Impaired functional organization in the visual cortex of muscarinic receptor knock-out mice

NeuroImage

Volumn 98, Issue , 2014, Pages 233-242

  Groleau, Marianne ^a   Nguyen, Hoang Nam ^a   Vanni, Matthieu P ^a   Huppé Gourgues, Frédéric ^a   Casanova, Christian ^a   Vaucher, Elvire ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Cartography; Cortical activity; Muscarinic receptors; Visual cortex

Indexed keywords

ACETYLCHOLINE; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; MUSCARINIC M4 RECEPTOR; MUSCARINIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SIZE; CONNECTOME; CONTROLLED STUDY; FLUORESCENCE IMAGING; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIGHT SCATTERING; MALE; MOUSE; NEUROMODULATION; NONHUMAN; PARASYMPATHETIC INNERVATION; PRIORITY JOURNAL; RETINOTECTAL PROJECTION; SIGNAL DETECTION; TASK PERFORMANCE; VISION; VISUAL CORTEX; VISUAL FIELD; VISUAL STIMULATION; ANATOMY AND HISTOLOGY; ANIMAL; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; PHOTOSTIMULATION; PHYSIOLOGY;

ANIMALS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOTIC STIMULATION; RECEPTOR, MUSCARINIC M1; RECEPTOR, MUSCARINIC M2; RECEPTOR, MUSCARINIC M3; RECEPTOR, MUSCARINIC M4; RECEPTORS, MUSCARINIC; VISUAL CORTEX; VISUAL FIELDS;

EID: 84902953874     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.05.016     Document Type: Article

References (85)

1. Amar M., Lucas-Meunier E., Baux G., Fossier P. Blockade of different muscarinic receptor subtypes changes the equilibrium between excitation and inhibition in rat visual cortex. Neuroscience 2010, 169:1610-1620.
2. Aubert I., Cecyre D., Gauthier S., Quirion R. Comparative ontogenic profile of cholinergic markers, including nicotinic and muscarinic receptors, in the rat brain. J. Comp. Neurol. 1996, 369:31-55.
3. Baccus S.A., Meister M. Fast and slow contrast adaptation in retinal circuitry. Neuron 2002, 36:909-919.
4. Bear M.F., Singer W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 1986, 320:172-176.
5. Bhattacharyya A., Biessmann F., Veit J., Kretz R., Rainer G. Functional and laminar dissociations between muscarinic and nicotinic cholinergic neuromodulation in the tree shrew primary visual cortex. Eur. J. NeuroSci. 2012, 35:1270-1280.
6. Bhattacharyya A., Veit J., Kretz R., Bondar I., Rainer G. Basal forebrain activation controls contrast sensitivity in primary visual cortex. BMC Neurosci. 2013, 14:55.
7. Buonomano D.V., Merzenich M.M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 1998, 21:149-186.
8. Cang J., Kaneko M., Yamada J., Woods G., Stryker M.P., Feldheim D.A. Ephrin-As guide the formation of functional maps in the visual cortex. Neuron 2005, 48:577-589.
9. Cang J., Renteria R.C., Kaneko M., Liu X., Copenhagen D.R., Stryker M.P. Development of precise maps in visual cortex requires patterned spontaneous activity in the retina. Neuron 2005, 48:797-809.
10. Cang J., Wang L., Stryker M.P., Feldheim D.A. Roles of ephrin-As and structured activity in the development of functional maps in the superior colliculus. J. Neurosci. 2008, 28:11015-11023.
11. Carandini M., Sengpiel F. Contrast invariance of functional maps in cat primary visual cortex. J. Vis. 2004, 4:130-143.
12. Caulfield M.P., Birdsall N.J. International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol. Rev. 1998, 50:279-290.
13. Chattopadhyaya B., Di Cristo G., Wu C.Z., Knott G., Kuhlman S., Fu Y., Palmiter R.D., Huang Z.J. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 2007, 54:889-903.
14. Collier B., Mitchell J.F. The central release of acetylcholine during stimulation of the visual pathway. J. Physiol. 1966, 184:239-254.
15. Delacour J., Houcine O., Costa J.C. Evidence for a cholinergic mechanism of "learned" changes in the responses of barrel field neurons of the awake and undrugged rat. Neuroscience 1990, 34:1-8.
16. Disney A.A., Aoki C. Muscarinic acetylcholine receptors in macaque V1 are most frequently expressed by parvalbumin-immunoreactive neurons. J. Comp. Neurol. 2008, 507:1748-1762.
17. Disney A.A., Domakonda K.V., Aoki C. Differential expression of muscarinic acetylcholine receptors across excitatory and inhibitory cells in visual cortical areas V1 and V2 of the macaque monkey. J. Comp. Neurol. 2006, 499:49-63.
18. Dotigny F., Ben Amor A.Y., Burke M., Vaucher E. Neuromodulatory role of acetylcholine in visually-induced cortical activation: behavioral and neuroanatomical correlates. Neuroscience 2008, 154:1607-1618.
19. Drager U.C. Receptive fields of single cells and topography in mouse visual cortex. J. Comp. Neurol. 1975, 160:269-290.
20. Dringenberg H.C., Hamze B., Wilson A., Speechley W., Kuo M.C. Heterosynaptic facilitation of in vivo thalamocortical long-term potentiation in the adult rat visual cortex by acetylcholine. Cereb. Cortex 2007, 17:839-848.
21. Duttaroy A., Gomeza J., Gan J.W., Siddiqui N., Basile A.S., Harman W.D., Smith P.L., Felder C.C., Levey A.I., Wess J. Evaluation of muscarinic agonist-induced analgesia in muscarinic acetylcholine receptor knockout mice. Mol. Pharmacol. 2002, 62:1084-1093.
22. Elhusseiny A., Cohen Z., Olivier A., Stanimirovic D.B., Hamel E. Functional acetylcholine muscarinic receptor subtypes in human brain microcirculation: identification and cellular localization. J. Cereb. Blood Flow Metab. 1999, 19:794-802.
23. Erisir A., Levey A.I., Aoki C. Muscarinic receptor M(2) in cat visual cortex: laminar distribution, relationship to gamma-aminobutyric acidergic neurons, and effect of cingulate lesions. J. Comp. Neurol. 2001, 441:168-185.
24. Fagiolini M., Pizzorusso T., Berardi N., Domenici L., Maffei L. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vis. Res. 1994, 34:709-720.
25. Frostig R.D., Lieke E.E., Ts'o D.Y., Grinvald A. Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:6082-6086.
26. Gericke A., Sniatecki J.J., Goloborodko E., Steege A., Zavaritskaya O., Vetter J.M., Grus F.H., Patzak A., Wess J., Pfeiffer N. Identification of the muscarinic acetylcholine receptor subtype mediating cholinergic vasodilation in murine retinal arterioles. Invest. Ophthalmol. Vis. Sci. 2011, 52:7479-7484.
27. Gil Z., Connors B.W., Amitai Y. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 1997, 19:679-686.
28. Greuel J.M., Luhmann H.J., Singer W. Pharmacological induction of use-dependent receptive field modifications in the visual cortex. Science 1988, 242:74-77.
29. Grinvald A., Lieke E., Frostig R.D., Gilbert C.D., Wiesel T.N. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 1986, 324:361-364.
30. Gundersen H.J., Jensen E.B., Kieu K., Nielsen J. The efficiency of systematic sampling in stereology-reconsidered. J. Microsc. 1999, 193:199-211.
31. Hagihara K.M., Ohki K. Long-term down-regulation of GABA decreases orientation selectivity without affecting direction selectivity in mouse primary visual cortex. Front. Neural Circ. 2013, 7:28.
32. Hamel E. Cholinergic modulation of the cortical microvascular bed. Prog. Brain Res. 2004, 145:171-178.
33. Hensch T.K. Critical period mechanisms in developing visual cortex. Curr. Top. Dev. Biol. 2005, 69:215-237.
34. Herrero J.L., Roberts M.J., Delicato L.S., Gieselmann M.A., Dayan P., Thiele A. Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature 2008, 454:1110-1114.
35. Heynen A.J., Bear M.F. Long-term potentiation of thalamocortical transmission in the adult visual cortex in vivo. J. Neurosci. 2001, 21:9801-9813.
36. Hillman E.M., Devor A., Bouchard M.B., Dunn A.K., Krauss G.W., Skoch J., Bacskai B.J., Dale A.M., Boas D.A. Depth-resolved optical imaging and microscopy of vascular compartment dynamics during somatosensory stimulation. Neuroimage 2007, 35:89-104.
37. Kalatsky V.A. Fourier approach for functional imaging. In Vivo Optical Imaging of Brain Function 2009, CRC Press, Boca Raton (FL), (Chapter 10). 2nd edition. R.D. Frostig (Ed.).
38. Kalatsky V.A., Stryker M.P. New paradigm for optical imaging: temporally encoded maps of intrinsic signal. Neuron 2003, 38:529-545.
39. Kang J.I., Vaucher E. Cholinergic pairing with visual activation results in long-term enhancement of visual evoked potentials. PLoS One 2009, 4:e5995.
40. Kang J.I., Groleau M., Dotigny F., Giguere H., Vaucher E. Visual training paired with electrical stimulation of the basal forebrain improves orientation-selective visual acuity in the rat. Brain Struct. Funct 2013, in press. 10.1007/s00429-013-0582-y.
41. Kimura F., Baughman R.W. Distinct muscarinic receptor subtypes suppress excitatory and inhibitory synaptic responses in cortical neurons. J. Neurophysiol. 1997, 77:709-716.
42. Kimura F., Fukuda M., Tsumoto T. Acetylcholine suppresses the spread of excitation in the visual cortex revealed by optical recording: possible differential effect depending on the source of input. Eur. J. NeuroSci. 1999, 11:3597-3609.
43. Laplante F., Morin Y., Quirion R., Vaucher E. Acetylcholine release is elicited in the visual cortex, but not in the prefrontal cortex, by patterned visual stimulation: a dual in vivo microdialysis study with functional correlates in the rat brain. Neuroscience 2005, 132:501-510.
44. Lawrence J.J. Cholinergic control of GABA release: emerging parallels between neocortex and hippocampus. Trends Neurosci. 2008, 31:317-327.
45. Lazareno S., Birdsall N.J. Detection, quantitation, and verification of allosteric interactions of agents with labeled and unlabeled ligands at G protein-coupled receptors: interactions of strychnine and acetylcholine at muscarinic receptors. Mol. Pharmacol. 1995, 48:362-378.
46. Lecrux C., Toussay X., Kocharyan A., Fernandes P., Neupane S., Levesque M., Plaisier F., Shmuel A., Cauli B., Hamel E. Pyramidal neurons are "neurogenic hubs" in the neurovascular coupling response to whisker stimulation. J. Neurosci. 2011, 31:9836-9847.
47. Levey A.I., Kitt C.A., Simonds W.F., Price D.L., Brann M.R. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J. Neurosci. 1991, 11:3218-3226.
48. McCormick D.A., Prince D.A. Two types of muscarinic response to acetylcholine in mammalian cortical neurons. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:6344-6348.
49. Mechawar N., Cozzari C., Descarries L. Cholinergic innervation in adult rat cerebral cortex: a quantitative immunocytochemical description. J. Comp. Neurol. 2000, 428:305-318.
50. Mouton P.R., Gokhale A.M., Ward N.L., West M.J. Stereological length estimation using spherical probes. J. Microsc. 2002, 206:54-64.
51. Movshon J.A., Lennie P. Pattern-selective adaptation in visual cortical neurones. Nature 1979, 278:850-852.
52. Mrzljak L., Levey A.I., Rakic P. Selective expression of m2 muscarinic receptor in the parvocellular channel of the primate visual cortex. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:7337-7340.
53. Murphy P.C., Sillito A.M. Cholinergic enhancement of direction selectivity in the visual cortex of the cat. Neuroscience 1991, 40:13-20.
54. Origlia N., Kuczewski N., Aztiria E., Gautam D., Wess J., Domenici L. Muscarinic acetylcholine receptor knockout mice show distinct synaptic plasticity impairments in the visual cortex. J. Physiol. 2006, 577:829-840.
55. Palmer S.M., Rosa M.G. A distinct anatomical network of cortical areas for analysis of motion in far peripheral vision. Eur. J. Neurosci. 2006, 24:2389-2405.
56. Paxinos, Franklin Paxinos and Franklin's the Mouse Brain in Stereotaxic Coordinates 2012, Academic Press. 4th edition.
57. Prusky G.T., Shaw C., Cynader M.S. Nicotine receptors are located on lateral geniculate nucleus terminals in cat visual cortex. Brain Res. 1987, 412:131-138.
58. Roberson E.D., English J.D., Adams J.P., Selcher J.C., Kondratick C., Sweatt J.D. The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J. Neurosci. 1999, 19:4337-4348.
59. Roberts M.J., Zinke W., Guo K., Robertson R., McDonald J.S., Thiele A. Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex. J. Neurophysiol. 2005, 93:2062-2072.
60. Rosa M.G.P., Tweedale R. Maps of the visual field in the cerebral cortex of primates: functional organization and significance. The Primate Visual System 2004, 261-288. CRC Press. J.H.C. Kaas, C.E. (Eds.).
61. Rouse S.T., Marino M.J., Potter L.T., Conn P.J., Levey A.I. Muscarinic receptor subtypes involved in hippocampal circuits. Life Sci. 1999, 64:501-509.
62. 2+-dependent PKC. J. Neurophysiol. 2007, 98:952-965.
63. Sato H., Hata Y., Masui H., Tsumoto T. A functional role of cholinergic innervation to neurons in the cat visual cortex. J. Neurophysiol. 1987, 58:765-780.
64. Schuett S., Bonhoeffer T., Hubener M. Mapping retinotopic structure in mouse visual cortex with optical imaging. J. Neurosci. 2002, 22:6549-6559.
65. Series P., Lorenceau J., Fregnac Y. The "silent" surround of V1 receptive fields: theory and experiments. J. Physiol. Paris 2003, 97:453-474.
66. Sillito A.M. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J. Physiol. 1975, 250:305-329.
67. Sillito A.M. The spatial extent of excitatory and inhibitory zones in the receptive field of superficial layer hypercomplex cells. J. Physiol. 1977, 273:791-803.
68. Silver M.A., Shenhav A., D'Esposito M. Cholinergic enhancement reduces spatial spread of visual responses in human early visual cortex. Neuron 2008, 60:904-914.
69. Soma S., Shimegi S., Osaki H., Sato H. Cholinergic modulation of response gain in the primary visual cortex of the macaque. J. Neurophysiol. 2012, 107:283-291.
70. Soma S., Shimegi S., Suematsu N., Sato H. Cholinergic modulation of response gain in the rat primary visual cortex. Sci. Rep. 2013, 3:1138.
71. Thiele A. Muscarinic signaling in the brain. Annu. Rev. Neurosci. 2013, 36:271-294.
72. Ts'o D.Y., Frostig R.D., Lieke E.E., Grinvald A. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 1990, 249:417-420.
73. Vanni M.P., Provost J., Lesage F., Casanova C. Evaluation of receptive field size from higher harmonics in visuotopic mapping using continuous stimulation optical imaging. J. Neurosci. Methods 2010, 189:138-150.
74. Vanzetta I., Grinvald A. Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. Science 1999, 286:1555-1558.
75. Vanzetta I., Grinvald A. Coupling between neuronal activity and microcirculation: implications for functional brain imaging. HFSP J. 2008, 2:79-98.
76. Volpicelli L.A., Levey A.I. Muscarinic acetylcholine receptor subtypes in cerebral cortex and hippocampus. Prog. Brain Res. 2004, 145:59-66.
77. Wess J. Muscarinic acetylcholine receptor knockout mice: novel phenotypes and clinical implications. Annu. Rev. Pharmacol. Toxicol. 2004, 44:423-450.
78. West M.J., Slomianka L., Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 1991, 231:482-497.
79. Willshaw D. Analysis of mouse EphA knockins and knockouts suggests that retinal axons programme target cells to form ordered retinotopic maps. Development 2006, 133:2705-2717.
80. Wong A.A., Brown R.E. Visual detection, pattern discrimination and visual acuity in 14 strains of mice. Genes Brain Behav. 2006, 5:389-403.
81. Yamada M., Lamping K.G., Duttaroy A., Zhang W., Cui Y., Bymaster F.P., McKinzie D.L., Felder C.C., Deng C.X., Faraci F.M., Wess J. Cholinergic dilation of cerebral blood vessels is abolished in M(5) muscarinic acetylcholine receptor knockout mice. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:14096-14101.
82. Yazaki-Sugiyama Y., Kang S., Cateau H., Fukai T., Hensch T.K. Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature 2009, 462:218-221.
83. Zhang W., Basile A.S., Gomeza J., Volpicelli L.A., Levey A.I., Wess J. Characterization of central inhibitory muscarinic autoreceptors by the use of muscarinic acetylcholine receptor knock-out mice. J. Neurosci. 2002, 22:1709-1717.
84. Zhang Z.W., Kang J.I., Vaucher E. Axonal varicosity density as an index of local neuronal interactions. PLoS One 2011, 6:e22543.
85. Zinke W., Roberts M.J., Guo K., McDonald J.S., Robertson R., Thiele A. Cholinergic modulation of response properties and orientation tuning of neurons in primary visual cortex of anaesthetized marmoset monkeys. Eur. J. NeuroSci. 2006, 24:314-328.