Modes and models of forebrain cholinergic neuromodulation of cognition

Neuropsychopharmacology

Volumn 36, Issue 1, 2011, Pages 52-73

  Hasselmo, Michael E ^a   Sarter, Martin ^b  

^a BOSTON UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

acetylcholine; attention; cognition; cortex; encoding; hippocampus

Indexed keywords

ABT 107; ACETYLCHOLINE; ATROPINE; BUNGAROTOXIN RECEPTOR; CHOLINESTERASE INHIBITOR; GLUTAMIC ACID; MUSCARINIC AGENT; MUSCARINIC RECEPTOR; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA4BETA2; SCOPOLAMINE; UNCLASSIFIED DRUG;

ACETYLCHOLINE RELEASE; ALZHEIMER DISEASE; ASSOCIATION; ATTENTION; CELL FUNCTION; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE CELL; CHOLINERGIC TRANSMISSION; COGNITION; COGNITIVE DEFECT; DEMENTIA; DISEASE SEVERITY; ELECTRONEUROLOGY; FOREBRAIN; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; MEMORY; MENTAL DISEASE; MESOLIMBIC DOPAMINERGIC SYSTEM; MICRODIALYSIS; NEUROMODULATION; ORIENTATION; PREFRONTAL CORTEX; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PSYCHOPHARMACOLOGY; REVIEW; SENSORY STIMULATION; THALAMUS MEDIALIS CENTRALIS NUCLEUS; THETA RHYTHM; UPREGULATION;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; ATTENTION; CHOLINERGIC FIBERS; COGNITION; HUMANS; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; NEURONS; PERCEPTION; PROSENCEPHALON;

EID: 78649674046     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2010.104     Document Type: Review

References (296)

1. Aarsland D, Larsen JP, ReinVang I, Aasland AM (1994). Effects of cholinergic blockade on language in healthy young men. Brain 117: 1377-1384.
2. Aggleton JP, Brown MW (1999). Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22: 425-444.
3. Aigner TG, Mishkin M (1986). The effects of physostigmine and scopolamine on recognition memory in monkeys. Behav Neurosci 45: 81-87.
4. Aigner TG, Mitchell SJ, Aggleton JP, DeLong MR, Struble RG, Price DL et al (1987). Effects of scopolamine and physostigmine on recognition memory in monkeys with ibotenic-acid lesions of the nucleus basalis of Meynert. Psychopharmacology 92: 292-300.
5. Aigner TG, Walker DL, Mishkin M (1991). Comparison of the effects of scopolamine administered before and after acquisition in a test of visual recognition memory in monkeys. Behav Neural Biol 55: 61-67.
6. Alkondon M, Albuquerque EX (2002). A non-alpha7 nicotinic acetylcholine receptor modulates excitatory input to hippocampal CA1 interneurons. J Neurophysiol 87: 1651-1654.
7. Arnold HM, Burk JA, Hodgson EM, Sarter M, Bruno JP (2002). Differential cortical acetylcholine release in rats performing a sustained attention task versus behavioral control tasks that do not explicitly tax attention. Neuroscience 114: 451-460.
8. Atri A, Sherman S, Norman KA, Kirchhoff BA, Nicolas MM, Greicius MD et al (2004). Blockade of central cholinergic receptors impairs new learning and increases proactive interference in a word paired-associate memory task. Behav Neurosci 118: 223-236.
9. Auerbach JM, Segal M (1994). A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol 72: 2034-2040.
10. Azam L, Winzer-Serhan U, Leslie FM (2003). Co-expression of alpha7 and beta2 nicotinic acetylcholine receptor subunit mRNAs within rat brain cholinergic neurons. Neuroscience 119: 965-977.
11. Bandyopadhyay S, Sutor B, Hablitz JJ (2006). Endogenous acetylcholine enhances synchronized interneuron activity in rat neocortex. J Neurophysiol 95: 1908-1916.
12. Bang SJ, Brown TH (2009). Muscarinic receptors in perirhinal cortex control trace conditioning. J Neurosci 29: 4346-4350.
13. Barkai E, Hasselmo ME (1994). Modulation of the input/output function of rat piriform cortex pyramidal cells. J Neurophysiol 72: 644-658.
14. Bartus RT (2000). On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol 163: 495-529.
15. Baxter MG, Bucci DJ, Gorman LK, Wiley RG, Gallagher M (1995). Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. Behav Neurosci 109: 714-722.
16. Baxter MG, Bucci DJ, Holland PC, Gallagher M (1999). Impairments in conditioned stimulus processing and conditioned responding after combined selective removal of hippocampal and neocortical cholinergic input. Behav Neurosci 113: 486-495.
17. Baxter MG, Bucci DJ, Sobel TJ, Williams MJ, Gorman LK, Gallagher M (1996). Intact spatial learning following lesions of basal forebrain cholinergic neurons. NeuroReport 7: 1417-1420.
18. Beatty WW, Butters N, Janowsky DS (1986). Patterns of memory failure after scopolamine treatment: implications for cholinergic hypotheses of dementia. Behav Neural Biol 45: 196-211.
19. Behrends JC, ten Bruggencate G (1993). Cholinergic modulation of synaptic inhibition in the guinea pig hippocampus in vitro: excitation of GABAergic interneurons and inhibition of GABA-release. J Neurophysiol 69: 626-629.
20. Bentley P, Driver J, Dolan RJ (2008). Cholinesterase inhibition modulates visual and attentional brain responses in Alzheimer's disease and health. Brain 131: 409-424.
21. Bentley P, Driver J, Dolan RJ (2009). Modulation of fusiform cortex activity by cholinesterase inhibition predicts effects on subsequent memory. Brain 132: 2356-2371.
22. Bentley P, Husain M, Dolan RJ (2004). Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory. Neuron 41: 969-982.
23. Bentley P, Vuilleumier P, Thiel CM, Driver J, Dolan RJ (2003). Effects of attention and emotion on repetition priming and their modulation by cholinergic enhancement. J Neurophysiol 90: 1171-1181.
24. Berg DK, Conroy WG (2002). Nicotinic alpha 7 receptors: synaptic options and downstream signaling in neurons. J Neurobiol 53: 512-523.
25. Bitner RS, Bunnelle WH, Anderson DJ, Briggs CA, Buccafusco J, Curzon P et al (2007). Broad-spectrum efficacy across cognitive domains by alpha7 nicotinic acetylcholine receptor agonism correlates with activation of ERK1/2 and CREB phosphorylation pathways. J Neurosci 27: 10578-10587.
26. Bland BH, Colom LV (1993). Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol 41: 157-208.
27. 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.
28. Blokland A, Honig W, Raaijmakers WGM (1992). Effects of intra-hippocampal scopolamine injections in a repeated spatial acquisition task in the rat. Psychopharmacology 109: 373-376.
29. Bodick NC, Offen WW, Levey AI, Cutler NR, Gauthier SG, Satlin A et al (1997). Effects of xanomeline, a selective muscarinic receptor agonist on cognitive function and behavioral symptoms in Alzheimer's disease. Arch Neurol 54: 465-473.
30. Bogacz R, Brown MW (2003). Comparison of computational models of familiarity discrimination in the perirhinal cortex. Hippocampus 13: 494-524.
31. Botly LC, De Rosa E (2009). Cholinergic deafferentation of the neocortex using 192 IgG-saporin impairs feature binding in rats. J Neurosci 29: 4120-4130.
32. Bozzali M, MacPherson SE, Dolan RJ, Shallice T (2006). Left prefrontal cortex control of novel occurrences during recollection: a psychopharmacological study using scopolamine and event-related fMRI. Neuroimage 33: 286-295.
33. Briand LA, Gritton H, Howe WM, Young DA, Sarter M (2007). Modulators in concert for cognition: modulator interactions in the prefrontal cortex. Prog Neurobiol 83: 69-91.
34. Broks P, Preston GC, Traub M, Poppleton P, Ward C, Stahl SM (1988). Modelling dementia: effects of scopolamine on memory and attention. Neuropsychologia 26: 685-700.
35. Broussard JI, Karelina K, Sarter M, Givens B (2009). Cholinergic optimization of cue-evoked parietal activity during challenged attentional performance. Eur J Neurosci 29: 1711-1722.
36. Browning PG, Gaffan D, Croxson PL, Baxter MG (2010). Severe scene learning impairment, but intact recognition memory, after cholinergic depletion of inferotemporal cortex followed by fornix transection. Cereb Cortex 20: 282-293.
37. Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB et al (2002). Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296: 2243-2246.
38. 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.
39. Burgess N, Barry C, O'Keefe J (2007). An oscillatory interference model of grid cell firing. Hippocampus 17: 801-812.
40. Burmeister JJ, Moxon K, Gerhardt GA (2000). Ceramic-based multisite microelec-trodes for electrochemical recordings. Anal Chem 72: 187-192.
41. Bussey TJ, Duck J, Muir JL, Aggleton JP (2000). Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behav Brain Res 111: 187-202.
42. Buzsaki G (2002). Theta oscillations in the hippocampus. Neuron 33: 325-340.
43. Chapman CA, Lacaille JC (1999). Cholinergic induction of theta-frequency oscillations in hippocampal inhibitory interneurons and pacing of pyramidal cell firing. J Neurosci 19: 8637-8645.
44. Chappell J, McMahan R, Chiba AA, Gallagher M (1998). A re-examination of the role of basal forebrain cholinergic neurons in spatial working memory. Neuropharmacol 37: 481-487.
45. Chen KC, Baxter MG, Rodefer JS (2004). Central blockade of muscarinic cholinergic receptors disrupts affective and attentional set-shifting. Eur J Neurosci 20: 1081-1088.
46. Chiba AA, Bucci DJ, Holland PC, Gallagher M (1995). Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing. J Neurosci 15: 7315-7322.
47. Chiba AA, Bushnell PJ, Oshiro WM, Gallagher M (1999). Selective removal of cholinergic neurons in the basal forebrain alters cued target detection. NeuroReport 29: 3119-3123.
48. Christensen H, Maltby N, Jorm AF, Creasey H, Broe GA (1992). Cholinergic blockade as a model of the cognitive deficits in Alzheimer's disease. Brain 115: 1681-1699.
49. Christophe E, Roebuck A, Staiger JF, Lavery DJ, Charpak S, Audinat E (2002). Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons. J Neurophysiol 88: 1318-1327.
50. Cole AE, Nicoll RA (1984). Characterization of a slow cholinergic postsynaptic potential recorded in vitro from rat hippocampal pyramidal cells. J Physiol (London) 352: 173-188.
51. Crick F (1984). Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci USA 81: 4586-4590.
52. Dalley JW, McGaughy J, O'Connell MT, Cardinal RN, Levita L, Robbins TW (2001). Distinct changes in cortical acetylcholine and noradrenaline efflux during contingent and noncontingent performance of a visual attentional task. J Neurosci 21: 4908-4914.
53. Dalley JW, Theobald DE, Bouger P, Chudasama Y, Cardinal RN, Robbins TW (2004). Cortical cholinergic function and deficits in visual attentional performance in rats following 192 IgG-saporin-induced lesions of the medial prefrontal cortex. Cereb Cortex 14: 922-932.
54. Davidson MC, Cutrell EB, Marrocco RT (1999). Scopolamine slows the orienting of attention in primates to cued visual targets. Psychopharmacology 142: 1-8.
55. Davidson MC, Marrocco RT (2000). Local infusion of scopolamine into intraparietal cortex slows covert orienting in rhesus monkeys. J Neurophysiol 83: 1536-1549.
56. Deco G, Thiele A (2009). Attention - oscillations and neuropharmacology. Eur J Neurosci 30: 347-354.
57. Deutsch JA (1971). The cholinergic synapse and the site of memory. Science 174: 788-794.
58. Deutsch JA, Rocklin KW (1967). Amnesia induced by scopolamine and its temporal variations. Nature 216: 89-90.
59. Dickinson JA, Kew JN, Wonnacott S (2008). Presynaptic alpha 7- and beta 2-containing nicotinic acetylcholine receptors modulate excitatory amino acid release from rat prefrontal cortex nerve terminals via distinct cellular mechanisms. Mol Pharmacol 74: 348-359.
60. Disney AA, Aoki C (2008). Muscarinic acetylcholine receptors in macaque V1 are most frequently expressed by parvalbumin-immunoreactive neurons. J Comp Neurol 507: 1748-1762.
61. Disney AA, Aoki C, Hawken MJ (2007). Gain modulation by nicotine in macaque v1. Neuron 56: 701-713.
62. Drachman DA (1977). Memory and cognitive function in man: does the cholinergic system have a specific role? Neurology 27: 783-790.
63. Drachman DA, Sahakian BJ (1980). Memory and cognitive function in the elderly. A preliminary trial of physostigmine. Arch Neurol 37: 674-675.
64. Duffy AM, Zhou P, Milner TA, Pickel VM (2009). Spatial and intracellular relationships between the alpha7 nicotinic acetylcholine receptor and the vesicular acetylcho-line transporter in the prefrontal cortex of rat and mouse. Neuroscience 161: 1091-1103.
65. Dunbar GC, Inglis F, Kuchibhatla R, Sharma T, Tomlinson M, Wamsley J (2007). Effect of ispronicline, a neuronal nicotinic acetylcholine receptor partial agonist, in subjects with age associated memory impairment (AAMI). J Psychopharmacol 21: 171-178.
66. Dunne MP, Hartley LR (1986). Scopolamine and the control of attention in humans. Psychopharmacology 89: 94-97.
67. Dunnett SB, Everitt BJ, Robbins TW (1991). The basal forebrain-cortical cholinergic system: interpreting the functional consequences of excitotoxic lesions. Trends Neurosci 14: 494-501.
68. Easton A, Ridley RM, Baker HF, Gaffan D (2002). Unilateral lesions of the cholinergic basal forebrain and fornix in one hemisphere and inferior temporal cortex in the opposite hemisphere produce severe learning impairments in rhesus monkeys. Cereb Cortex 12: 729-736.
69. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA (2002). Graded persistent activity in entorhinal cortex neurons. Nature 420: 173-178.
70. Ellis JR, Ellis KA, Bartholomeusz CF, Harrison BJ, Wesnes KA, Erskine FF et al (2006). Muscarinic and nicotinic receptors synergistically modulate working memory and attention in humans. Int J Neuropsychopharmacol 9: 175-189.
71. Ennaceur A, Neave N, Aggleton JP (1996). Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav Brain Res 80: 9-25.
72. Erskine FF, Ellis JR, Ellis KA, Stuber E, Hogan K, Miller V et al (2004). Evidence for synergistic modulation of early information processing by nicotinic and muscarinic receptors in humans. Human Psychopharmacol Clin Exp 19: 503-509.
73. Esclassan F, Coutureau E, Di Scala G, Marchand AR (2009). A cholinergic-dependent role for the entorhinal cortex in trace fear conditioning. J Neurosci 29: 8087-8093.
74. Demonstrates the specific role of entorhinal cortex in trace conditioning, and shows that local infusion of an M1 antagonist impairs trace conditioning. Fibiger HC (1991). Cholinergic mechanisms in learning, memory and dementia: a review of recent evidence. Trends Neurosci 14: 220-223.
75. Flicker C, Feris SH, Serby M (1992). Hypersensitivity to scopolamine in the elderly. Psychopharmacology 107: 437-441.
76. Foldi NS, White RE, Schaefer LA (2005). Detecting effects of donepezil on visual selective attention using signal detection parameters in Alzheimer's disease. Int J Geriatr Psychiat 20: 485-488.
77. Foster TC, Deadwyler SA (1992). Acetylcholine modulates averaged sensory evoked responses and perforant path evoked field potentials in the rat dentate gyrus. Brain Res 587: 95-101.
78. Fransen E, Alonso AA, Hasselmo ME (2002). Simulations of the role of the muscarinic-activated calcium-sensitive nonspecific cation current INCM in entorhinal neuronal activity during delayed matching tasks. J Neurosci 22: 1081-1097.
79. Fransen E, Tahvildari B, Egorov AV, Hasselmo ME, Alonso AA (2006). Mechanism of graded persistent cellular activity of entorhinal cortex layer v neurons. Neuron 49: 735-746.
80. Fraser DD, MacVicar BA (1996). Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci 16: 4113-4128.
81. Freedman R, Olincy A, Buchanan RW, Harris JG, Gold JM, Johnson L et al (2008). Initial phase 2 trial of a nicotinic agonist in schizophrenia. Am J Psychiatry 165: 1040-1047.
82. Frick KM, Kim JJ, Baxter MG (2004). Effects of complete immunotoxin lesions of the cholinergic basal forebrain on fear conditioning and spatial learning. Hippocampus 14: 244-254.
83. Furey ML, Pietrini P, Haxby JV (2000). Cholinergic enhancement and increased selectivity of perceptual processing during working memory. Science 290: 2315-2319.
84. Furey ML, Pietrini P, Haxby JV, Drevets WC (2008). Selective effects of cholinergic modulation on task performance during selective attention. Neuropsychophar-macology 33: 913-923.
85. Gaffan D, Harrison S (1989). Place memory and scene memory: effects of fornix transection in the monkey. Exp Brain Res 74: 202-212.
86. Gais S, Born J (2004). Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc Natl Acad Sci USA 101: 2140-2144.
87. Galani R, Lehmann O, Bolmont T, Aloy E, Bertrand F, Lazarus C et al (2002). Selective immunolesions of CH4 cholinergic neurons do not disrupt spatial memory in rats. Physiol Behav 76: 75-90.
88. Ghoneim MM, Mewaldt SP (1975). Effects of diazepam and scopolamine on storage, retrieval and organizational processes in memory. Psychopharmacolo-gia 44: 257-262.
89. Ghoneim MM, Mewaldt SP (1977). Studies on human memory: the interactions of diazepam, scopolamine, and physostigmine. Psychopharmacology 52: 1-6.
90. Giessing C, Fink GR, Rosler F, Thiel CM (2007). fMRI data predict individual differences of behavioral effects of nicotine: a partial least square analysis. J Cogn Neurosci 19: 658-670.
91. Giessing C, Thiel CM, Rosler F, Fink GR (2006). The modulatory effects of nicotine on parietal cortex activity in a cued target detection task depend on cue reliability. Neuroscience 137: 853-864.
92. Gil Z, Conners BW, Amitai Y (1997). Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19: 679-686.
93. Gill TM, Sarter M, Givens B (2000). Sustained visual attention performance-associated prefrontal neuronal activity: evidence for cholinergic modulation. J Neurosci 20: 4745-4757.
94. Gioanni Y, Rougeot C, Clarke PB, Lepouse C, Thierry AM, Vidal C (1999). Nicotinic receptors in the rat prefrontal cortex: increase in glutamate release and facilitation of mediodorsal thalamo-cortical transmission. Eur J Neurosci 11: 18-30.
95. Giocomo LM, Hasselmo ME (2005). Nicotinic modulation of glutamatergic synaptic transmission in region CA3 of the hippocampus. Eur J Neurosci 22: 1349-1356.
96. Giuliano C, Parikh V, Ward JR, Chiamulera C, Sarter M (2008). Increases in cholinergic neurotransmission measured by using choline-sensitive microelec-trodes: enhanced detection by hydrolysis of acetylcholine on recording sites? Neurochem Int 52: 1343-1350.
97. Givens BS, Olton DS (1990). Cholinergic and GABAergic modulation of the medial septal area: effect on working memory. Behav Neurosci 104: 849-855.
98. Grasby PM, Frith CD, Paulesu E, Friston KJ, Frackowiak RS, Dolan RJ (1995). The effect of the muscarinic antagonist scopolamine on regional cerebral blood flow during the performance of a memory task. Exp Brain Res 104: 337-348.
99. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996). Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383: 713-716.
100. Green A, Ellis KA, Ellis J, Bartholomeusz CF, Ilic S, Croft RJ et al (2005). Muscarinic and nicotinic receptor modulation of object and spatial n-back working memory in humans. Pharmacol Biochem Behav 81: 575-584.
101. Greenwood PM, Lin MK, Sundararajan R, Fryxell KJ, Parasuraman R (2009). Synergistic effects of genetic variation in nicotinic and muscarinic receptors on visual attention but not working memory. Proc Natl Acad Sci USA 106: 3633-3638.
102. Grottick AJ, Higgins GA (2000). Effect of subtype selective nicotinic compounds on attention as assessed by the five-choice serial reaction time task. Behav Brain Res 117: 197-208.
103. Guillery RW, Feig SL, Lozsadi DA (1998). Paying attention to the thalamic reticular nucleus. Trends Neurosci 21: 28-32.
104. Gulledge AT, Bucci DJ, Zhang SS, Matsui M, Yeh HH (2009). M1 receptors mediate cholinergic modulation of excitability in neocortical pyramidal neurons. J Neurosci 28: 9888-9902.
105. Gulledge AT, Stuart GJ (2005). Cholinergic inhibition of neocortical pyramidal neurons. J Neurosci 25: 10308-10320.
106. Hahn B, Sharples CG, Wonnacott S, Shoaib M, Stolerman IP (2003). Attentional effects of nicotinic agonists in rats. Neuropharmacology 44: 1054-1067.
107. Haj-Dahmane S, Andrade R (1996). Muscarinic activation of a voltage-dependent cation nonselective current in rat association cortex. J Neurosci 16: 3848-3861.
108. Haj-Dahmane S, Andrade R (1997). Calcium-activated cation nonselective current contributes to the fast afterdepolarization in rat prefrontal cortex neurons. J Neurophysiol 78: 1983-1989.
109. Haj-Dahmane S, Andrade R (1998). Ionic mechanism of the slow afterdepolarization induced by muscarinic receptor activation in rat prefrontal cortex. J Neurophysiol 80: 1197-1210.
110. Hallanger AE, Levey AI, Lee HJ, Rye DB, Wainer BH (1987). The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 262: 105-124.
111. Hasselmo ME (1999). Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3: 351-359.
112. Hasselmo ME (2006). The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16: 710-715.
113. Hasselmo ME (2008). Temporally structured replay of neural activity in a model of entorhinal cortex, hippocampus and postsubiculum. Eur J Neurosci 28: 1301-1315.
114. Hasselmo ME (2009). A model of episodic memory: mental time travel along encoded trajectories using grid cells. Neurobiol Learn Mem 92: 559-573.
115. Hasselmo ME, Anderson BP, Bower JM (1992). Cholinergic modulation of cortical associative memory function. J Neurophysiol 67: 1230-1246.
116. Hasselmo ME, Bower JM (1992). Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J Neurophysiol 67: 1222-1229.
117. Hasselmo ME, Bower JM (1993). Acetylcholine and memory. Trends Neurosci 16: 218-222.
118. 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.
119. 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.
120. Hasselmo ME, Schnell E (1994). Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 14: 3898-3914.
121. Hasselmo ME, Schnell E, Barkai E (1995). Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci 15: 5249-5262.
122. Hasselmo ME, Stern CE (2006). Mechanisms underlying working memory for novel information. Trends Cogn Sci 10: 487-493.
123. Herreras O, Solis JM, Herranz AS, Martin del Rio R, Lerma J (1988). Sensory modulation of hippocampal transmission. II. Evidence for a cholinergic locus of inhibition in the Schaffer-CA1 synapse. Brain Res 461: 303-313.
124. Herrero JL, Roberts MJ, Delicato LS, Gieselmann MA, Dayan P, Thiele A (2008). Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature 454: 1110-1114.
125. Herzog CD, Nowak KA, Sarter M, Bruno JP (2003). Microdialysis without acetylcholinesterase inhibition reveals an age-related attenuation in stimulated cortical acetylcholine release. Neurobiol Aging 24: 861-863.
126. Heys JG, Giocomo LM, Hasselmo ME (2010). Cholinergic modulation of the resonance properties of stellate cells in layer II of medial entorhinal cortex. J Neurophysiol 104: 258-270.
127. Himmelheber AM, Sarter M, Bruno JP (1997). Operant performance and cortical acetylcholine release: role of response rate, reward density, and non-contingent stimuli. Brain Res Cogn Brain Res 6: 23-36.
128. Himmelheber AM, Sarter M, Bruno JP (2000). Increases in cortical acetylcholine release during sustained attention performance in rats. Cogn Brain Res 9: 313-325.
129. Hounsgaard J (1978). Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus. Exp Neurol 62: 787-797.
130. Howe WM, Ji J, Parikh V, Williams S, Mocaer E, Trocme-Thibierge C et al (2010). Enhanced attentional performance by selective stimulation of a4b2* nAChRs: underlying cholinergic mechanisms. Neuropsychopharmacology 35: 1391-1401.
131. Howe WM, Parikh V, Martinez V, Sarter M (2007). Prefrontal cholinergic switching from associational processing to cue detection: evidence from sub-second measures of prefrontal cholinergic neurotransmission, using choline-sensitive microelectrodes, in animals performing an operant sustained attention task. . Society for Neuroscience Annual Meeting: San Diego, CA.
132. Hoyle E, Genn RF, Fernandes C, Stolerman IP (2006). Impaired performance of alpha7 nicotinic receptor knockout mice in the five-choice serial reaction time task. Psychopharmacology (Berl) 189: 211-223.
133. Hsieh CY, Cruikshank SJ, Metherate R (2000). Differential modulation of auditory thalamocortical and intracortical synaptic transmission by cholinergic agonist. Brain Res 880: 51-64.
134. Huff FJ, Mickel SF, Corkin S, Growdon JH (1988). Cognitive functions affected by scopolamine in Alzheimer's disease and normal aging. Drug Develop Res 12: 271-278.
135. Hurst RS, Hajos M, Raggenbass M, Wall TM, Higdon NR, Lawson JA et al (2005). A novel positive allosteric modulator of the alpha7 neuronal nicotinic acetylcho-line receptor: in vitro and in vivo characterization. J Neurosci 25: 4396-4405.
136. Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL (1984). Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225: 1168-1170.
137. Isaac JT, Buchanan KA, Muller RU, Mellor JR (2009). Hippocampal place cell firing patterns can induce long-term synaptic plasticity in vitro. J Neurosci 29: 6840-6850.
138. Ji J, Maren S (2008). Differential roles for hippocampal areas CA1 and CA3 in the contextual encoding and retrieval of extinguished fear. Learn Mem 15: 244-251.
139. Keefe RS, Malhotra AK, Meltzer HY, Kane JM, Buchanan RW, Murthy A et al (2008). Efficacy and safety of donepezil in patients with schizophrenia or schizoaffective disorder: significant placebo/practice effects in a 12-week, randomized, double-blind, placebo-controlled trial. Neuropsychopharmacology 33: 1217-1228.
140. Keefe RSE, Vinogradov S, Medalia A, Silverstein SM, Bell MD, Dickinson D et al (2010). Report form the working group conference on multisite trial design for cognitive remediation in schizophrenia. Schizophren Bull, in press (e-pub ahead of print
141. Kimura F (2000). Cholinergic modulation of cortical function: a hypothetical role in shifting the dynamics in cortical network. Neurosci Res 38: 19-26.
142. Kimura F, Baughman RW (1997). Distinct muscarinic receptor subtypes suppress excitatory and inhibitory synaptic responses in cortical neurons. J Neurophysiol 77: 709-716.
143. Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF (1999). Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 19: 1599-1609.
144. Kitt CA, Hohmann C, Coyle JT, Price DL (1994). Cholinergic innervation of mouse forebrain structures. J Comp Neurol 341: 117-129.
145. 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.
146. Kohler CG, Martin EA, Kujawski E, Bilker W, Gur RE, Gur RC (2007). No effect of donepezil on neurocognition and social cognition in young persons with stable schizophrenia. Cogn Neuropsychiatry 12: 412-421.
147. Kopelman MD, Corn TH (1988). Cholinergic 'blockade' as a model for cholinergic depletion. A comparison of the memory deficits with those of Alzheimer-type dementia and the alcoholic Korsakoff syndrome. Brain 111: 1079-1110.
148. Kozak R, Bruno JP, Sarter M (2006). Augmented prefrontal acetylcholine release during challenged attentional performance. Cereb Cortex 16: 9-17.
149. Kozak R, Martinez V, Young D, Brown H, Bruno JP, Sarter M (2007). Toward a neuro-cognitive animal model of the cognitive symptoms of schizophrenia: disruption of cortical cholinergic neurotransmission following repeated amphetamine exposure in attentional task-performing, but not non-performing, rats. Neuropsychopharmacology 32: 2074-2086.
150. Kremin T, Hasselmo ME (2007). Cholinergic suppression of glutamatergic synaptic transmission in hippocampal region CA3 exhibits laminar selectivity: implication for hippocampal network dynamics. Neuroscience 149: 760-767.
151. Krnjevic K, Pumain R, Renaud L (1971). The mechanism of excitation by acetylcholine in the cerebral cortex. J Physiol 215: 247-268.
152. Kukolja J, Thiel CM, Fink GR (2009). Cholinergic stimulation enhances neural activity associated with encoding but reduces neural activity associated with retrieval in humans. J Neurosci 29: 8119-8128.
153. Lambe EK, Picciotto MR, Aghajanian GK (2003). Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychophar-macology 28: 216-225.
154. Lawrence JJ, Grinspan ZM, Statland JM, McBain CJ (2006a). Muscarinic receptor activation tunes mouse stratum oriens interneurones to amplify spike reliability. J Physiol 571: 555-562.
155. Lawrence JJ, Statland JM, Grinspan ZM, McBain CJ (2006b). Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones. J Physiol 570: 595-610.
156. Lawson VH, Bland BH (1993). The role of the septohippocampal pathway in the regulation of hippocampal field activity and behavior: analysis by the intraseptal microinfusion of carbachol, atropine, and procaine. Exp Neurol 120: 132-144.
157. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsaki G (1994). Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62: 1033-1047.
158. Leiser SC, Bowlby MR, Comery TA, Dunlop J (2009). A cog in cognition: how the alpha7 nicotinic acetylcholine receptor is geared towards improving cognitive deficits. Pharmacol Ther 122: 302-311.
159. Leung VL, Zhao Y, Brown TH (2006). Graded persistent firing in neurons of rat perirhinal cortex. Soc Neurosci Abstr 32: 636.618.
160. Levin ED, Conners CK, Silva D, Hinton SC, Meck WH, March J et al (1998). Transdermal nicotine effects on attention. Psychopharmacology (Berl) 140: 135-141.
161. Levin ED, McClernon FJ, RezVani AH (2006). Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology 184: 523-539.
162. Little JT, Johnson DN, Minichiello M, Weingartner H, Sunderland T (1998). Combined nicotinic and muscarinic blockade in elderly normal volunteers: cognitive, behavioral, and physiologic responses. Neuropsychopharmacology 19: 60-69.
163. Lysakowski A, Wainer BH, Bruce G, Hersh LB (1989). An atlas of the regional and laminar distribution of choline acetyltransferase immunoreactivity in rat cerebral cortex. Neuroscience 28: 291-336.
164. Maclean KA, Aichele SR, Bridwell DA, Mangun GR, Wojciulik E, Saron CD (2009). Interactions between endogenous and exogenous attention during vigilance. Atten Percept Psychophys 71: 1042-1058.
165. Madison DV, Lancaster B, Nicoll RA (1987). Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7: 733-741.
166. Madison DV, Nicoll RA (1984). Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J Physiol 354: 319-331.
167. Marrosu F, Portas C, Mascia MS, Casu MA, Fa M, Giagheddu M et al (1995). Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671: 329-332.
168. Martin LF, Kem WR, Freedman R (2004). Alpha-7 nicotinic receptor agonists: potential new candidates for the treatment of schizophrenia. Psychopharmacol-ogy 174: 54-64.
169. McAlonan K, CaVanaugh J, Wurtz RH (2006). Attentional modulation of thalamic reticular neurons. J Neurosci 26: 4444-4450.
170. McGaughy J, Decker MW, Sarter M (1999). Enhancement of sustained attention performance by the nicotinic acetylcholine receptor agonist ABT-418 in intact but not basal forebrain-lesioned rats. Psychopharmacology 144: 175-182.
171. McGaughy J, Everitt BJ, Robbins TW, Sarter M (2000). The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotox-ins. Behav Brain Res 115: 251-263.
172. McGaughy J, Kaiser T, Sarter M (1996). Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav Neurosci 110: 247-265.
173. McGaughy J, Koene RA, Eichenbaum H, Hasselmo ME (2005). Cholinergic deafferentation of the entorhinal cortex in rats impairs encoding of novel but not familiar stimuli in a delayed nonmatch-to-sample task. J Neurosci 25: 10273-10281.
174. McGaughy J, Sarter M (1998). Sustained attention performance in rats with
175. McQuiston AR, Madison DV (1999a). Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J Neurosci 19: 2887-2896.
176. McQuiston AR, Madison DV (1999b). Muscarinic receptor activity induces an afterdepolarization in a subpopulation of hippocampal CA1 interneurons. J Neurosci 19: 5703-5710.
177. McQuiston AR, Madison DV (1999c). Muscarinic receptor activity has multiple effects on the resting membrane potentials of CA1 hippocampal interneurons. J Neurosci 19: 5693-5702.
178. Mesulam M (2004). The cholinergic lesion of Alzheimer's disease: pivotal factor or side show? Learn Mem 11: 43-49.
179. Mesulam MM, Hersh LB, Mash DC, Geula C (1992). Differential cholinergic innervation within functional subdivisions of the human cerebral cortex: a choline acetyltransferase study. J Comp Neurol 318: 316-328.
180. M'Harzi M, Palacios A, Monmaur P, Willig F, Houcine O, Delacour J (1987). Effects of selective lesions of fimbria-fornix on learning set in the rat. Physiol Behav 40: 181-188.
181. Miller EK, Desimone R (1993). Scopolamine affects short-term memory but not inferior temporal neurons. NeuroReport 4: 81-84.
182. Mitchell JF, Sundberg KA, Reynolds JH (2007). Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55: 131-141.
183. Mizumori SJY, Barnes CA, McNaughton BL (1989). Reversible inactivation of the medial septum - selective effects on the spontaneous unit-activity of different hippocampal cell-types. Brain Res 500: 99-106.
184. Molchan SE, Martinez RA, Hill JL, Weingartner HJ, Thompson K, Vitiello B et al (1992). Increased cognitive sensitivity to scopolamine with age and a perspective on the scopolamine model. Brain Res Rev 17: 215-226.
185. Monmaur P, Collet A, Puma C, Frankel-Kohn L, Sharif A (1997). Relations between acetylcholine release and electrophysiological characteristics of theta rhythm: a microdialysis study in the urethane-anesthetized rat hippocampus. Brain Res Bull 42: 141-146.
186. Muir JL, Dunnett SB, Robbins TW, Everitt BJ (1992). Attentional functions of the forebrain cholinergic systems: effects of intraventricular hemicholinium, physos-tigmine, basal forebrain lesions and intracortical grafts on a multiple-choice serial reaction time task. Exp Brain Res 89: 611-622.
187. Nelson CL, Sarter M, Bruno JP (2005). Prefrontal cortical modulation of acetylcholine release in posterior parietal cortex. Neuroscience 132: 347-359.
188. Newman LA, McGaughy J (2008). Cholinergic deafferentation of prefrontal cortex increases sensitivity to cross-modal distractors during a sustained attention task. J Neurosci 28: 2642-2650.
189. Newhouse PA, Potter A, Kelton M, Corwin J (2001). Nicotinic treatment of Alzheimer's disease. Biol Psychiat 49: 268-278.
190. Newhouse PA, Potter A, Singh A (2004). Effects of nicotinic stimulation on cognitive performance. Curr Opin Pharmacol 4: 36-46.
191. Nilsson OG, Shapiro ML, Gage FH, Olton DS, Bjorklund A (1987). Spatial learning and memory following fimbria-fornix transection and grafting of fetal septal neurons to the hippocampus. Exp Brain Res 67: 195-215.
192. Nissen MJ, Knopman DS, Schacter DL (1987). Neurochemical dissociation of memory systems. Neurology 37: 789-794.
193. Pang KC, Nocera R (1999). Interactions between 192-IgG saporin and intraseptal cholinergic and GABAergic drugs: role of cholinergic medial septal neurons in spatial working memory. Behav Neurosci 113: 265-275.
194. Pang KC, Nocera R, Secor AJ, Yoder RM (2001). GABAergic septohippocampal neurons are not necessary for spatial memory. Hippocampus 11: 814-827.
195. Paolone G, Ji J, Williams S, Howe WM, Ward J, Parikh V et al (2009). Effects of the selective alpha 7 nAChR agonist ABT-107 on prefrontal glutamatergic and cholinergic activity and attentional performance. Society for Neuroscience Annual Meeting. Chicago, IL.
196. Parikh V, Ji J, Decker MW, Sarter M (2010). Prefrontal b2 subunit-containing and a7 nAChRs differentially control prefrontal glutamatergic and cholinergic signaling. J Neurosci 30: 2518-3530.
197. Parikh V, Kozak R, Martinez V, Sarter M (2007). Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 56: 141-154.
198. Parikh V, Man K, Decker MW, Sarter M (2008). Glutamatergic contributions to nicotinic acetylcholine receptor agonist-evoked cholinergic transients in the prefrontal cortex. J Neurosci 28: 3769-3780.
199. Parikh V, Pomerleau F, Huettl P, Gerhardt GA, Sarter M, Bruno JP (2004). Rapid assessment of in vivo cholinergic transmission by amperometric detection of changes in extracellular choline levels. Eur J Neurosci 20: 1545-1554.
200. Parikh V, Sarter M (2008). Cholinergic mediation of attention: contributions of phasic and tonic increases in prefrontal cholinergic activity. Ann NY Acad Sci 1129: 225-235.
201. Parrott AC (1986). The effects of transdermal scopolamine and four dose levels of oral scopolamine (0.15, 0.3, 0.6, and 1.2 mg) upon psychological performance. Psychopharmacology 89: 347-354.
202. Passetti F, Dalley JW, O'Connell MT, Everitt BJ, Robbins TW (2000). Increased acetylcholine release in the rat medial prefrontal cortex during performance of a visual attentional task. Eur J Neurosci 12: 3051-3058.
203. Patil MM, Hasselmo ME (1999). Modulation of inhibitory synaptic potentials in the piriform cortex. J Neurophysiol 81: 2103-2118.
204. Pazzagli A, Pepeu G (1965). Amnesic properties of scopolamine and brain acetylcholine in the rat. Int J Neuropharmacol 4: 291-299.
205. Penetar DM, McDonough JH (1983). Effects of cholinergic drugs on delayed match to sample performance of Rhesus monkeys. Pharmacol Biochem Behav 19: 963-967.
206. Pepeu G, GioVannini MG (2009). Cholinesterase inhibitors and beyond. Curr Alzheimer Res 6: 86-96.
207. Perry E, Walker M, Grace J, Perry R (1999). Acetylcholine in mind: a neurotransmitter correlate of consciousness? Trends Neurosci 22: 273-280.
208. Petersen RC (1977). Scopolamine induced learning failures in man. Psychophar-macology 52: 283-289.
209. Phillips JM, McAlonan K, Robb WGK, Brown VJ (2000). Cholinergic neurotransmis-sion influences covert orientation of visuospatial attention in the rat. Psychopharmacology 150: 112-116.
210. Pinault D (2004). The thalamic reticular nucleus: structure, function and concept. Brain Res Rev 46: 1-31.
211. Pitler TA, Alger BE (1992). Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol 450: 127-142.
212. Posner MI (1980). Orienting of attention. Quart J Expl Psychol 32: 3 ##. Posner MI (2008). Measuring alertness. In: Pfaff DW, Kieffer BL (eds). Molecular and Biophysical Mechanisms of Arousal, Alertness, and Attention. Blackwell Publishing: Boston, MA, 1129: 193-199.
213. Posner MI, Rothbart MK (2007). Research on attention networks as a model for the integration of psychological science. Ann Rev Psychol 58: 1-23.
214. Posner MI, Snyder CRR, Davidson BJ (1980). Attention and the detection of signals. J Exp Psychol 109: 160-174.
215. Potter A, Corwin J, Lang J, Piasecki M, Lenox R, Newhouse PA (1999). Acute effects of the selective cholinergic channel activator (nicotinic agonist) ABT-418 in Alzheimer's disease.
216. Psychopharmacology (Berl) 142: 334-342.
217. Radcliffe KA, Dani JA (1998). Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18: 7075-7083.
218. Raffaele KC, Asthana S, Berardi A, Haxby JV, Morris PP, Schapiro MB et al (1996). Differential response to the cholinergic agonist arecoline among different cognitive modalities in Alzheimer's disease. Neuropsychopharmacology 15: 163-170.
219. Rasch BH, Born J, Gais S (2006). Combined blockade of cholinergic receptors shifts the brain from stimulus encoding to memory consolidation. J Cogn Neurosci 18: 793-802.
220. Rasmusson DD, Smith SA, Semba K (2007). Inactivation of prefrontal cortex abolishes cortical acetylcholine release evoked by sensory or sensory pathway stimulation in the rat. Neuroscience 149: 232-241.
221. Robbins TW, Everitt BJ, Marston HM, Wilkinson J, Jones GH, Page KJ (1989). Comparative effects of ibotenic acid- and quisqualic acid-induced lesions of the substantia innominata on attentional function in the rat: further implications for the role of the cholinergic neurons of the nucleus basalis in cognitive processes. Behav Brain Res 35: 221-240.
222. Robbins TW, Mehta MA, Sahakian BJ (2000). Neuroscience. Boosting working memory. Science 290: 2275-2276.
223. Robbins TW, Semple J, Kumar R, Truman MI, Shorter J, Ferraro A et al (1997). Effects of scopolamine on delayed-matching-to-sample and paired associates tests of visual memory and learning in human subjects: comparison with diazepam and implications for dementia. Psychopharmacology (Berl) 134: 95-106.
224. Roberts AC, Robbins TW, Everitt BJ, Muir JL (1992). A specific form of cognitive rigidity following excitotoxic lesions of the basal forebrain in marmosets. Neuroscience 47: 251-264.
225. Roberts MJ, Thiele A (2008). Spatial integration and its moderation by attention and acetylcholine. Front Biosci 13: 3742-3759.
226. 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.
227. Rogers JL, Kesner RP (2003). Cholinergic modulation of the hippocampus during encoding and retrieval. Neurobiol Learn Mem 80: 332-342.
228. Rogers JL, Kesner RP (2004). Cholinergic modulation of the hippocampus during encoding and retrieval of tone/shock-induced fear conditioning. Learn Mem 11: 102-107.
229. Rosier AM, Cornette L, Dupont P, Bormans G, Mortelmans L, Orban GA (1999). Regional brain activity during shape recognition impaired by a scopolamine challenge to encoding. Eur J Neurosci 11: 3701-3714.
230. Rusted JM, Caulfield D, King L, Goode A (2000). Moving out of the laboratory: does nicotine improve everyday attention? Behav Pharmacol 11: 621-629.
231. Rusted JM, Warburton DM (1992). Facilitation of memory by post-trial administration of nicotine: evidence for an attentional explanation. Psychopharmacology 108: 452-455.
232. Rye DB, Wainer BH, Mesulam MM, Mufson EJ, Saper CB (1984). Cortical projections arising from the basal forebrain: a study of cholinergic and non-cholinergic components employing combined retrograde tracing and immuno-histochemical localization of choline acetyltransferase. Neuroscience 13: 627-643.
233. Sahakian BJ, Owen AM, Morant NJ, Eagger SA, Boddington S, Crayton L et al (1993). Further analysis of the cognitive effects of tetrahydroaminoacridine (THA) in Alzheimer's disease: assessment of attentional and mnemonic function using CANTAB. Psychopharmacology 110: 395-401.
234. Sarter M (2010). Attention. In: Stolerman I (ed). Encyclopedia of Psycho-pharmacology. Springer, Berlin, in press.
235. Sarter M, Bruno JP (1997). Trans-synaptic stimulation of cortical acetylcholine and enhancement of attentional functions: a rational approach for the development of cognition enhancers. Behav Brain Res 83: 7-14.
236. Sarter M, Bruno JP (2002). Mild cognitive impairment and the cholinergic hypothesis: a very different take on recent data. Ann Neurol 52: 384-385.
237. Sarter M, Bruno JP, Parikh V (2007). Abnormal neurotransmitter release underlying behavioral and cognitive disorders: toward concepts of dynamic and function-specific dysregulation. Neuropsychopharmacology 32: 1452-1461.
238. Sarter M, Gehring WJ, Kozak R (2006). More attention must be paid: the neurobiology of attentional effort. Brain Res Rev 51: 145-160.
239. Sarter M, Nelson CL, Bruno JP (2005). Cortical cholinergic transmission and cortical information processing in schizophrenia. Schizophr Bull 31: 117-138.
240. Sarter M, Parikh V, Howe WM (2009a). Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat Rev Neurosci 10: 383-390.
241. Sarter M, Parikh V, Howe WM (2009b). nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochem Pharmacol 78: 658-667.
242. Schon K, Atri A, Hasselmo ME, Tricarico MD, LoPresti ML, Stern CE (2005). Scopolamine reduces persistent activity related to long-term encoding in the parahippocampal gyrus during delayed matching in humans. J Neurosci 25: 9112-9123.
243. Schon K, Hasselmo ME, LoPresti ML, Tricarico MD, Stern CE (2004). Persistence of parahippocampal representation in the absence of stimulus input enhances long-term encoding: a functional magnetic resonance imaging study of subsequent memory after a delayed match-to-sample task. Neurosci 24: 11088-11097.
244. 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.
245. 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.
246. Sheffler DJ, Williams R, Bridges TM, Xiang Z, Kane AS, Byun NE et al (2009). A novel selective muscarinic acetylcholine receptor subtype 1 antagonist reduces seizures without impairing hippocampus-dependent learning. Mol Pharmacol 76: 356-368.
247. Shirey JK, Brady AE, Jones PJ, Davis AA, Bridges TM, Kennedy JP et al (2009). A selective allosteric potentiator of the M1 muscarinic acetylcholine receptor increases activity of medial prefrontal cortical neurons and restores impairments in reversal learning. J Neurosci 29: 14271-14286.
248. Shirey JK, Xiang Z, Orton D, Brady AE, Johnson KA, Willians R et al (2008). An allosteric potentiator of M4 mAChR modulates hippocampal synaptic transmission. Nat Chem Biol 4: 42-50.
249. Silver MA, Shenhav A, D'Esposito M (2008). Cholinergic enhancement reduces spatial spread of visual responses in human early visual cortex. Neuron 60: 904-914.
250. Stolerman IP, Mirza NR, Hahn B, Shoaib M (2000). Nicotine in an animal model of attention. Eur J Pharmacol 393: 147-154.
251. Sunderland T, Tariot PN, Cohen RM, Weingartner H, Mueller III EA, Murphy DL (1987). Anticholinergic sensitivity in patients with dementia of the Alzheimer type and age-matched controls. A dose-response study. Arch Gen Psychiatry 44: 418-426.
252. Sunderland T, Tariot PN, Newhouse PA (1988). Differential responsivity of mood, behavior, and cognition to cholinergic agents in elderly neuropsychiatric populations. Brain Res Rev 472: 371-389.
253. Suzuki WA, Miller EK, Desimone R (1997). Object and place memory in the macaque entorhinal cortex. J Neurophysiol 78: 1062-1081.
254. Tahvildari B, Fransen E, Alonso AA, Hasselmo ME (2007). Switching between 'On' and 'Off' states of persistent activity in lateral entorhinal layer III neurons. Hippocampus 17: 257-263.
255. Taly A, Corringer PJ, Guedin D, Lestage P, Changeux JP (2009). Nicotinic receptors: allosteric transitions and therapeutic targets in the nervous system. Nat Rev Drug Discov 8: 733-750.
256. Tang Y, Mishkin M, Aigner TG (1997). Effects of muscarinic blockade in perirhinal cortex during visual recognition. Proc Natl Acad Sci USA 94: 12667-12669.
257. Thiel CM, Fink GR (2008). Effects of the cholinergic agonist nicotine on reorienting of visual spatial attention and top-down attentional control. Neuroscience 152: 381-390.
258. Turchi J, Sarter M (1997). Cortical acetylcholine and processing capacity: effects of cortical cholinergic deafferentation on crossmodal divided attention in rats. Cogn Brain Res 6: 147-158.
259. Turchi J, Saunders RC, Mishkin M (2005). Effects of cholinergic deafferentation of the rhinal cortex on visual recognition memory in monkeys. Proc Natl Acad Sci USA 102: 2158-2161.
260. Valentino RJ, Dingledine R (1981). Presynaptic inhibitory effect of acetylcholine in the hippocampus. J Neurosci 1: 784-792.
261. Vogt KE, Regehr WG (2001). Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J Neurosci 21: 75-83.
262. Vossel S, Thiel CM, Fink GR (2008). Behavioral and neural effects of nicotine on visuospatial attentional reorienting in non-smoking subjects. Neuropsychophar-macology 33: 731-738.
263. Voytko ML, Olton DS, Richardson RT, Gorman LK, Tobin JR, Price DL (1994). Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J Neurosci 14: 167-186.
264. Vuckovich JA, Semel ME, Baxter MG (2004). Extensive lesions of cholinergic basal forebrain neurons do not impair spatial working memory. Learn Memory 11: 87-94.
265. Walsh H, Govind AP, Mastro R, Hoda JC, Bertrand D, Vallejo Y et al (2008). Upregulation of nicotinic receptors by nicotine varies with receptor subtype. J Biol Chem 283: 6022-6032.
266. Warburton DM, Brown K (1971). Attenuation of stimulus sensitivity induced by scopolamine. Nature 230: 126-127.
267. Warburton DM, Mancuso G (1998). Evaluation of the information processing and mood effects of a transdermal nicotine patch. Psychopharmacology 135: 305-310.
268. Warburton EC, Koder T, Cho K, Massey PV, Duguid G, Barker GR et al (2003). Cholinergic neurotransmission is essential for perirhinal cortical plasticity and recognition memory. Neuron 38: 987-996.
269. Weese GD, Phillips JM, Brown VJ (1999). Attentional orienting is impaired by unilateral lesions of the thalamic reticular nucleus in the rat. J Neurosci 19: 10135-10139.
270. Wenk H (1989). The nucleus basalis magnocellularis Meynert (NbmM) complex-a central integrator of coded 'limbic signals' linked to neocortical modular operation? A proposed (heuristic) model of function. J Hirnforsch 30: 127-151.
271. Wesnes K, Simpson P, Kidd A (1988). An investigation of the range of cognitive impairments induced by scopolamine 0.6 mg s.c. Hum Psychopharmacol 3: 27-41.
272. Wesnes K, Warburton DM (1984). Effects of scopolamine and nicotine on human rapid information processing performance. Psychopharmacology 82: 147-150.
273. Wienrich M, Ceci A, Ensinger HA, Gaida W, Mendla KD, Osugi T et al (2002). Talsaclidine (WAL 2014 FU), a muscarinic M1 receptor agonist for the treatment of Alzheimer's disease. Drug Develop Res 56: 321-334.
274. Wilens TE, Biederman J, Spencer TJ, Bostic J, Prince J, Monuteaux MC et al (1999). A pilot controlled clinical trial of ABT-418, a cholinergic agonist, in the treatment of adults with attention deficit hyperactivity disorder.
275. Am J Psychiatry 156: 1931-1937.
276. Wilens TE, Decker MW (2007). Neuronal nicotinic receptor agonists for the treatment of attention-deficit/hyperactivity disorder: focus on cognition. Biochem Pharmacol 74: 1212-1223.
277. Wilens TE, Verlinden MH, Adler LA, Wozniak PJ, West SA (2006). ABT-089, a neuronal nicotinic receptor partial agonist, for the treatment of attention-deficit/hyperactivity disorder in adults: results of a pilot study. Biol Psychiatry 59: 1065-1070.
278. Winson J, Abzug C(1977). Gating of neuronal transmission in the hippocampus: efficacy of transmission varies with behavioral state. Science 196, 1223-1225
279. Winson J, Abzug C (1978). Neuronal transmission through hippocampal pathways dependent on behavior. J Neurophysiol 41: 716-732.
280. Witte EA, Marrocco RT (1997). Alteration of brain noradrenergic activity in rhesus monkey affects the alerting component of covert orienting. Psychopharmacoloy 132: 315-323.
281. Woolf NJ (1991). Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37: 475-524.
282. Xiang Z, Huguenard JR, Prince DA (1998). Cholinergic switching within neocortical inhibitory networks. Science 281: 985-988.
283. Yamada M, Basile AS, Fedorova I, Zhang W, Duttaroy A, Cui Y et al (2003). Novel insights into M5 muscarinic acetylcholine receptor function by the use of gene targeting technology. Life Sci 74: 345-353.
284. Yamasaki M, Matsui M, Watanabe M (2010). Preferential localization of muscarinic M1 receptors on dendritic shaft and spine of cortical pyramidal cells and its anatomical evidence for volume transmission. J Neurosci 30: 4408-4418.
285. Yates SL, Bencherif M, Fluhler EN, Lippiello PM (1995). Up-regulation of nicotinic acetylcholine receptors following chronic exposure of rats to mainstream cigarette smoke or alpha 4 beta 2 receptors to nicotine. Biochem Pharmacol 50: 2001-2008.
286. Yoshida M, Hasselmo ME (2009). Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. J Neurosci 29: 4945-4952.
287. Young BJ, Otto T, Fox GD, EIchenbaum H (1997). Memory representation within the parahippocampal region. J Neurosci 17: 5183-5195.
288. Young JW, Crawford N, Kelly JS, Kerr LE, Marston HM, Spratt C et al (2007). Impaired attention is central to the cognitive deficits observed in alpha 7 deficient mice. Eur Neuropsychopharmacol 17: 145-155.
289. Zaborszky L (2002). The modular organization of brain systems. Basal forebrain: the last frontier. Prog Brain Res 136: 359-372.
290. Zaborszky L, Buhl DL, Pobalashingham S, Bjaalie JG, Nadasdy Z (2005). Three-dimensional chemoarchitecture of the basal forebrain: spatially specific association of cholinergic and calcium binding protein-containing neurons. Neuroscience 136: 697-713.
291. Zaborszky L, Hoemke L, Mohlberg H, Schleicher A, Amunts K, Zilles K (2008). Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain. Neuroimage 42: 1127-1141.
292. Zikopoulos B, Barbas H (2006). Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. J Neurosci 26: 7348-7361.
293. Zikopoulos B, Barbas H (2007a). Circuits for multisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Rev Neurosci 18: 417-438.
294. Zikopoulos B, Barbas H (2007b). Parallel driving and modulatory pathways link the prefrontal cortex and thalamus. PLoS ONE 2: e848.
295. Zmarowski A, Sarter M, Bruno JP (2005). NMDA and dopamine interactions in the nucleus accumbens modulate cortical acetylcholine release. Eur J Neurosci 22: 1731-1740.
296. Zmarowski A, Sarter M, Bruno JP (2007). Glutamate receptors in nucleus accumbens mediate regionally selective increases in cortical acetylcholine release. Synapse 61: 115-123.