Cholinergic inhibition of neocortical pyramidal neurons

Journal of Neuroscience

Volumn 25, Issue 44, 2005, Pages 10308-10320

  Gulledge, Allan T ^a,b   Stuart, Greg J ^a  

^a Biology and Environment   (Australia)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

Acetylcholine; Calcium imaging; Muscarinic receptor; Neocortex; Pyramidal neuron; SK channel

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; ACETYLCHOLINE; ATROPINE; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; CADMIUM; CALCIUM; CALCIUM CHELATING AGENT; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; MUSCARINIC M1 RECEPTOR; MUSCARINIC RECEPTOR; PICROTOXIN; PIRENZEPINE; SODIUM CHANNEL;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CHANNEL GATING; CHOLINERGIC ACTIVITY; COGNITION; CONTROLLED STUDY; DEPOLARIZATION; HYPERPOLARIZATION; MEMBRANE CONDUCTANCE; NEOCORTEX; NEUROTRANSMISSION; NONHUMAN; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR BLOCKING; SOMATOSENSORY CORTEX;

ANIMALS; MUSCARINIC AGONISTS; NEOCORTEX; NEURAL INHIBITION; NEURONS; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTORS, MUSCARINIC;

EID: 27744452369     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2697-05.2005     Document Type: Article

References (54)

1. Andrade R (1991) Cell excitation enhances muscarinic cholinergic responses in rat association cortex. Brain Res 548:81-93.
2. Bandrowski AE, Moore SL, Ashe JH (2001) Cholinergic synaptic potentials in the supragranular layers of auditory cortex. Synapse 41:118-130.
3. Bartus RT, Dean III RL, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-414.
4. Blitzer RD, Gil O, Landau EM (1990) Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett 119:207-210.
5. Buresova O, Bolhuis JJ, Bures J (1986) Differential effects of cholinergic blockade on performance of rats in the water tank navigation task and in a radial water maze. Behav Neurosci 100:476-482.
6. Burgard EC, Sarvey JM (1990) Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus. Neurosci Lett 116:34-39.
7. Casu MA, Wong TP, De Koninck Y, Ribeiro-da-Silva A, Cuello AC (2002) Aging causes a preferential loss of cholinergic innervation of characterized neocortical pyramidal neurons. Cereb Cortex 12:329-337.
8. Courtney C, Farrell D, Gray R, Hills R, Lynch L, Sellwood E, Edwards S, Hardyman W, Raftery J, Crome P, Lendon C, Shaw H, Bentham P (2004) Long-term donepezil treatment in 565 patients with Alzheimer's disease (AD2000): randomised double-blind trial. Lancet 363:2105-2115.
9. Drachman DA, Leavitt JK (1974) Human memory and the cholinergic system. A relationship to aging? Arch Neurol 30:113-121.
10. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420:173-178.
11. 2+-independent muscarinic excitation of rat medial entorhinal cortex layer V neurons. Eur J Neurosci 18:3343-3351.
12. Fiorillo CD, Williams JT (1998) Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature 394:78-82.
13. Fiorillo CD, Williams JT (2000) Cholinergic inhibition of ventral midbrain dopamine neurons. J Neurosci 20:7855-7860.
14. Flynn DD, Ferrari-DiLeo G, Mash DC, Levey AI (1995) Differential regulation of molecular subtypes of muscarinic receptors in Alzheimer's disease. J Neurochem 64:1888-1891.
15. Gil Z, Connors BW, Amitai Y (1997) Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679-686.
16. i signalling in projection cells of medial entorhinal cortex layers II and III. Eur J Neurosci 11:3626-3636.
17. Hagan JJ, Morris RGM (1988) The cholinergic hypothesis of memory: a review of animal experiments. In: Handbook of psychopharmacology (Iversen LL, Iversen SD, Snyder SH, eds), pp 237-323. New York: Plenum.
18. Haj-Dahmane S, Andrade R (1996) Muscarinic activation of a voltage-dependent cation nonselective current in rat association cortex. J Neurosci 16:3848-3861.
19. Haj-Dahmane S, Andrade R (1998) Ionic mechanism of the slow after depolarization induced by muscarinic receptor activation in rat prefrontal cortex. J Neurophysiol 80:1197-1210.
20. Halliwell JV (1989) Cholinergic responses in human neocortical neurones. EXS 57:138-149.
21. Hasselmo ME, Barkai E (1995) Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J Neurosci 15:6592-6604.
22. Hasselmo ME, Bower JM (1992) Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J Neurophysiol 67:1222-1229.
23. Hasselmo ME, Cekic M (1996) Suppression of synaptic transmission may allow combination of associative feedback and self-organizing feedforward connections in the neocortex. Behav Brain Res 79:153-161.
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. Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T, Schultz G (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397:259-263.
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. + currents. Neurosci Lett 231:13-16.
28. Kasa P, Rakonczay Z, Gulya K (1997) The cholinergic system in Alzheimer's disease. Prog Neurobiol 52:511-535.
29. Klink R, Alonso A (1997) Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. J Neurophysiol 77:1813-1828.
30. Krnjevic K, Pumain R, Renaud L (1971) The mechanism of excitation by acetylcholine in the cerebral cortex. J Physiol (Lond) 215:247-268.
31. 2+ waves in layer 2/3 and layer 5 rat neocortical pyramidal neurons. J Physiol (Lond) 549:471-488.
32. McCormick DA (1990) Cellular mechanisms of cholinergic control of neocortical and thalamic neuronal excitability. In: Brain cholinergic systems (Steriade M, Biesold D, eds), pp 236-264. Oxford: Oxford UP.
33. McCormick DA, Prince DA (1985) Two types of muscarinic response to acetylcholine in mammalian cortical neurons. Proc Natl Acad Sci USA 82:6344-6348.
34. McCormick DA, Prince DA (1986) Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol (Lond) 375:169-194.
35. McCormick DA, Williamson A (1989) Convergence and divergence of neurotransmitter action in human cerebral cortex. Proc Natl Acad Sci USA 86:8098-8102.
36. Metherate R, Cox CL, Ashe JH (1992) Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 12:4701-4711.
37. Mrzljak L, Pappy M, Leranth C, Goldman-Rakic PS (1995) Cholinergic synaptic circuitry in the macaque prefrontal cortex. J Comp Neurol 357:603-617.
38. Müller CM, Singer W (1989) Acetylcholine-induced inhibition in the cat visual cortex is mediated by a GABAergic mechanism. Brain Res 487:335-342.
39. Nishikawa M, Munakata M, Akaike N (1994) Muscarinic acetylcholine response in pyramidal neurones of rat cerebral cortex. Br J Pharmacol 112:1160-1166.
40. Ovsepian SV, Anwyl R, Rowan MJ (2004) Endogenous acetylcholine lowers the threshold for long-term potentiation induction in the CA1 area through muscarinic receptor activation: in vivo study. Eur J Neurosci 20:1267-1275.
41. Pepeu G, Giovannini MG (2004) Changes in acetylcholine extracellular levels during cognitive processes. Learn Mem 11:21-27.
42. Power JM, Sah P (2005) Intracellular calcium store filling by an L-type calcium current in the basolateral amygdala at subthreshold membrane potentials. J Physiol (Lond) 562:439-453.
43. Sah P, Faber ES (2002) Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol 66:345-353.
44. Schmitt H, Meves H (1993) Protein kinase C as mediator of arachidonic acid-induced decrease of neuronal M current. Pflügers Arch 425:134-139.
45. Schwindt PC, Spain WJ, Foehring RC, Chubb MC, Crill WE (1988) Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J Neurophysiol 59:450-467.
46. Shalinsky MH, Magistretti J, Ma L, Alonso AA (2002) Muscarinic activation of a cation current and associated current noise in entorhinal-cortex layer-II neurons. J Neurophysiol 88:1197-1211.
47. Smiley JF, Morrell F, Mesulam MM (1997) Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections. Exp Neurol 144:361-368.
48. 2+ signaling in mouse cortical neurons studied by two-photon imaging and photoreleased inositol triphosphate. J Neurosci 23:758-765.
49. 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.
50. Vinson PN, Justice Jr JB (1997) Effect of neostigmine on concentration and extraction fraction of acetylcholine using quantitative microdialysis. J Neurosci Methods 73:61-67.
51. 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.
52. Winkler J, Suhr ST, Gage FH, Thai LJ, Fisher LJ (1995) Essential role of neocortical acetylcholine in spatial memory. Nature 375:484-487.
53. 2+ release in a feedback regulation of pyramidal cell excitability. J Neurophysiol 91:2322-2329.
54. Yamamoto K, Hashimoto K, Nakano M, Shimohama S, Kato N (2002) A distinct form of calcium release down-regulates membrane excitability in neocortical pyramidal cells. Neuroscience 109:665-676.