallidus to the thalamic reticular nucleus via presynaptic D4 receptors. Neuroscience. 2010; 169: 1672-1681. doi: 10.1016/j.neuroscience.2010.05.048 PMID: 20561570
25. Mastro KJ, Bouchard RS, Holt HAK, Gittis AH. Transgenic Mouse Lines Subdivide External Segment of the Globus Pallidus (GPe) Neurons and Reveal Distinct GPe Output Pathways. J Neurosci. 2014; 34: 2087-2099. doi: 10.1523/JNEUROSCI.4646-13.2014 PMID: 24501350
26. Grove EA, Domesick VB, Nauta WJ. Light microscopic evidence of striatal input to intrapallidal neurons of cholinergic cell group Ch4 in the rat: A study employing the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res. 1986; 367: 379-384. PMID: 3697714
27. Henderson Z. The projection from the striatum to the nucleus basalis in the rat: An electron microscopic study. Neuroscience. 1997; 78: 943-955. PMID: 9174063
28. Saunders A, Oldenburg IA, Berezovskii VK, Johnson CA, Kingery ND, Elliott HL, et al. A direct GABAergic output from the basal ganglia to frontal cortex. Nature. 2015; 521: 85-89. doi: 10.1038/nature14179 PMID: 25739505
29. Chen MC, Ferrari L, Sacchet MD, Foland-Ross LC, Qiu M-H, Gotlib IH, et al. Identification of a direct GABAergic pallidocortical pathway in rodents. Eur J Neurosci. 2015; 41: 748-759. doi: 10.1111/ejn. 12822 PMID: 25581560
30. Tkatch T, Baranauskas G, Surmeier DJ. Basal forebrain neurons adjacent to the globus pallidus coexpress GABAergic and cholinergic marker mRNAs. Neuroreport. 1998; 9: 1935-1939. PMID: 9674570
31. Kita H. Globus pallidus external segment. Prog Brain Res. 2007; 160: 111-133. PMID: 17499111
32. Bevan MD, Magill PJ, Terman D, Bolam JP, Wilson CJ. Move to the rhythm: Oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci. 2002; 25: 525-531. PMID: 12220881
33. Nambu A, Llina R. Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol. 1994; 72: 1127-1139. PMID: 7807199
34. Nambu A, Llinás R. Morphology of globus pallidus neurons: Its correlation with electrophysiology in guinea pig brain slices. J Comp Neurol. 1997; 377: 85-94. PMID: 8986874
35. Cooper AJ, Stanford IM. Electrophysiological and morphological characteristics of three subtypes of rat globus pallidus neurone in vitro. J Physiol. 2000; 527 Pt 2: 291-304. PMID: 10970430
36. Dodson PD, Larvin JT, Duffell JM, Garas FN, Doig NM, Kessaris N, et al. Distinct Developmental Origins Manifest in the Specialized Encoding of Movement by Adult Neurons of the External Globus Pallidus. Neuron. 2015; 86: 501-513. doi: 10.1016/j.neuron.2015.03.007 PMID: 25843402
37. Abdi A, Mallet N, Mohamed FY, Sharott A, Dodson PD, Nakamura KC, et al. Prototypic and Arkypallidal Neurons in the Dopamine-Intact External Globus Pallidus. J Neurosci. 2015; 35: 6667-6688. doi: 10. 1523/JNEUROSCI.4662-14.2015 PMID: 25926446
38. Hernandez VM, Hegeman DJ, Cui Q, Kelver DA, Fiske MP, Glajch KE, et al. Parvalbumin+ Neurons and Npas1+ Neurons Are Distinct Neuron Classes in the Mouse External Globus Pallidus. J Neurosci. 2015; 35: 11830-11847. doi: 10.1523/JNEUROSCI.4672-14.2015 PMID: 26311767
39. Kita H. Parvalbumin-immunopositive neurons in rat globus pallidus: A light and electron microscopic study. Brain Res. 1994; 657: 31-41. PMID: 7820633
40. Mallet N, Micklem BR, Henny P, Brown MT, Williams C, Bolam JP, et al. Dichotomous Organization of the External Globus Pallidus. 2012; 74: 1075-1086.
41. Fujiyama F, Nakano T, Matsuda W, Furuta T, Udagawa J, Kaneko T. A single-neuron tracing study of arkypallidal and prototypic neurons in healthy rats. Brain Structure and Function. 2015 (published online: Doi: 10.1007/s00429-015-1152-2).
42. Hoover BR, Marshall JF. Further characterization of preproenkephalin mRNA-containing cells in the rodent globus pallidus. Neuroscience. 2002; 111: 111-125. PMID: 11955716
43. Staines WA, Fibiger HC. Collateral projections of neurons of the rat globus pallidus to the striatum and substantia nigra. Exp Brain Res. 1984; 56: 217-220. PMID: 6479259
44. Gage GJ, Stoetzner CR, Wiltschko AB, Berke JD. Selective Activation of Striatal Fast-Spiking Interneurons during Choice Execution. 2010; 67: 466-479.
45. Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, Ladle DR, et al. A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling. Plos Biol. 2005; 3: E159. PMID: 15836427
46. Saunders A, Johnson CA, Sabatini BL. Novel recombinant adeno-associated viruses for Cre activated and inactivated transgene expression in neurons. Front Neural Circuits. 2012; 6, 47 doi: 10.3389/fncir. 2012.00047 PMID: 22866029
47. Wickersham IR, Sullivan HA, Seung HS. Production of glycoprotein-deleted rabies viruses for monosynaptic tracing and high-level gene expression in neurons. Nat Protoc. 2010; 5: 595-606. doi: 10. 1038/nprot.2009.248 PMID: 20203674
48. Bennett BD, Bolam JP. Localisation of parvalbumin-immunoreactive structures in primate caudateputamen. J Comp Neurol. 1994; 347: 340-356. PMID: 7822489
49. Castle MJ, Gershenson ZT, Giles AR, Holzbaur ELF, Wolfe JH. Adeno-Associated Virus Serotypes 1, 8, and 9 Share Conserved Mechanisms for Anterograde and Retrograde Axonal Transport. Hum Gene Ther. 2014; 25: 705-720. doi: 10.1089/hum.2013.189 PMID: 24694006
50. Miyamichi K, Shlomai-Fuchs Y, Shu M, Weissbourd BC, Luo L, Mizrahi A. Dissecting Local Circuits: Parvalbumin Interneurons Underlie Broad Feedback Control of Olfactory Bulb Output. Neuron. 2013; 80: 1232-1245. doi: 10.1016/j.neuron.2013.08.027 PMID: 24239125
51. Ibanez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koós T, Tepper JM. A Novel Functionally Distinct Subtype of Striatal Neuropeptide Y Interneuron. J Neurosci. 2011; 31: 16757-16769. doi: 10.1523/JNEUROSCI.2628-11.2011 PMID: 22090502
52. Bevan MD, Booth PA, Eaton SA, Bolam JP. Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J Neurosci. 1998; 18: 9438-9452. PMID: 9801382
53. Kita H, Kita T. Number, origins, and chemical types of rat pallidostriatal projection neurons. J Comp Neurol. 2001; 437: 438-448. PMID: 11503145
54. Dejean C, Arbuthnott G, Wickens JR, Le Moine C, Boraud T, Hyland BI. Power Fluctuations in Beta and Gamma Frequencies in Rat Globus Pallidus: ASSOCIATION WITH Specific Phases of Slow Oscillations and Differential Modulation by Dopamine D1 and D2 Receptors. J Neurosci. 2011; 31: 6098-6107. doi: 10.1523/JNEUROSCI.3311-09.2011 PMID: 21508235
55. Schmidt R, Leventhal DK, Mallet N, Chen F, Berke JD. Canceling actions involves a race between basal ganglia pathways. Nat Neuro. 2013; 16: 1118-1124.
56. Gittis AH, Nelson AB, Thwin MT, Palop JJ, Kreitzer AC. Distinct Roles of GABAergic Interneurons in the Regulation of Striatal Output Pathways. J Neurosci. 2010; 30: 2223-2234. doi: 10.1523/JNEUROSCI.4870-09.2010 PMID: 20147549
57. Person AL, Raman IM. Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei. Nature. 2012; 481: 502-505.
58. Macosko EZ, Basu A, Satija R, Nemesh J, Shekhar K, Goldman M, et al. Highly Parallel Genome-wide Expression Profiling of Individual Cells Using Nanoliter Droplets. Cell. 2015; 161: 1202-1214. doi: 10. 1016/j.cell.2015.05.002 PMID: 26000488