Sympathetic sprouting in visual cortex stimulated by cholinergic denervation rescues expression of two forms of long-term depression at layer 2/3 synapses

Neuroscience

Volumn 168, Issue 3, 2010, Pages 591-604

  McCoy, P A ^a   McMahon, L L ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

ERK; LTD; M1 mAChR; M3 mAChR; Sympathetic sprouting

Indexed keywords

ACETYLCHOLINE; GLUTAMIC ACID; MUSCARINIC M1 RECEPTOR; MUSCARINIC M3 RECEPTOR; VESICULAR ACETYLCHOLINE TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN INJURY; BRAIN SLICE; CHOLINERGIC NERVE; CHOLINERGIC SYSTEM; COGNITION; CONTROLLED STUDY; DENERVATION; EXPERIMENTAL MODEL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING; LONG TERM DEPRESSION; MAGNOCELLULAR NUCLEUS; MALE; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NERVE REGENERATION; NERVE SPROUTING; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; OLIVARY NUCLEUS; PARASYMPATHETIC INNERVATION; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SUPERIOR CERVICAL GANGLION; SUPERIOR CERVICAL GANGLIONECTOMY; SYMPATHETIC NERVE; SYNAPSE; VISUAL CORTEX; ADRENERGIC NERVE; ANIMAL; ELECTROSTIMULATION; IN VITRO STUDY; METABOLISM; MEYNERT BASAL NUCLEUS; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYMPATHETIC NERVE CELL;

ADRENERGIC FIBERS; ANIMALS; BASAL NUCLEUS OF MEYNERT; CHOLINERGIC FIBERS; ELECTRIC STIMULATION; GLUTAMIC ACID; LONG-TERM SYNAPTIC DEPRESSION; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MUSCARINIC M1; RECEPTOR, MUSCARINIC M3; SUPERIOR CERVICAL GANGLION; SYMPATHETIC FIBERS, POSTGANGLIONIC; SYNAPSES; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS; VISUAL CORTEX; IN VITRO TECHNIQUES;

EID: 77953121119     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.04.027     Document Type: Article

References (61)

1. Aigner T.G., Mitchell S.J., Aggleton J.P., DeLong M.R., Struble R.G., Price D.L., Wenk G.L., Pettigrew K.D., Mishkin M. Transient impairment of recognition memory following ibotenic-acid lesions of the basal forebrain in macaques. Exp Brain Res 1991, 86:18-26.
2. Balducci C., Nurra M., Pietropoli A., Samanin R., Carli M. Reversal of visual attention dysfunction after AMPA lesions of the nucleus basalis magnocellularis (NBM) by the cholinesterase inhibitor donepezil and by a 5-HT1A receptor antagonist WAY 100635. Psychopharmacology (Berl) 2003, 167:28-36.
3. Barefoot H.C., Baker H.F., Ridley R.M. Synergistic effects of unilateral immunolesions of the cholinergic projections from the basal forebrain and contralateral ablations of the inferotemporal cortex and hippocampus in monkeys. Neuroscience 2000, 98:243-251.
4. Barefoot H.C., Baker H.F., Ridley R.M. Crossed unilateral lesions of temporal lobe structures and cholinergic cell bodies impair visual conditional and object discrimination learning in monkeys. Eur J Neurosci 2002, 15:507-516.
5. Bentley P., Husain M., Dolan R.J. Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory. Neuron 2004, 41:969-982.
6. Bierer L.M., Haroutunian V., Gabriel S., Knott P.J., Carlin L.S., Purohit D.P., Perl D.P., Schmeidler J., Kanof P., Davis K.L. Neurochemical correlates of dementia severity in Alzheimer's disease: relative importance of the cholinergic deficits. J Neurochem 1995, 64:749-760.
7. Bodick N.C., Offen W.W., Shannon H.E., Satterwhite J., Lucas R., van Lier R., Paul S.M. The selective muscarinic agonist xanomeline improves both the cognitive deficits and behavioral symptoms of Alzheimer disease. Alzheimer Dis Assoc Disord 1997, 11(Suppl 4):S16-S22.
8. Booze R.M., Mactutus C.F., Gutman C.R., Davis J.N. Frequency analysis of catecholamine axonal morphology in human brain. II. Alzheimer's disease and hippocampal sympathetic ingrowth. J Neurol Sci 1993, 119:110-118.
9. Caccamo A., Fisher A., LaFerla F.M. M1 agonists as a potential disease-modifying therapy for Alzheimer's disease. Curr Alzheimer Res 2009, 6:112-117.
10. Choi S.Y., Chang J., Jiang B., Seol G.H., Min S.S., Han J.S., Shin H.S., Gallagher M., Kirkwood A. Multiple receptors coupled to phospholipase C gate long-term depression in visual cortex. J Neurosci 2005, 25:11433-11443.
11. Clader J.W., Wang Y. Muscarinic receptor agonists and antagonists in the treatment of Alzheimer's disease. Curr Pharm Des 2005, 11:3353-3361.
12. Conner J.M., Varon S. Nerve growth factor influences the distribution of sympathetic sprouting into the hippocampal formation by implanted superior cervical ganglia. Exp Neurol 1994, 130:15-23.
13. Conner J.M., Varon S. Effects of exogenous nerve growth factor upon sympathetic sprouting into the hippocampal formation. Exp Neurol 1995, 136:123-135.
14. Crutcher K.A. Cholinergic denervation of rat neocortex results in sympathetic innervation. Exp Neurol 1981, 74:324-329.
15. Crutcher K.A. Sympathetic sprouting in the central nervous system: a model for studies of axonal growth in the mature mammalian brain. Brain Res 1987, 434:203-233.
16. Davies P., Maloney A.J. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 1976, 2:1403.
17. Dechant G., Barde Y.A. The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat Neurosci 2002, 5:1131-1136.
18. DeKosky S.T., Ikonomovic M.D., Styren S.D., Beckett L., Wisniewski S., Bennett D.A., Cochran E.J., Kordower J.H., Mufson E.J. Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment. Ann Neurol 2002, 51:145-155.
19. Dobrunz L.E., Stevens C.F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 1997, 18:995-1008.
20. Drachman D.A., Leavitt J. Human memory and the cholinergic system. A relationship to aging?. Arch Neurol 1974, 30:113-121.
21. Dudek S.M., Bear M.F. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 1993, 13:2910-2918.
22. Dunnett S.B., Fibiger H.C. Role of forebrain cholinergic systems in learning and memory: relevance to the cognitive deficits of aging and Alzheimer's dementia. Prog Brain Res 1993, 98:413-420.
23. Eckenstein F., Baughman R.W. Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide. Nature 1984, 309:153-155.
24. Ferrari-DiLeo G., Flynn D.D. Diminished muscarinic receptor-stimulated [3H]-PIP2 hydrolysis in Alzheimer's disease. Life Sci 1993, 53:PL439-PL444.
25. Ferrari-DiLeo G., Mash D.C., Flynn D.D. Attenuation of muscarinic receptor-G-protein interaction in Alzheimer disease. Mol Chem Neuropathol 1995, 24:69-91.
26. Fisher A. Cholinergic treatments with emphasis on m1 muscarinic agonists as potential disease-modifying agents for Alzheimer's disease. Neurotherapeutics 2008, 5:433-442.
27. Fisher A., Michaelson D.M., Brandeis R., Haring R., Chapman S., Pittel Z. M1 muscarinic agonists as potential disease-modifying agents in Alzheimer's disease. Rationale and perspectives. Ann N Y Acad Sci 2000, 920:315-320.
28. Fletcher B.R., Baxter M.G., Guzowski J.F., Shapiro M.L., Rapp P.R. Selective cholinergic depletion of the hippocampus spares both behaviorally induced arc transcription and spatial learning and memory. Hippocampus 2007, 17:227-234.
29. Francis N.J., Landis S.C. Cellular and molecular determinants of sympathetic neuron development. Annu Rev Neurosci 1999, 22:541-566.
30. Frolich L. The cholinergic pathology in Alzheimer's disease-discrepancies between clinical experience and pathophysiological findings. J Neural Transm 2002, 109:1003-1013.
31. Furshpan E.J., MacLeish P.R., O'Lague P.H., Potter D.D. Chemical transmission between rat sympathetic neurons and cardiac myocytes developing in microcultures: evidence for cholinergic, adrenergic, and dual-function neurons. Proc Natl Acad Sci U S A 1976, 73:4225-4229.
32. Gibbs R.B., Johnson D.A. Cholinergic lesions produce task-selective effects on delayed matching to position and configural association learning related to response pattern and strategy. Neurobiol Learn Mem 2007, 88:19-32.
33. Gwyther L.P. Caring for people with Alzheimer's disease: a manual for facility staff 2001, American Health Care Association, Washington, DC.
34. Harrell L.E., Kolasa K., Parsons D.S., Ayyagari V. Hippocampal sympathetic ingrowth and cholinergic denervation uniquely alter muscarinic receptor subtypes in the hippocampus. Brain Res 1995, 676:386-393.
35. Hashimoto M., Masliah E. Cycles of aberrant synaptic sprouting and neurodegeneration in Alzheimer's and dementia with Lewy bodies. Neurochem Res 2003, 28:1743-1756.
36. Houser C.R., Crawford G.D., Barber R.P., Salvaterra P.M., Vaughn J.E. Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res 1983, 266:97-119.
37. Kirkwood A., Rozas C., Kirkwood J., Perez F., Bear M.F. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 1999, 19:1599-1609.
38. Kolasa K., Harrell L.E., Parsons D.S. Effect of hippocampal sympathetic ingrowth and cholinergic denervation on hippocampal phospholipase C activity and G-protein function. Neuroscience 1997, 77:111-120.
39. Kuczewski N., Aztiria E., Leanza G., Domenici L. Selective cholinergic immunolesioning affects synaptic plasticity in developing visual cortex. Eur J Neurosci 2005, 21:1807-1814.
40. Loy R., Moore R.Y. Anomalous innervation of the hippocampal formation by peripheral sympathetic axons following mechanical injury. Exp Neurol 1977, 57:645-650.
41. Masliah E., Alford M., Adame A., Rockenstein E., Galasko D., Salmon D., Hansen L.A., Thal L.J. Abeta1-42 promotes cholinergic sprouting in patients with AD and Lewy body variant of AD. Neurology 2003, 61:206-211.
42. Masliah E., Mallory M., Hansen L., Alford M., Albright T., DeTeresa R., Terry R., Baudier J., Saitoh T. Patterns of aberrant sprouting in Alzheimer's disease. Neuron 1991, 6:729-739.
43. Mayo W., Kharouby M., Le Moal M., Simon H. Memory disturbances following ibotenic acid injections in the nucleus basalis magnocellularis of the rat. Brain Res 1988, 455:213-222.
44. McCoy P.A., McMahon L.L. Muscarinic receptor dependent long term depression in rat visual cortex is PKC independent but requires ERK1/2 activation and protein synthesis. J Neurophysiol 2007, 98:1862-1870.
45. McCoy P.A., Norton T.T., McMahon L.L. Layer 2/3 synapses in monocular and binocular regions of tree shrew visual cortex express mAChR dependent long-term depression and long-term potentiation. J Neurophysiol 2008, 100:336-345.
46. Mufson E.J., Counts S.E., Perez S.E., Ginsberg S.D. Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Expert Rev Neurother 2008, 8:1703-1718.
47. Mufson E.J., Ginsberg S.D., Ikonomovic M.D., deKosky S.T. Human cholinergic basal forebrain: chemoanatomy and neurologic dysfunction. J Chem Neuroanat 2003, 26:233-242.
48. Nobili L., Sannita W.G. Cholinergic modulation, visual function and Alzheimer's dementia. Vision Res 1997, 37:3559-3571.
49. Origlia N., Kuczewski N., Aztiria E., Gautam D., Wess J., Domenici L. Muscarinic acetylcholine receptor knock-out mice show distinct synaptic plasticity impairments in the visual cortex. J Physiol 2006, 577:829-840.
50. Parent M.B., Baxter M.G. Septohippocampal acetylcholine: involved in but not necessary for learning and memory?. Learn Mem 2004, 11:9-20.
51. Pearce B.D., Potter L.T. Coupling of m1 muscarinic receptors to G protein in Alzheimer disease. Alzheimer Dis Assoc Disord 1991, 5:163-172.
52. Perry E.K., Perry R.H., Blessed G., Tomlinson B.E. Changes in brain cholinesterases in senile dementia of Alzheimer type. Neuropathol Appl Neurobiol 1978, 4:273-277.
53. Rizzo M., Anderson S.W., Dawson J., Nawrot M. Vision and cognition in Alzheimer's disease. Neuropsychologia 2000, 38:1157-1169.
54. Scalapino K., Conner J.M., Varon S. The role of NGF and afferent denervation in the process of sympathetic fiber ingrowth into the hippocampal formation. Exp Neurol 1996, 141:310-317.
55. Schafer M.K., Eiden L.E., Weihe E. Cholinergic neurons and terminal fields revealed by immunohistochemistry for the vesicular acetylcholine transporter. II. The peripheral nervous system. Neuroscience 1998, 84:361-376.
56. Scheiderer C.L., McCutchen E., Thacker E.E., Kolasa K., Ward M.K., Parsons D., Harrell L.E., Dobrunz L.E., McMahon L.L. Sympathetic sprouting drives hippocampal cholinergic reinnervation that prevents loss of a muscarinic receptor-dependent long-term depression at CA3-CA1 synapses. J Neurosci 2006, 26:3745-3756.
57. Scheiderer C.L., Smith C.C., McCutchen E., McCoy P.A., Thacker E.E., Kolasa K., Dobrunz L.E., McMahon L.L. Coactivation of M1 muscarinic and alpha1 adrenergic receptors stimulates extracellular signal-regulated protein kinase and induces long-term depression as ca3-ca1 synapses in rat hippocmapus. J Neurosci 2008, 28:5350-5358.
58. Volk L.J., Pfeiffer B.E., Gibson J.R., Huber K.M. Multiple Gq-coupled receptors converge on a common protein synthesis-dependent long-term depression that is affected in fragile X syndrome mental retardation. J Neurosci 2007, 27:11624-11634.
59. Weihe E., Schutz B., Hartschuh W., Anlauf M., Schafer M.K., Eiden L.E. Coexpression of cholinergic and noradrenergic phenotypes in human and nonhuman autonomic nervous system. J Comp Neurol 2005, 492:370-379.
60. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., Delon M.R. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 1982, 215:1237-1239.
61. Wolinsky E., Patterson P.H. Tyrosine hydroxylase activity decreases with induction of cholinergic properties in cultured sympathetic neurons. J Neurosci 1983, 3:1495-1500.