Layer 2/3 synapses in monocular and binocular regions of tree shrew visual cortex express mAChR-dependent long-term depression and long-term potentiation

Journal of Neurophysiology

Volumn 100, Issue 1, 2008, Pages 336-345

  McCoy, Portia ^a   Norton, Thomas T ^c   McMahon, Lori L ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBACHOL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCARINIC RECEPTOR; PHOSPHOLIPASE C; ATROPINE; CHOLINERGIC RECEPTOR BLOCKING AGENT; CHOLINERGIC RECEPTOR STIMULATING AGENT; ENZYME INHIBITOR; GABAERGIC RECEPTOR AFFECTING AGENT;

ANIMAL TISSUE; ARTICLE; CHOLINERGIC SYSTEM; CONTROLLED STUDY; ENZYME ACTIVATION; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; VISUAL CORTEX; ANIMAL; BIOLOGICAL MODEL; DRUG EFFECT; DRUG INTERACTION; ELECTROSTIMULATION; HISTOLOGY; IN VITRO STUDY; METHODOLOGY; PATCH CLAMP; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION RESPONSE; SCANDENTIA; SYNAPSE; VISION;

ANIMALS; ATROPINE; CARBACHOL; CHOLINERGIC AGONISTS; CHOLINERGIC ANTAGONISTS; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; GABA AGENTS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MODELS, BIOLOGICAL; PATCH-CLAMP TECHNIQUES; RECEPTORS, MUSCARINIC; SYNAPSES; TUPAIIDAE; VISION; VISUAL CORTEX;

EID: 55249098839     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01134.2007     Document Type: Article

References (47)

1. 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 167: 28-36, 2003.
2. Barefoot HC, Baker HF, Ridley RM. 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 98: 243-251, 2000.
3. Bear MF. Homosynaptic long-term depression: a mechanism for memory? Proc Natl Acad Sci USA 96: 9457-9458, 1999.
4. Bentley P, Husain M, Dolan RJ. Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory. Neuron 41: 969-982, 2004.
5. Blokland A. Acetylcholine: a neurotransmitter for learning and memory? Brain Res Brain Res Rev 21: 285-300, 1995.
6. Bodick NC, Offen WW, Shannon HE, Satterwhite J, Lucas R, van Lier R, Paul SM. The selective muscarinic agonist xanomeline improves both the cognitive deficits and behavioral symptoms of Alzheimer disease. Alzheimer Dis Assoc Disord 11, Suppl 4: S16-22, 1997.
7. Budd DC, Willars GB, McDonald JE, Tobin AB. Phosphorylation of the Gq/11-coupled m3-muscarinic receptor is involved in receptor activation of the ERK-1/2 mitogen-activated protein kinase pathway. J Biol Chem 276: 4581-4587, 2001.
8. Caccamo A, Oddo S, Billings LM, Green KN, Martinez-Coria H, Fisher A, LaFerla FM. M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 49: 671-682, 2006.
9. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105, 2000.
10. Dean B. M1 receptor agonism, a possible treatment for cognitive deficits in schizophrenia. Neuropsychopharmacology 29: 1583-1584; author reply 1585-1586, 2004.
11. Dean B, McLeod M, Keriakous D, McKenzie J, Scarr E. Decreased muscarinic1 receptors in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 7: 1083-1091, 2002.
12. Dobrunz LE, Stevens CF. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008, 1997.
13. Dringenberg HC, Hamze B, Wilson A, Speechley W, Kuo MC. Heterosynaptic facilitation of in vivo thalamocortical long-term potentiation in the adult rat visual cortex by acetylcholine. Cereb Cortex 17: 839-848, 2007.
14. Ehlert FJ. The interaction of 4-DAMP mustard with subtypes of the muscarinic receptor. Life Sci 58: 1971-1978, 1996.
15. Hao J, Li K, Zhang D, Wang W, Yang Y, Yan B, Shan B, Zhou X. Visual attention deficits in Alzheimer's disease: an fMRI study. Neurosci Lett 385: 18-23, 2005.
16. Himmelheber AM, Sarter M, Bruno JP. Increases in cortical acetylcholine release during sustained attention performance in rats. Brain Res Cogn Brain Res 9: 313-325, 2000.
17. Humphrey AL, Albano JE, Norton TT. Organization of ocular dominance in tree shrew striate cortex. Brain Res 134: 225-236, 1977.
18. Ikonomovic MD, Mufson EJ, Wuu J, Bennett DA, DeKosky ST. Reduction of choline acetyltransferase activity in primary visual cortex in mild to moderate Alzheimer's disease. Arch Neurol 62: 425-430, 2005.
19. Ismailov I, Kalikulov D, Inoue T, Friedlander MJ. The kinetic profile of intracellular calcium predicts long-term potentiation and long-term depression. J Neurosci 24: 9847-9861, 2004.
20. Jacobs GH, Neitz J. Spectral mechanisms and color vision in the tree shrew (Tupaia belangeri). Vision Res 26: 291-298, 1986.
21. Kaas JH, Hall WC, Killackey H, Diamond IT. Visual cortex of the tree shrew (Tupaia glis): architectonic subdivisions and representations of the visual field. Brain Res 42: 491-496, 1972.
22. Karmarkar UR, Dan Y. Experience-dependent plasticity in adult visual cortex. Neuron 52: 577-585, 2006.
23. Kemp PM, Holmes C, Hoffmann S, Wilkinson S, Zivanovic M, Thom J, Bolt L, Fleming J, Wilkinson DG. A randomised placebo controlled study to assess the effects of cholinergic treatment on muscarinic receptors in Alzheimer's disease. J Neurol Neurosurg Psychiatry 74: 1567-1570, 2003.
24. Kimura F, Baughman RW. Distinct muscarinic receptor subtypes suppress excitatory and inhibitory synaptic responses in cortical neurons. J Neurophysiol 77: 709-716, 1997.
25. 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 11: 3597-3609, 1999.
26. Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 19: 1599-1609, 1999.
27. Koga H, Ishibashi H, Shimada H, Jang IS, Nakamura TY, Nabekura J. Activation of presynaptic GABAA receptors increases spontaneous glutamate release onto noradrenergic neurons of the rat locus coeruleus. Brain Res 1046: 24-31, 2005.
28. Kojic L, Gu Q, Douglas RM, Cynader MS. Laminar distribution of cholinergic-and serotonergic-dependent plasticity within kitten visual cortex. Brain Res Dev Brain Res 126: 157-162, 2001.
29. Li H, Zhang J, Xiong W, Xu T, Cao J, Xu L. Long-term depression in rat CA1-subicular synapses depends on the G-protein coupled mACh receptors. Neurosci Res 52: 287-294, 2005.
30. Luckett WP. Comparative Biology and Evolutionary Relationships of Tree Shrews. New York: Plenum, 1980.
31. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 44: 5-21, 2004.
32. Marino MJ, Rouse ST, Levey AI, Potter LT, Conn PJ. Activation of the genetically defined m1 muscarinic receptor potentiates N-methyl- D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc Natl Acad Sci USA 95: 11465-11470, 1998.
33. McCoy PA, McMahon LL. Muscarinic receptor-dependent long-term depression in rat visual cortex is PKC independent but requires ERK1/2 activation and protein synthesis. J Neurophysiol 98: 1862-1870, 2007.
34. McQuiston AR, Madison DV. Muscarinic receptor activity has multiple effects on the resting membrane potentials of CA1 hippocampal interneurons. J Neurosci 19: 5693-5702, 1999.
35. Mrzljak L, Levey AI, Goldman-Rakic PS. 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 USA 90: 5194-5198, 1993.
36. Offermanns S, Wieland T, Homann D, Sandmann J, Bombien E, Spicher K, Schultz G, Jakobs KH. Transfected muscarinic acetylcholine receptors selectively couple to Gi-type G proteins and Gq/11. Mol Pharmacol 45: 890-898, 1994.
37. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC. Storage of spatial information by the maintenance mechanism of LTP. Science 313: 1141-1144, 2006.
38. Peavy RD, Chang MS, Sanders-Bush E, Conn PJ. Metabotropic glutamate receptor 5-induced phosphorylation of extracellular signal-regulated kinase in astrocytes depends on transactivation of the epidermal growth factor receptor. J Neurosci 21: 9619-9628, 2001.
39. Petry HM, Fox R, Casagrande VA. Spatial contrast sensitivity of the tree shrew. Vision Res 24: 1037-1042, 1984.
40. Potter DD, Pickles CD, Roberts RC, Rugg MD. The effects of scopolamine on event-related potentials in a continuous recognition memory task. Psychophysiology 29: 29-37, 1992.
41. Richards MH. Pharmacology and second messenger interactions of cloned muscarinic receptors. Biochem Pharmacol 42: 1645-1653, 1991.
42. Scheiderer CL, McCutchen E, Thacker EE, Kolasa K, Ward MK, Parsons D, Harrell LE, Dobrunz LE, McMahon LL. Sympathetic sprouting drives hippocampal cholinergic reinnervation that prevents loss of a muscarinic receptor-dependent long-term depression at CA3-CA1 synapses. J Neurosci 26: 3745-3756, 2006.
43. Soffie M, Bronchart M, Lebailly B. Scopolamine-induced deficits in acquisition of a complex spatial learning. Physiol Behav 37: 79-84, 1986.
44. Taffe MA, Weed MR, Gutierrez T, Davis SA, Gold LH. Differential muscarinic and NMDA contributions to visuo-spatial paired-associate learning in rhesus monkeys. Psychopharmacology 160: 253-262, 2002.
45. Thiel CM, Henson RN, Dolan RJ. Scopolamine but not lorazepam modulates face repetition priming: a psychopharmacological fMRI study. Neuropsychopharmacology 27: 282-292, 2002.
46. Tsanov M, Manahan-Vaughan D. The adult visual cortex expresses dynamic synaptic plasticity that is driven by the light/dark cycle. J Neurosci 27: 8414-8421, 2007.
47. Whitlock JR, Heynen AJ, Shuler MG, Bear MF. Learning induces long-term potentiation in the hippocampus. Science 313: 1093-1097, 2006.