Differential expression of muscarinic acetylcholine receptors across excitatory and inhibitory cells in visual cortical areas V1 and V2 of the macaque monkey

Journal of Comparative Neurology

Volumn 499, Issue 1, 2006, Pages 49-63

  Disney, Anita A ^a   Domakonba, Kunal V ^a   Aoki, Chiye ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Cholinergic; Dual labelling; Electron microscopy; GABAergic; Immunofluorescence; Neuromodulation; Striate cortex; Ultrastructure

Indexed keywords

4 AMINOBUTYRIC ACID; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC RECEPTOR;

ANIMAL TISSUE; ARTICLE; ATTENTION; CELLULAR DISTRIBUTION; CHOLINERGIC ACTIVITY; DENDRITE; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MACACA; MALE; NERVE CELL; NERVE FIBER; NEUROANATOMY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; VISUAL CORTEX;

ANIMALS; BLOTTING, WESTERN; CELL COUNT; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MACACA FASCICULARIS; MALE; MICROSCOPY, IMMUNOELECTRON; NEURAL INHIBITION; NEURONS; RECEPTORS, MUSCARINIC; VISUAL CORTEX;

EID: 33748878752     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21096     Document Type: Article

References (83)

1. Aoki C, Kabak S. 1992. Cholinergic terminals in the cat visual cortex: ultrastructural basis for interaction with glutamate-immunoreactive neurons and other cells. Vis Neurosci 8:177-191.
2. Beaulieu C, Somogyi P. 1991. Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat. J Comp Neurol 304:666-680.
3. Beaulieu C, Kisvarday Z, Somogyi P, Cynader M, Cowey A. 1992. Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). Cereb Cortex 2:295-309.
4. Bernard V, Laribi O, Levey AI, Bloch B. 1998. Subcellular redistribution of m2 muscarinic acetylcholine receptors in striatal interneurons in vivo after acute cholinergic stimulation. J Neurosci 18:10207-10218.
5. Brann MR, Ellis J, Jorgensen H, Hill-Eubanks H, Jones SVP. 1993. Muscarinic acetylcholine receptor subtypes: localization and structure/function. Prog Brain Res 98:121-127.
6. Burette A, Zabel U, Weinberg RJ, Schmidt HH, Valtschanoff JG. 2002. Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J Neurosci 22:8961-8970.
7. Chessell IP, Francis PT, Pangalos MN, Pearson RC, Bowen DM. 1993. Localisation of muscarinic (m1) and other neurotransmitter receptors on corticofugal-projecting pyramidal neurones. Brain Res 632:86-94.
8. de Lima AD, Singer W. 1986. Cholinergic innervation of the cat striate cortex: a choline acetyltransferase immunocytochemical analysis. J Comp Neurol 250:324-338.
9. DeFelipe J. 1993. Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. Cereb Cortex 3:273-289.
10. Descarries L, Gisiger V, Steriade M. 1997. Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53:603-625.
11. Disney AA, Aoki C. 2003a. Cholinergic modulation of inhibitory network sub-elements in V1 of the macaque. Program No. POS-167, Proceedings of the Australian Neuroscience Society.
12. Disney AA, Aoki C. 2003b. Nicotinic, but not muscarinic, acetylcholine receptors are expressed by thalamic afferents and their terminals in layer IVC of macaque V1. Program No. 701.16, Washington DC: Society for Neuroscience, 2003 [online].
13. Duttaroy A, Gomeza J, Gan JW, Siddiqui N, Basile AS, Harman WD, Smith PL, Felder CC, Levey AI, Wess J. 2002. Evaluation of muscarinic agonist-induced analgesia in muscarinic acetylcholine receptor knockout mice. Mol Pharmacol 62:1084-1093.
14. Edeline JM. 2003. The thalamocortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems. Exp Brain Res 153:554-572.
15. Erisir A, Levey AI, Aoki C. 2001. Muscarinic receptor m2R distribution in the cat visual cortex: laminar distribution, relationship to GABAergic neurons, and the effect of cingulate lesions. J Comp Neurol 441:168-185.
16. Fitzpatrick D, Lund JS, Schmechel DE, Towles AC. 1987. Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. J Comp Neurol 264:73-91.
17. Fries P, Reynolds JH, Rorie AE, Desimone R. 2001. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560-1563.
18. Gil Z, Connors BW, Amitai Y. 1997. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679-686.
19. Gruber T, Muller MM, Keil A, Elbert T. 1999. Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clin Neurophysiol 110:2074-2085.
20. Gu Q. 2003. Contribution of acetylcholine to visual cortex plasticity. Neurobiol Learn Mem 80:291-301.
21. Hamilton SE, Loose MD, Qi M, Levey AI, Hille B, McKnight GS, Idzerda RL, Nathanson NM. 1997. Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. Proc Natl Acad Sci U S A 94:13311-13316.
22. Han ZY, Le Novere N, Zoli M, Hill JA, Champtiaux N, Changeux JP. 2000. Localization of nAChR subunit mRNAs in the brain of Macaca mulatta. Eur J Neurosci 12:3664-3674.
23. Hasselmo ME, Bower JM. 1992. Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J Neurophysiol 67:1222-1229.
24. Hasselmo ME, McGaughy J. 2004. High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Prog Brain Res 145:207-231.
25. Hendry SH, Schwark HD, Jones EG, Yan J. 1987. Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7:1503-1519.
26. Hsieh CY, Cruikshank SJ, Metherate R. 2000. Differential modulation of auditory thalamocortical and intracortical synaptic transmission by cholinergic agonist. Brain Res 880:51-64.
27. Hsu SM, Raine L, Fanger H. 1981. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29: 577-580.
28. Hulme EC, Lu ZL, Bee M, Curtis CA, Saldanha J. 2001. The conformational switch in muscarinic acetylcholine receptors. Life Sci 68:2495-2500.
29. Jones EG. 1993. GABAergic neurons and their role in cortical plasticity in primates. Cereb Cortex 3:361-372.
30. Jones SVP. 1993. Muscarinic receptor subtypes-modulation of ion channels. Life Sci 52:457-464.
31. Kawaguchi Y, Kubota Y. 1993. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387-396.
32. Kilgard M. 2003. Cholinergic modulation of skill learning and plasticity. Neuron 38:678-680.
33. Levey AI, Kitt CA, Simonds WF, Price DL, Brann MR. 1991. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 11:3218-3226.
34. Linster C, Cleland TA. 2002. Cholinergic modulation of sensory representations in the olfactory bulb. Neural Netw 15:709-717.
35. Linster C, Maloney M, Patil M, Hasselmo ME. 2003. Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex. Neurobiol Learn Mem 80:302-314.
36. Luck SJ, Chelazzi L, Hillyard SA, Desimone R. 1997. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J Neurophysiol 77:24-42.
37. McCormick DA. 1993. Actions of acetylcholine in the cerebral cortex and thalamus and implications for function. Prog Brain Res 98:303-308.
38. McCormick DA, Prince DA. 1985. Two types of muscarinic response to acetylcholine in mammalian cortical neurons. Proc Natl Acad Sci U S A 82:6344-6348.
39. McCormick DA, Prince DA. 1986. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol 375:169-194.
40. Mesulam MM, Mufson EJ, Levey AI, Wainer BH. 1983a. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214:170-197.
41. Mesulam MM, Mufson EJ, Wainer BH, Levey AI. 1983b. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201.
42. Metherate R, Weinberger NM. 1989. Acetylcholine produces stimulus-specific receptive field alterations in cat auditory cortex. Brain Res 480:372-377.
43. Moran J, Desimone R. 1985. Selective attention gates visual processing in the extrastriate cortex. Science 229:782-784.
44. Mrzljak L, Levey AI, Goldman-Rakic PS. 1993. Association of m1 and m2 muscarinic receptor proteins with asymmetric synapses in the primate cerebral cortex: morphological evidence for cholinergic modulation of excitatory neurotransmission. Proc Natl Acad Sci U S A 90:5194-5198.
45. Mrzljak L, Pappy M, Leranth C, Goldman-Rakic PS. 1995. Cholinergic synaptic circuitry in the macaque prefrontal cortex. J Comp Neurol 357:603-617.
46. Mrzljak L, Levey AI, Rakic P. 1996. Selective expression of m2 muscarinic receptor in the parvocellular channel of the primate visual cortex. Proc Natl Acad Sci U S A 93:7337-7340.
47. Muller CM, Singer W. 1989. Acetylcholine-induced inhibition in the cat visual cortex is mediated by a GABAergic mechanism. Brain Res 487: 335-342.
48. Pangalos MN, Davies CH, editors. 2002. Understanding G protein-coupled receptors and their role in the CNS. New York: Oxford University Press.
49. Park PS, Wells JW. 2004. Oligomeric potential of the M2 muscarinic cholinergic receptor. J Neurochem 90:537-548.
50. Platt ML, Glimcher PW. 1997. Responses of intraparietal neurons to saccadic targets and visual distractors. J Neurophysiol 78:1574-1589.
51. Rasmusson DD. 2000. The role of acetylcholine in cortical synaptic plasticity. Behav Brain Res 115:205-218.
52. Rezvani AH, Levin ED. 2001. Cognitive effects of nicotine. Biol Psychiatry 49:258-267.
53. Roberts MJ, Zinke W, Guo K, Robertson R, McDonald JS, Thiele A. 2005. Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex. J Neurophysiol 93:2062-2072.
54. Rodriguez R, Kallenbach U, Singer W, Munk MH. 2004. Short- and long-term effects of cholinergic modulation on gamma oscillations and response synchronization in the visual cortex. J Neurosci 24:10369-10378.
55. Sarter M, Bruno JP, Givens B. 2003. Attentional functions of cortical cholinergic inputs: what does it mean for learning and memory? Neurobiol Learn Mem 80:245-256.
56. Sarter M, Hasselmo ME, Bruno JP, Givens B. 2005. Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res Brain Res Rev 48:98-111.
57. Sato H, Hata Y, Masui H, Tsumoto T. 1987. A functional role of cholinergic innervation to neurons in the cat visual cortex. J Neurophysiol 58:765-780.
58. Schoneberg T, Liu J, Wess J. 1995. Plasma membrane localization and functional rescue of truncated forms of a G protein-coupled receptor. J Biol Chem 270:18000-18006.
59. Schuh TJ, Mueller GC. 1993. Estrogen receptor-dependent formation of two distinct multiprotein complexes on the human pS2 gene regulatory segment. Participation of a c-fos related protein. Receptor 3:125-143.
60. Sillito AM, Kemp JA. 1983. Cholinergic modulation of the functional organization of the cat visual cortex. Brain Res 289:143-155.
61. Smiley JF, Morrell F, Mesulam MM. 1997. Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections. Exp Neurol 144:361-368.
62. Solomon SG, Peirce JW, Lennie P. 2004. The impact of suppressive surrounds on chromatic properties of cortical neurons. J Neurosci 24:148-160.
63. Steriade M, Timofeev I, Durmuller N, Grenier F. 1998. Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30-40 Hz) spike bursts. J Neurophysiol 79:483-490.
64. 2+ channel currents in rat sensorimotor pyramidal cells via two distinct pathways. J Neurophysiol 81:72-84.
65. Stone TW. 1972a. Cholinergic mechanisms in the rat cerebral cortex. J Physiol 222:155P-156P.
66. Stone TW. 1972b. Cholinergic mechanisms in the rat somatosensory cerebral cortex. J Physiol 225:485-499.
67. Tiesinga PH, Fellous JM, Jose JV, Sejnowski TJ. 2001. Computational model of carbachol-induced delta, theta, and gamma oscillations in the hippocampus. Hippocampus 11:251-274.
68. Tiesinga PH, Fellous JM, Salinas E, Jose JV, Sejnowski TJ. 2004. Inhibitory synchrony as a mechanism for attentional gain modulation. J Physiol (Paris) 98:296-314.
69. Tigges M, Tigges J, Rees H, Rye D, Levey AI. 1997. Distribution of muscarinic cholinergic receptor proteins m1 to m4 in area 17 of normal and monocularly deprived rhesus monkeys. J Comp Neurol 388:130-145.
70. Tootell RB, Hadjikhani N, Hall EK, Marrett S, Vanduffel W, Vaughan JT, Dale AM. 1998. The retinotopy of visual spatial attention. Neuron 21:1409-1422.
71. Traub RD, Whittington MA, Colling SB, Buzsaki G, Jefferys JG. 1996. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol 493:471-484.
72. Turrini P, Casu MA, Wong TP, De Koninck Y, Ribeiro-da-Silva A, Cuello AC. 2001. Cholinergic nerve terminals establish classical synapses in the rat cerebral cortex: synaptic pattern and age-related atrophy. Neuroscience 105:277-285.
73. Umbriaco D, Watkins KC, Descarries L, Cozzari C, Hartman BK. 1994. Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J Comp Neurol 348:351-373.
74. Venter JC. 1983. Muscarinic cholinergic receptor structure. Receptor size, membrane orientation, and absence of major phylogenetic structural diversity. J Biol Chem 258:4842-4848.
75. Vreugdenhil M, Jefferys JG, Celio MR, Schwaller B. 2003. Parvalbumin-deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus. J Neurophysiol 89:1414-1422.
76. Wang Z, McCormick DA. 1993. Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and 1S,3R-ACPD. J Neurosci 13:2199-2216.
77. White EL. 1989. Cortical circuits: synaptic organization of the cerebral cortex-structure, function and theory. Boston: Birkhauser.
78. +ATPaSe, NADPH-diaphorase, nitric oxide synthase, and N-methyl-D-aspartate receptor subunit 1. Neuroscience 83:1025-1045.
79. Wouterlood FG, Jorritsma-Byham B. 1993. The anterograde neuroanatomical tracer biotinylated dextran-amine: comparison with the tracer Phaseolus vulgaris-leucoagglutinin in preparations for electron microscopy. J Neurosci Methods 48:75-87.
80. Wozniak DF, Stewart GR, Finger S, Olney JW. 1989. Comparison of behavioral effects of nucleus basalis magnocellularis lesions and somatosensory cortex ablation in the rat. Neuroscience 32:685-700.
81. Xiang Z, Huguenard JR, Prince DA. 1998. Cholinergic switching within neocortical inhibitory networks. Science 281:985-988.
82. Yu AJ, Dayan P. 2005. Uncertainty, neuromodulation, and attention. Neuron 46:681-692.
83. Zaitsev AV, Gonzalez-Burgos G, Povysheva NV, Kroner S, Lewis DA, Krimer LS. 2005. Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. Cereb Cortex 15:1178-1186.