Number and type of synapses on the distal dendrite of a rat striatal cholinergic interneuron: A quantitative, ultrastructural study

Journal of Anatomy

Volumn 217, Issue 3, 2010, Pages 223-235

  Sizemore, Rachel J ^a   Reynolds, John N J ^a   Oorschot, Dorothy E ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Striatal cholinergic interneuron; Synapse; Three dimensional mapping; Transmission electron microscopy

Indexed keywords

CHOLINE ACETYLTRANSFERASE; MUSCARINIC RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN CORTEX; CELL COUNT; CELL DENSITY; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DENDRITE; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC AGENTS; CORPUS STRIATUM; DENDRITES; INTERNEURONS; MALE; MICROSCOPY, ELECTRON; RATS; RATS, WISTAR; RECEPTOR, MUSCARINIC M2; SYNAPSES;

MAMMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 77955367185     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2010.01264.x     Document Type: Article

References (58)

1. Alcantara AA, Mrzljak L, Jakab RL. Muscarinic m1 and m2 receptor proteins in local circuit and projection neurons of the primate striatum: anatomical evidence for cholinergic modulation of glutamatergic prefronto-striatal pathways. J Comp Neurol 2001, 434:445-460.
2. Anderson JC, Douglas RJ, Martin KAC. Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex. J Comp Neurol 1994, 341:25-38.
3. Aoki C, Pickel VM. Neuropeptide Y-containing neurons in the rat striatum: ultrastructure and cellular relations with tyrosine hydroxylase-containing terminals with astrocytes. Brain Res 1988, 459:205-225.
4. Aosaki T, Tsubokawa H, Ishisa A. Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioural sensorimotor conditioning. J Neurosci 1994, 14:3969-3984.
5. Armstrong DM, Saper CB, Levey AI. Distribution of cholinergic neurons in rat brain: demonstrated by the immunocytochemical localization of choline acetyltransferase. J Comp Neurol 1983, 216:53-68.
6. Bernard V, Normand E, Block B. Phenotypical characterization of the rat striatal neurons expressing muscarinic receptor genes. J Neurosci 1992, 12:3591-3600.
7. Bernard V, Laribi O, Levey AI. Subcellular redistribution of m2 muscarinic acetylcholine receptors in striatal interneurons in vivo after acute cholinergic stimulation. J Neurosci 1998, 18:10207-10218.
8. Bolam JP, Wainer BH, Smith AD. Characterization of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry, golgi-impregnation and electron microscopy. Neuroscience 1984, 12:711-718.
9. Bolam JP, Ingham CA, Izzo PN. Substance-P containing terminals in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain: a double immunocytochemical study in the rat. Brain Res 1986, 397:279-289.
10. Braitenberg V, Schüz A. Cortex: Statistics and Geometry of Neuronal Connectivity 1998, Berlin, Springer
11. Chang HT. Dopamine-acetylcholine interaction in the rat striatum: a dual-labeling immunocytochemical study. Brain Res Bull 1988, 21:295-304.
12. Chang HT, Kita H. Interneurons in the rat striatum: relationships between parvalbumin neurons and cholinergic neurons. Brain Res Bull 1992, 574:307-311.
13. Chen Z-L, Indyk JA, Strickland S. The hippocampal laminin matrix is dynamic and critical for neuronal survival. Mol Biol Cell 2003, 14:2665-2676.
14. Connors BW, Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 1990, 13:99-104.
15. Dimova R, Vuillet J, Nieoullon A. Ultrastructural features of the choline acetyltransferase-containing neurons and relationships with nigral dopaminergic and cortical afferent pathways in the rat striatum. Neuroscience 1993, 53:1059-1071.
16. Fino E, Deniau JM, Venance L. Cell-specific spike-timing dependent plasticity in GABAergic and cholinergic interneurons in corticostriatal rat brain slices. J Physiol 2008, 586:265-282.
17. Gray EG. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat 1959, 93:420-433.
18. Izzo PN, Bolam JP. Cholinergic synaptic input to different parts of spiny striatonigral neurons in the rat. J Comp Neurol 1988, 269:219-234.
19. Jositsch G, Papadakis T, Haberberger RV. Suitability of muscarinic acetylcholine receptor antibodies for immunohistochemistry evaluated on tissue sections of receptor gene-deficient mice. Naunyn Schmiedebergs Arch Pharmacol 2009, 279:389-395.
20. Kawaguchi Y. Physiological, morphological, and histochemical characterization of three classes of interneurons in the rat neostriatum. J Neurosci 1993, 13:4908-4923.
21. Kawaguchi Y, Wilson CJ, Augood SJ. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 1995, 18:527-535.
22. Kawaguchi Y, Aosaki T, Kubota Y. Cholinergic and GABAergic interneurons in the striatum. Jap J Psycho-pharmacol 1997, 17:87-90.
23. Kita H, Kosaka T, Heizmann CW. Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 1990, 536:1-15.
24. Kubota Y, Inagaki S, Kito S. Dopaminergic axons directly make synapses with GABAergic neurons in the rat neostriatum. Brain Res 1987, 406:147-156.
25. Lapper SR, Bolam JP. Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience 1992, 51:533-545.
26. Levey AI, Kitt CA, Simonds WF. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 1991, 11:3218-3226.
27. Levey AI, Edmunds SM, Hersch SM. Light and electron microscopic study of m2 muscarinic acetylcholine receptor in the basal forebrain of the rat. J Comp Neurol 1995, 351:339-356.
28. Ligorio M, Descarries L, Warren RA. Cholinergic innervation and thalamic input in rat nucleus accumbens. J Chem Neuroanat 2009, 37:33-45.
29. Llewellyn-Smith IJ, Pilowsky P, Minson JB. The tungstate-stabilized tetramethylbenzidine reaction for light and electron microscopic immunocytochemistry and for revealing biocytin-filled neurons. J Neurosci Methods 1993, 46:27-40.
30. Luk KC, Sadikot AF. GABA promotes survival but not proliferation of parvalbumin-immunoreactive interneurons in rodent neostriatum: an in vivo study with stereology. Neuroscience 2001, 104:93-103.
31. Martone ME, Armstrong DM, Young SJ. Ultrastructural examination of enkephalin and substance P input to cholinergic neurons within the rat neostriatum. Brain Res 1992, 594:253-262.
32. McCormick DA, Connors BW, Lighthall JW. Comparative electrophysiology of pyramidal and sparely spiny stellate neurons of the neocortex. J Neurophysiol 1985, 54:782-806.
33. McGeorge AJ, Faull RLM. Organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 1989, 29:503-537.
34. Meredith GE, Chang HT. Synaptic relationships of enkephalinergic and cholinergic neurons in the nucleus accumbens of the rat. Brain Res 1994, 667:67-76.
35. Meredith GE, Wouterlood FG. Hippocampal and midline thalamic fibres and terminals in relation to choline acetyltransferase-immunoreactive neurons in the nucleus accumbens of the rat: a light and electron microscopic study. J Comp Neurol 1990, 296:201-221.
36. Oorschot DE. 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. J Comp Neurol 1996, 366:580-599.
37. Oorschot DE, Zhang R, Wickens JR. Absolute number and three-dimensional spatial distribution of rat neostriatal large interneurons: a first and second order stereological study. 1999, Proc Xth Int Congr Stereol, pp
38. Oorschot DE, Tunstall MJ, Wickens JR. Local connectivity between striatal spiny projection neurons: a re-evalulation. The Basal Ganglia VII 2002, 421-434. Nicholson LFB, Faull RLM, In, eds, pp, New York, Kluwer Academic/Plenum Publishers
39. Partadiredja G, Miller R, Oorschot DE. The number, size, and type of axons in rat subcortical white matter on left and right sides: a stereological, ultrastructural study. J Neurocytol 2003, 32:1165-1179.
40. Paxinos G, Watson C. The Rat Brain Atlas in Stereotaxic Coordinates 1998, New York, Academic Press
41. Peters A, Palay SL, Webster HD. The Fine Structure of the Nervous System: Neurons and Their Supporting Cells 1991, New York, Oxford University Press
42. Phelps PE, Houser CR, Vaughn JE. Immunocytochemical localization of choline acetyltransferase within the rat neo-striatum: a correlated light and electron microscopic study of cholinergic neurons and synapses. J Comp Neurol 1985, 238:286-307.
43. Ramanathan S, Hanley JJ, Deniau JM. Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J Neurosci 2002, 22:8158-8169.
44. Reynolds JNJ, Wickens JR. The corticostriatal input to giant aspiny interneurons in the rat: a candidate pathway for synchronising the response to reward-related cues. Brain Res 2004, 1011:115-128.
45. Reynolds JNJ, Hyland BI, Wickens JR. Modulation of an afterhyperpolarisation by the substantia nigra induces pauses in the tonic firing of striatal cholinergic interneurons. J Neurosci 2004, 24:9870-9877.
46. Rymar VV, Sasseville R, Luk KC. Neurogenesis and stereological morphometry of calretinin-immunoreactive GABAergic interneurons of the neostriatum. J Comp Neurol 2004, 469:325-339.
47. Sharott A, Moll CKE, Engler G. Different subtypes of striatal neurons are selectively modulated by cortical oscillations. J Neurosci 2009, 29:4571-4585.
48. Sheffield EB, Quick MW, Lester RAJ. Nicotinic acetylcholine receptor subunit mRNA expression and channel function in medial habenula neurons. Neuropharmacology 2000, 39:2591-2603.
49. Song P, Sekhon HS, Fu XW. Activated cholinergic signaling provides a target in squamous cell lung carcinoma. Cancer Res 2008, 68:4693-4700.
50. Tepper JM, Bolam JP. Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol 2004, 14:685-692.
51. Thind KK, Ribak CE, Buckmaster PS. Synaptic input to dentate granule cell basal dendrites in a rat model of temporal lobe epilepsy. J Comp Neurol 2008, 509:190-202.
52. Thomas TM, Smith Y, Levey AI. Cortical inputs to m2-immunoreactive striatal interneurons in rat and monkey. Synapse 2000, 37:252-261.
53. Vuillet J, Dimova R, Neoullon A. Ultrastructural relationships between choline acetyltransferase- and neuropeptide Y-containing neurons in the rat striatum. Neuroscience 1992, 46:351-360.
54. Weiner DM, Levey AI, Brann MR. Expression of muscarinic acetylcholine and dopamine receptor nRNAs in rat basal ganglia. Proc Natl Acad Sci U S A 1990, 87:7050-7054.
55. West MJ, Østergaard K, Andreassen OA. Estimation of the number of somatostatin neurons in the striatum: an in situ hybridization study using the optical fractionator method. J Comp Neurol 1996, 370:11-22.
56. Wilson CJ, Groves PM, Kitai ST. Three-dimensional structure of dendritic spines in the rat neostriatum. J Neurosci 1983, 3:383-398.
57. Wiseman LAB, Sahin G, Maingay M. Functional convergence of dopaminergic and cholinergic input is critical for hippocampus-dependent working memory. J Neurosci 2008, 28:7797-7807.
58. Yang Z, You Y, Levison SW. Neonatal hypoxic/ischemic brain injury induces production of calretinin-expressing interneurons in the striatum. J Comp Neurol 2008, 511:19-33.