Leveraging the cortical cholinergic system to enhance attention

Neuropharmacology

Volumn 64, Issue , 2013, Pages 294-304

  Demeter, Elise ^a   Sarter, Martin ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Acetylcholine; Attentional control; Cognition enhancers; Cue detection

Indexed keywords

ACETYLCHOLINE; CHOLINESTERASE INHIBITOR; DONEPEZIL; GALANTAMINE; NICOTINIC RECEPTOR;

ATTENTION; CHOLINERGIC ACTIVITY; CHOLINERGIC SYSTEM; COGNITION; DEGENERATIVE DISEASE; DRUG MECHANISM; HUMAN; NEUROPSYCHIATRY; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW;

ANIMALS; ATTENTION; CHOLINERGIC NEURONS; CHOLINESTERASE INHIBITORS; COGNITION DISORDERS; HUMANS; MOLECULAR TARGETED THERAPY; MUSCARINIC AGONISTS; NERVE TISSUE PROTEINS; NICOTINIC AGONISTS; NOOTROPIC AGENTS; PERFORMANCE-ENHANCING SUBSTANCES; PREFRONTAL CORTEX;

EID: 84866366581     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.06.060     Document Type: Review

References (169)

1. T.G. Aigner, D.L. Walker, and M. Mishkin Comparison of the effects of scopolamine administered before and after acquisition in a test of visual recognition memory in monkeys Behav. Neural Biol. 55 1991 61 67 10.1016/0163-1047(91)80127-Z
2. S.G. Anagnostaras, G.G. Murphy, S.E. Hamilton, S.L. Mitchell, N.P. Rahnama, N.M. Nathanson, and A.J. Silva Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice Nat. Neurosci. 6 2003 51 58 10.1038/nn992
3. J.R. Andrews-Hanna, K.L. Mackiewicz Seghete, E.D. Claus, G.C. Burgess, L. Ruzic, and M.T. Banich Cognitive control in adolescence: neural underpinnings and relation to self-report behaviors PLoS One 6 2011 e21598 10.1371/journal.pone.0021598
4. G. Apostol, W. Abi-Saab, C.J. Kratochvil, L.A. Adler, W.Z. Robieson, L.M. Gault, Y.L. Pritchett, D. Feifel, M.A. Collins, and M.D. Saltarelli Efficacy and safety of the novel α4β2* neuronal nicotinic receptor partial agonist ABT-089 in adults with attention-deficit/hyperactivity disorder: a randomized, double-blind, placebo-controlled crossover study Psychopharmacology 219 2012 715 725 10.1007/s00213-011-2393-2
5. H.M. Arnold, J.A. Burk, E.M. Hodgson, M. Sarter, and J.P. Bruno Differential cortical acetylcholine release in rats performing a sustained attention task versus behavioral control tasks that do not explicitly tax attention Neuroscience 114 2002 451 460 10.1016/S0306-4522(02)00292-0
6. R.F. Asarnow, and D.J. Maccrimmon Residual performance deficits in clinically remitted schizophrenics - marker of schizophrenia J. Abnorm. Psychol. 87 1978 597 608 10.1037/0021-843X.87.6.597
7. C.D. Bailey, M. De Biasi, P.J. Fletcher, and E.K. Lambe The nicotinic acetylcholine receptor alpha5 subunit plays a key role in attention circuitry and accuracy J. Neurosci. 30 2010 9241 9252 10.1523/JNEUROSCI.2258-10.2010
8. W.W. Beatty, N. Butters, and D.S. Janowsky Patterns of memory failure after scopolamine treatment: implications for cholinergic hypotheses of dementia Behav. Neural Biol. 45 1986 196 211 10.1016/S0163-1047(86)90772-7
9. P. Bentley, M. Husain, and R.J. Dolan Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory Neuron 41 2004 969 982 10.1016/S0896-6273(04)00145-X
10. P. Bentley, J. Driver, and R.J. Dolan Cholinesterase inhibition modulates visual and attentional brain responses in Alzheimer's disease and health Brain 131 2008 409 424 10.1093/brain/awm299
11. P. Bentley, J. Driver, and R.J. Dolan Cholinergic modulation of cognition: insights from human pharmacological functional neuroimaging Prog. Neurobiol. 94 2011 360 388 10.1016/j.pneurobio.2011.06.002
12. A. Blondel, D.J. Sanger, and P.C. Moser Characterisation of the effects of nicotine in the five-choice serial reaction time task in rats: antagonist studies Psychopharmacology 149 2000 293 305 10.1007/s002130000378
13. N.C. Bodick, W.W. Offen, H.E. Shannon, J. Satterwhite, R. Lucas, R. van Lier, and S.M. Paul The selective muscarinic agonist xanomeline improves both the cognitive deficits and behavioral symptoms of Alzheimer disease Alzheimer Dis. Assoc. Disord. 11 Suppl. 4 1997 S16 S22 10.1176/appi.ajp.2008.06091591
14. D.L. Braff, and D.P. Saccuzzo The time course of information-processing deficits in schizophrenia Am. J. Psychiatry 142 1985 170 174
15. F. Briggs, and W.M. Usrey Corticogeniculate feedback and visual processing in the primate J. Physiol. 589 2011 33 40 10.1113/jphysiol.2010. 193599
16. P. Broks, G.C. Preston, M. Traub, P. Poppleton, C. Ward, and S.M. Stahl Modelling dementia: effects of scopolamine on memory and attention Neuropsychologia 26 1988 685 700 10.1016/0028-3932(88)90004-8
17. R.W. Buchanan, R.R. Conley, D. Dickinson, M.P. Ball, S. Feldman, J.M. Gold, and R.P. McMahon Galantamine for the treatment of cognitive impairments in people with schizophrenia Am. J. Psychiatry 165 2008 82 89 10.1176/appi.ajp. 2007.07050724
18. P.J. Bushnell, W.M. Oshiro, and B.K. Padnos Detection of visual signals by rats: effects of chlordiazepoxide and cholinergic and adrenergic drugs on sustained attention Psychopharmacology (Berl.) 134 1997 230 241 10.1007/s002130050446
19. R. Cabeza, and L. Nyberg Imaging cognition II: an empirical review of 275 PET and fMRI studies J. Cogn. Neurosci. 12 2000 1 47 10.1162/08989290051137585
20. A. Caccamo, S. Oddo, L.M. Billings, K.N. Green, H. Martinez-Coria, A. Fisher, and F.M. LaFerla M1 receptors play a central role in modulating AD-like pathology in transgenic mice Neuron 49 2006 671 682 10.1016/j.neuron.2006.01.020
21. A. Caccamo, A. Fisher, and F.M. LaFerla M1 agonists as a potential disease-modifying therapy for Alzheimer's disease Curr. Alzheimer Res. 6 2009 112 117
22. C.S. Carter, and D.M. Barch Cognitive neuroscience-based approaches to measuring and improving treatment effects on cognition in schizophrenia: the CNTRICS initiative Schizophr. Bull. 33 2007 1131 1137 10.1093/schbul/sbm081
23. C.S. Carter, D.M. Barch, R.W. Buchanan, E. Bullmore, J.H. Krystal, J. Cohen, M. Geyer, M. Green, K.H. Nuechterlein, T. Robbins, S. Silverstein, E.E. Smith, M. Strauss, T. Wykes, and R. Heinssen Identifying cognitive mechanisms targeted for treatment development in schizophrenia: an overview of the first meeting of the cognitive neuroscience treatment research to improve cognition in schizophrenia initiative Biol. Psychiatry 64 2008 4 10 10.1016/j.biopsych.2008. 03.020
24. M.P. Caulfield, and N.J. Birdsall International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors Pharmacol. Rev. 50 1998 279 290
25. P.J. Conn, C.K. Jones, and C.W. Lindsley Subtype-selective allosteric modulators of muscarinic receptors for the treatment of CNS disorders Trends Pharmacol. Sci. 30 2009 148 155 10.1016/j.tips.2008.12.002
26. C.K. Conners, E.D. Levin, E. Sparrow, S.C. Hinton, D. Erhardt, W.H. Meck, J.E. Rose, and J. March Nicotine and attention in adult attention deficit hyperactivity disorder (ADHD) Psychopharmacol. Bull. 32 1996 67 73
27. M. Corbetta, and G.L. Shulman Control of goal-directed and stimulus-driven attention in the brain Nat. Rev. Neurosci. 3 2002 201 215 10.1038/nrn755
28. F. Crick Function of the thalamic reticular complex: the searchlight hypothesis Proc. Natl. Acad. Sci. U. S. A. 81 1984 4586 4590
29. J.W. Dalley, J. McGaughy, M.T. O'Connell, R.N. Cardinal, L. Levita, and T.W. Robbins Distinct changes in cortical acetylcholine and noradrenaline efflux during contingent and noncontingent performance of a visual attentional task J. Neurosci. 21 2001 4908 4914
30. M.E. Dawson, and K.H. Nuechterlein Psychophysiological dysfunctions in the developmental course of schizophrenic disorders Schizophr. Bull. 10 1984 204 232 10.1093/schbul/10.2.204
31. M.E. Dawson Psychophysiology at the interface of clinical science, cognitive science, and neuroscience Psychophysiology 27 1990 243 255 10.1111/j.1469-8986.1990.tb00378.x
32. G. Deco, and A. Thiele Attention - oscillations and neuropharmacology Eur. J. Neurosci. 30 2009 347 354 10.1111/j.1460-9568.2009.06833.x
33. E. Demeter, M. Sarter, and C. Lustig Rats and humans paying attention: cross-species task development for translational research Neuropsychology 22 2008 787 799 10.1037/a0013712
34. E. Demeter, L. Hernandez-Garcia, M. Sarter, and C. Lustig Challenges to attention: a continuous arterial spin labeling (ASL) study of the effects of distraction on sustained attention Neuroimage 54 2011 1518 1529 10.1016/j.neuroimage.2010.09.026
35. G.C. Dunbar, F. Inglis, R. Kuchibhatla, T. Sharma, M. Tomlinson, and J. Wamsley Effect of ispronicline, a neuronal nicotinic acetylcholine receptor partial agonist, in subjects with age associated memory impairment (AAMI) J. Psychopharmacol. 21 2007 171 178 10.1177/0269881107066855
36. J.R. Ellis, K.A. Ellis, C.F. Bartholomeusz, B.J. Harrison, K.A. Wesnes, F.F. Erskine, L. Vitetta, and P.J. Nathan Muscarinic and nicotinic receptors synergistically modulate working memory and attention in humans Int. J. Neuropsychopharmacol. 9 2006 175 189
37. M. Ernst, J.A. Matochik, S.J. Heishman, J.D. Van Horn, P.H. Jons, J.E. Henningfield, and E.D. London Effect of nicotine on brain activation during performance of a working memory task Proc. Natl. Acad. Sci. U. S. A. 98 2001 4728 4733 10.1073/pnas.061369098
38. F.F. Erskine, J.R. Ellis, K.A. Ellis, E. Stuber, K. Hogan, V. Miller, E. Moore, C. Bartholomeusz, B.J. Harrison, B. Lee, K.L. Phan, D. Liley, and P.J. Nathan Evidence for synergistic modulation of early information processing by nicotinic and muscarinic receptors in humans Hum. Psychopharmacol. 19 2004 503 509 10.1002/hup.613
39. U. Ettinger, S.C. Williams, D. Patel, T.M. Michel, A. Nwaigwe, A. Caceres, M.A. Mehta, A.P. Anilkumar, and V. Kumari Effects of acute nicotine on brain function in healthy smokers and non-smokers: estimation of inter-individual response heterogeneity Neuroimage 45 2009 549 561 10.1016/j.neuroimage.2008.12.029
40. C.C. Felder, F.P. Bymaster, J. Ward, and N. DeLapp Therapeutic opportunities for muscarinic receptors in the central nervous system J. Med. Chem. 43 2000 4333 4353
41. R. Freedman, A. Olincy, R.W. Buchanan, J.G. Harris, J.M. Gold, and L. Johnson Initial phase 2 trial of a nicotinic agonist in schizophrenia Am. J. Psychiatry 165 2008 1040 1047 10.1176/appi.ajp.2008.07071135
42. M.L. Furey, P. Pietrini, and J.V. Haxby Cholinergic enhancement and increased selectivity of perceptual processing during working memory Science 290 2000 2315 2319 10.1126/science.290.5500.2315
43. P.H. Ghatan, M. Ingvar, L. Eriksson, S. Stone-Elander, M. Serrander, K. Ekberg, and J. Wahren Cerebral effects of nicotine during cognition in smokers and non-smokers Psychopharmacology (Berl.) 136 1998 179 189 10.1007/ s002130050554
44. M.M. Ghoneim, and S.P. Mewaldt Effects of diazepam and scopolamine on storage, retrieval and organizational processes in memory Psychopharmacologia 44 1975 257 262 10.1007/BF00428903
45. M.M. Ghoneim, and S.P. Mewaldt Studies on human memory: the interactions of diazepam, scopolamine, and physostigmine Psychopharmacology (Berl.) 52 1977 1 6 10.1007/BF00426592
46. C. Giessing, C.M. Thiel, F. Rosler, and G.R. Fink The modulatory effects of nicotine on parietal cortex activity in a cued target detection task depend on cue reliability Neuroscience 137 2006 853 864 10.1016/j.neuroscience.2005.10. 005
47. T.M. Gill, M. Sarter, and B. Givens Sustained visual attention performance-associated prefrontal neuronal activity: evidence for cholinergic modulation J. Neurosci. 20 2000 4745 4757
48. L.M. Giocomo, and M.E. Hasselmo Neuromodulation by glutamate and acetylcholine can change circuit dynamics by regulating the relative influence of afferent input and excitatory feedback Mol. Neurobiol. 36 2007 184 200 10.1007/s12035-007-0032-z
49. L. Golmayo, A. Nunez, and L. Zaborszky Electrophysiological evidence for the existence of a posterior cortical-prefrontal-basal forebrain circuitry in modulating sensory responses in visual and somatosensory rat cortical areas Neuroscience 119 2003 597 609 10.1016/S0306-4522(03)00031-9
50. M.F. Green, R.S. Kern, D.L. Braff, and J. Mintz Neurocognitive deficits and functional outcome in schizophrenia: are we measuring the "right stuff" Schizophr. Bull. 26 2000 119 136
51. A.J. Grottick, and G.A. Higgins Effect of subtype selective nicotinic compounds on attention as assessed by the five-choice serial reaction time task Behav. Brain Res. 117 2000 197 208 10.1016/S0166-4328(00)00305-3
52. A.J. Grottick, M. Haman, R. Wyler, and G.A. Higgins Reversal of a vigilance decrement in the aged rat by subtype-selective nicotinic ligands Neuropsychopharmacology 28 2003 880 887 10.1038/sj.npp.1300102
53. A.J. Gruber, R.J. Hussain, and P. O'Donnell The nucleus accumbens: a switchboard for goal-directed behaviors PLoS One 4 2009 e5062 10.1371/journal.pone.0005062
54. K. Guillem, B. Bloem, R.B. Poorthuis, M. Loos, A.B. Smit, U. Maskos, S. Spiker, and H.D. Mansvelder Nicotinic acetylcholine receptor β2 subunits in the medial prefrontal cortex control attention Science 333 2011 888 891 10.1126/science.1207079
55. B. Hahn, C.G. Sharples, S. Wonnacott, M. Shoaib, and I.P. Stolerman Attentional effects of nicotinic agonists in rats Neuropharmacology 44 2003 1054 1067 10.1016/S0028-3908(03)00099-6
56. B. Hahn, T.J. Ross, Y. Yang, I. Kim, M.A. Huestis, and E.A. Stein Nicotine enhances visuospatial attention by deactivating areas of the resting brain default network J. Neurosci. 27 2007 3477 3489 10.1523/JNEUROSCI.5129-06. 2007
57. B. Hahn, T.J. Ross, and F.A. Wolkenberg Performance effects of nicotine during selective attention, divided attention, and simple stimulus detection: an fMRI study Cereb. Cortex 19 2009 1990 2000 10.1093/cercor/bhn226
58. M.E. Hasselmo, and M. Sarter Modes and models of forebrain cholinergic neuromodulation of cognition Neuropsychopharmacology 36 2011 52 73 10.1038/npp.2010.104
59. R.W. Heinrichs, and K.K. Zakzanis Neurocognitive deficit in schizophrenia: a quantitative review of the evidence Neuropsychology 12 1998 426 445 10.1037/0894-4105.12.3.426
60. C.D. Herzog, K.A. Nowak, M. Sarter, and J.P. Bruno Microdialysis without acetylcholinesterase inhibition reveals an age-related attenuation in stimulated cortical acetylcholine release Neurobiol. Aging 24 2003 861 863 10.1016/S0197-4580(02)00226-9
61. A.M. Himmelheber, M. Sarter, and J.P. Bruno Increases in cortical acetylcholine release during sustained attention performance in rats Brain Res. Cogn. Brain Res. 9 2000 313 325 10.1016/S0926-6410(00)00012-4
62. W.M. Howe, and M. Sarter Prefrontal; glutamatergic-cholinergic interactions for attention: glutamatergic coding of signal salience as a function of performance levels B. Westerink, R. Clinckers, S. Smolders, S. Sarre, Y. Michotte, Monitoring Molecules in Neuroscience 2010 Vrije Universiteit Brussels Brussels, Belgium 57 59
63. W.M. Howe, V. Parikh, V. Martinez, and M. Sarter Prefrontal Cholinergic Switching from Associational Processing to Cue Detection: Evidence from Sub-second Measures of Prefrontal Cholinergic Neurotransmission, Using Choline-sensitive Microlectrodes, in Animals Performing an Operant Sustained Attention Task 2007 Society for Neuroscience Annual Meeting San Diego, CA
64. W.M. Howe, J. Ji, V. Parikh, S. Williams, E. Mocaer, C. Trocme- Thibierge, and M. Sarter Enhancement of attentional performance by selective stimulation of a α4β2* nAChRs: underlying cholinergic mechanisms Neuropsychopharmacology 35 2010 1391 1401 10.1038/npp.2010.9
65. C.A. Ingham, J.P. Bolam, and A.D. Smith GABA-immunoreactive synaptic boutons in the rat basal forebrain: comparison of neurons that project to the neocortex with pallidosubthalamic neurons J. Comp. Neurol. 273 1988 263 282 10.1002/cne.902730210
66. J. Jeon, D. Dencker, G. Wörtwein, D.P. Woldbye, Y. Cui, A.A. Davis, A.I. Levey, G. Schütz, T.N. Sager, A. Mork, C. Li, C.X. Deng, A. Fink-Jensen, and J. Wess A subpopulation of neuronal M4 muscarinic acetylcholine receptors plays a critical role in modulating dopamine-dependent behaviors J. Neurosci. 30 2010 2396 2405 10.1523/JNEUROSCI.3843-09.2010
67. G.M. Jones, B.J. Sahakian, R. Levy, D.M. Warburton, and J.A. Gray Effects of acute subcutaneous nicotine on attention, information processing and short-term memory in Alzheimer's disease Psychopharmacology (Berl.) 108 1992 485 494 10.1007/BF02247426
68. J.D. Kassel Smoking and attention: a review and reformulation of the stimulus-filter hypothesis Clin. Psychol. Rev. 17 1997 451 478 10.1016/S0272-7358(97)00032-9
69. S. Kastner, and L.G. Ungerleider Mechanisms of visual attention in the human cortex Annu. Rev. Neurosci. 23 2000 315 341 10.1146/annurev.neuro.23.1.315
70. R. Keefe, A. Malhotra, H. Meltzer, J. Kane, R. Buchanan, A. Murthy, M. Sovel, C. Li, and R. Goldman 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 2008 1217 1228 10.1038/sj.npp.1301499
71. M.L. Kietzman, B. Spring, and J. Zubin Perception, cognition and attention third ed. H.I. Kaplan, A.M. Freedman, B.J. Sadock, Comprehensive Textbook of Psychiatry vol. 1 1985 Williams & Wilkins Maryland 334 370
72. C. Kohler, E. Martin, E. Kujawski, W. Bilker, R. Gur, and R. Gur No effect of donepezil on neurocognition and social cognition in young persons with stable schizophrenia Cogn. Neuropsychiatry 12 2007 412 421 10.1080/ 13546800701307263
73. R. Kozak, J.P. Bruno, and M. Sarter Augmented prefrontal acetylcholine release during challenged attentional performance Cereb. Cortex 16 2006 9 17 10.1093/cercor/bhi079
74. R. Kozak, W. Lipinski, A. Kantarowksi, D. Lankford, S. Williams, J. Michel, L.T. Meltzer, and M. Sarter Behavioral Screening of Cognition Enhancers: Effects of Standard Compounds on Attentional Performance and in Interaction with Performance Challenges 2007 Society for Neuroscience Annual Meeting San Diego, CA
75. R. Kozak, V. Martinez, D. Young, H. Brown, J.P. Bruno, and M. Sarter 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 2007 2074 2086 10.1038/sj.npp.1301352
76. N.S. Lawrence, T.J. Ross, and E.A. Stein Cognitive mechanisms of nicotine on visual attention Neuron 36 2002 539 548 10.1016/S0896-6273(02)01004-8
77. J. Le Houezec, R. Halliday, N.L. Benowitz, E. Callaway, H. Naylor, and K. Herzig A low dose of subcutaneous nicotine improves information processing in nonsmokers Psychopharmacology (Berl.) 114 1994 628 634 10.1007/BF02244994
78. A.I. Levey, C.A. Kitt, W.F. Simonds, D.L. Price, and M.R. Brann Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies J. Neurosci. 11 1991 3218 3226
79. E.D. Levin, C.K. Conners, E. Sparrow, S.C. Hinton, D. Erhardt, W.H. Meck, J.E. Rose, and J. March Nicotine effects on adults with attention-deficit/ hyperactivity disorder Psychopharmacology 123 1996 55 63 10.1007/BF02246281
80. E.D. Levin Nicotinic receptor subtypes and cognitive function J. Neurobiol. 53 2002 633 640 10.1002/neu.10151
81. J.T. Little, D.N. Johnson, M. Minichiello, H. Weingartner, and T. Sunderland Combined nicotinic and muscarinic blockade in elderly normal volunteers: cognitive, behavioral, and physiologic responses Neuropsychopharmacology 19 1998 60 69 10.1016/S0893-133X(98)00002-5
82. G. Mancuso, D.M. Warburton, M. Melen, N. Sherwood, and E. Tirelli Selective effects of nicotine on attentional processes Psychopharmacology (Berl.) 146 1999 199 204 10.1007/s002130051107
83. N.L. Marchant, S. Trawley, and J.M. Rusted Prospective memory or prospective attention: physiological and pharmacological support for an attentional model Int. J. Neuropsychopharmacol. 11 2008 401 411 10.1017/S146114570700819X
84. J.E. Marlo, C.M. Niswender, E.L. Days, T.M. Bridges, Y. Xiang, A.L. Rodriguez, J.K. Shirey, A.E. Brady, T. Nalywajko, Q. Luo, C.A. Austin, M.B. Williams, K. Kim, R. Williams, D. Orton, H.A. Brown, C.W. Lindsley, C.D. Weaver, and P.J. Conn Discovery and characterization of novel allosteric potentiators of M1 muscarinic receptors reveals multiple modes of activity Mol. Pharmacol. 75 2009 577 588 10.1124/mol.108.052886
85. K. McAlonan, J. Cavanaugh, and R.H. Wurtz Attentional modulation of thalamic reticular neurons J. Neurosci. 26 2006 4444 4450 10.1523/JNEUROSCI. 5602-05.2006
86. J. McGaughy, and M. Sarter Behavioral vigilance in rats: task validation and effects of age, amphetamine, and benzodiazepine receptor ligands Psychopharmacology 117 1995 340 357 10.1007/BF02246109
87. J. McGaughy, and M. Sarter Sustained attention performance in rats with intracortical infusions of 192 IgG-saporin-induced cortical cholinergic deafferentation: effects of physostigmine and FG 7142 Behav. Neurosci. 112 1998 1519 1525 10.1037/0735-7044.112.6.1519
88. J. McGaughy, J. Turchi, and M. Sarter Crossmodal divided attention in rats: effects of chlordiazepoxide and scopolamine Psychopharmacology (Berl.) 115 1994 213 220 10.1007/BF02244774
89. J. McGaughy, T. Kaiser, and M. Sarter 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 1996 247 265 10.1037/0735-7044.110.2.247
90. J. McGaughy, M.W. Decker, and M. Sarter Enhancement of sustained attention performance by the nicotinic acetylcholine receptor agonist ABT-418 in intact but not basal forebrain-lesioned rats Psychopharmacology (Berl.) 144 1999 175 182 10.1007/s002130050991
91. N.R. Mirza, and I.P. Stolerman Nicotine enhances sustained attention in the rat under specific task conditions Psychopharmacology (Berl.) 138 1998 266 274 10.1007/s002130050671
92. T. Miyakawa, M. Yamada, A. Duttaroy, and J. Wess Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor J. Neurosci. 21 2001 5239 5250
93. G.J. Mogenson, D.L. Jones, and C.Y. Yim From motivation to action: functional interface between the limbic system and the motor system Prog. Neurobiol. 14 1980 69 97 10.1016/0301-0082(80)90018-0
94. E.G. Mohler, S.R. Franklin, L.E. Rueter, G.B. Fox, M.W. Decker, and K.E. Browman ABT-594 improves performance in the 5-choice serial reaction time task under conditions of increased difficulty, sub-chronic dosing, and in poorly-performing subjects Pharmacol. Biochem. Behav. 95 2010 146 157 10.1016/j.pbb.2009.12.019
95. S.E. Molchan, R.A. Martinez, J.L. Hill, H.J. Weingartner, K. Thompson, B. Vitiello, and T. Sunderland Increased cognitive sensitivity to scopolamine with age and a perspective on the scopolamine model Brain Res. Rev. 17 1992 215 226 10.1016/0165-0173(92)90017-G
96. J.L. Muir, B.J. Everitt, and T.W. Robbins AMPA-induced excitotoxic lesions of the basal forebrain: a significant role for the cortical cholinergic system in attentional function J. Neurosci. 14 1994 2313 2326
97. J.L. Muir, B.J. Everitt, and T.W. Robbins Reversal of visual attentional dysfunction following lesions of the cholinergic basal forebrain by physostigmine and nicotine but not by the 5-HT3 receptor antagonist, ondansetron Psychopharmacology (Berl.) 118 1995 82 92 10.1007/BF02245253
98. C.L. Nelson, M. Sarter, and J.P. Bruno Prefrontal cortical modulation of acetylcholine release in posterior parietal cortex Neuroscience 132 2005 347 359 10.1016/j.neuroscience.2004.12.007
99. P.A. Newhouse, A. Potter, M. Kelton, and J. Corwin Nicotinic treatment of Alzheimer's disease Biol. Psychiatry 49 2001 268 278 10.1016/S0006-3223(00) 01069-6
100. K.H. Nuechterlein, K.S. Snyder, and J. Mintz Paths to relapse - possible transactional processes connecting patient illness onset, expressed emotion, and psychotic relapse Br. J. Psychiatry 161 1992 88 96
101. K.H. Nuechterlein, D.M. Barch, and J.M. Gold Identification of separable cognitive factors in schizophrenia Schizophr. Res. 72 2004 29 39 10.1016/j.schres.2004.09.007
102. D.H. O'Connor, M.M. Fukui, M.A. Pinsk, and S. Kastner Attention modulates responses in the human lateral geniculate nucleus Nat. Neurosci. 5 2002 1203 1209 10.1038/nn957
103. A. Olincy, and K.E. Stevens Treating schizophrenia symptoms with an α7 nicotinic agonist, from mice to men Biochem. Pharmacol. 74 2007 1192 1201 10.1016/j.bcp.2007.07.015
104. G. Paolone, M.W. Howe, M. Gopalakrishnan, M.W. Decker, and M. Sarter Regulation and function of the tonic component of cortical acetylcholine release B. Westerink, R. Clinckers, I. Smolders, S. Sarre, Y. Michotte, Monitoring Molecules in Neuroscience 2010 Vrije Universiteit Brussels Brussels, Belgium 363 365
105. V. Parikh, and M. Sarter Cholinergic mediation of attention: the contributions of phasic versus tonic components of prefrontal cholinergic activity D. Pfaff, B. Kieffer, Molecular and Biophysical Mechanisms of Arousal, Alertness and Attention Annals of the New York Academy of Sciences vol. 1129 2008 The New York Academy of Sciences NY 225 235
106. V. Parikh, F. Pomerleau, P. Huettl, G.A. Gerhardt, M. Sarter, and J.P. Bruno Rapid assessment of in vivo cholinergic transmission by amperometric detection of changes in extracellular choline levels Eur. J. Neurosci. 20 2004 1545 1554 10.1111/j.1460-9568.2004.03614.x
107. V. Parikh, R. Kozak, V. Martinez, and M. Sarter Prefrontal acetylcholine release controls cue detection on multiple timescales Neuron 56 2007 141 154 10.1016/j.neuron.2007.08.025
108. V. Parikh, K. Man, M.W. Decker, and M. Sarter Glutamatergic contributions to nicotinic acetylcholine receptor agonist-evoked cholinergic transients in the prefrontal cortex J. Neurosci. 28 2008 3769 3780 10.1523/JNEUROSCI.5251-07. 2008
109. V. Parikh, J. Ji, M.W. Decker, and M. Sarter Prefrontal β2 subunit-containing and α7 nicotinic acetylcholine receptors differentially control glutamatergic and cholinergic signaling J. Neurosci. 30 2010 3518 3530 10.1523/JNEUROSCI.5712-09.2010
110. F. Passetti, J.W. Dalley, and M.T. O'Connell Increased acetylcholine release in the rat medial prefrontal cortex during performance of a visual attentional task Eur. J. Neurosci. 12 2000 3051 3058 10.1046/j.1460-9568.2000. 00183.x
111. L. Pessoa, S. Kastner, and L.G. Ungerleider Neuroimaging studies of attention: from modulation of sensory processing to top-down control J. Neurosci. 23 2003 3990 3998
112. R.B. Poorthuis, B. Bloem, B. Schak, J. Wester, C.P. de Kock, and H.D. Mansvelder Layer-specific modulation of the prefrontal cortex by nicotinic acetylcholine receptors Cereb. Cortex 2012 10.1093/cercor/bhr390 [Epub ahead of print]
113. M.I. Posner, C.R. Snyder, and B.J. Davidson Attention and the detection of signals J. Exp. Psychol. Gen. 109 1980 160 174 10.1037/0096-3445.109.2.160
114. M.E. Raichle, and A.Z. Snyder A default mode of brain function: a brief history of an evolving idea Neuroimage 37 2007 1083 1090 10.1016/j.neuroimage. 2007.02.041
115. J. Ramirez-Latorre, C.R. Yu, X. Qu, F. Perin, A. Karlin, and L. Role Functional contributions of alpha5 subunit to neuronal acetylcholine receptor channels Nature 380 1996 347 351 10.1038/380347a0
116. M.A. Raskind, E.R. Peskind, T. Wessel, and W. Yuan Galantamine in AD - A 6-month randomized, placebo-controlled trial with a 6-month extension Neurology 54 2000 2261 2268
117. E. Ricciardi, P. Pietrini, M.B. Schapiro, S.I. Rapoport, and M.L. Furey Cholinergic modulation of visual working memory during aging: a parametric PET study Brain Res. Bull. 79 2009 322 332 10.1016/j.brainresbull.2009.01.013
118. T.W. Robbins, B.J. Everitt, H.M. Marston, J. Wilkinson, G.H. Jones, and K.J. Page 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 1989 221 240 10.1016/S0166-4328(89) 80143-3
119. S.L. Rogers, and L.T. Friedhoff The efficacy and safety of donepezil in patients with Alzheimer's disease: results of a US multicentre, randomized, double-blind, placebo-controlled trial Dementia 7 1996 293 303 10.1159/000106895
120. S.L. Rogers, M.R. Farlow, R.S. Doody, R. Mohs, and L.T. Friedhoff A 24-week, double-blind, placebo-controlled trial of donepezil in patients with Alzheimer's disease Neurology 50 1998 136 145
121. A. Rokem, A.N. Landau, D. Garg, W. Prinzmetal, and M.A. Silver Cholinergic enhancement increases the effects of voluntary attention but does not affect involuntary attention Neuropsychopharmacology 35 2010 2538 2544 10.1038/npp.2010.118
122. S.T. Rouse, S.E. Hamilton, L.T. Potter, N.M. Nathanson, and P.J. Conn Muscarinic-induced modulation of potassium conductances is unchanged in mouse hippocampal pyramidal cells that lack functional M1 receptors Neurosci. Lett. 278 2000 61 64 10.1016/S0304-3940(99)00914-3
123. J.M. Rusted, R. Sawyer, C. Jones, S.L. Trawley, and N.L. Marchant Positive effects of nicotine on cognition: the deployment of attention for prospective memory Psychopharmacology 202 2009 93 102 10.1007/s00213-008-1320-7
124. B. Sahakian, G. Jones, R. Levy, J. Gray, and D. Warburton The effects of nicotine on attention, information processing, and short-term memory in patients with dementia of the Alzheimer type Br. J. Psychiatry 154 1989 797 800 10.1192/bjp.154.6.797
125. M. Sarter, and H.J. Markowitsch Collateral innervation of the medial and lateral prefrontal cortex by amygdaloid, thalamic, and brain-stem neurons J. Comp. Neurol. 224 1984 445 460 10.1002/cne.902240312
126. M. Sarter, and G. Paolone Deficits in attentional control: cholinergic mechanisms and circuitry-based treatment approaches Behav. Neurosci. 125 2011 825 835 10.1037/a0026227
127. M. Sarter, J. Hagan, and P. Dudchenko Behavioral screening for cognition enhancers: from indiscriminate to valid testing: part I Psychopharmacology (Berl.) 107 1992 144 159 10.1007/BF02245132
128. M. Sarter, J. Hagan, and P. Dudchenko Behavioral screening for cognition enhancers: from indiscriminate to valid testing: part II Psychopharmacology (Berl.) 107 1992 461 473 10.1007/BF02245257
129. M. Sarter, B. Givens, and J.P. Bruno The cognitive neuroscience of sustained attention: where top-down meets bottom-up Brain Res. Brain Res. Rev. 35 2001 146 160 10.1016/S0165-0173(01)00044-3
130. M. Sarter, M. Hasselmo, J. Bruno, and B. Givens Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection Brain Res. Brain Res. Rev. 48 2005 98 111 10.1016/j.brainresrev.2004.08.006
131. M. Sarter, W. Gehring, and R. Kozak More attention must be paid: the neurobiology of attentional effort Brain Res. Rev. 51 2006 145 160 10.1016/j.brainresrev.2005.11.002
132. M. Sarter, V. Parikh, and W.M. Howe nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms Biochem. Pharmacol. 78 2009 658 667 10.1016/j.bcp.2009.04.019
133. M. Sarter, C. Lustig, and S.F. Taylor Cholinergic contributions to the cognitive symptoms of schizophrenia and the viability of cholinergic treatments Neuropharmacology 62 2012 1544 1553 10.1016/j.neuropharm.2010.12.001
134. M. Sarter Preclinical research into cognition enhancers Trends Pharmacol. Sci. 27 2006 602 608 10.1016/j.tips.2006.09.004
135. H. Sato, Y. Hata, K. Hagihara, and T. Tsumoto Effects of cholinergic depletion on neuron activities in the cat visual cortex J. Neurophysiol. 58 1987 781 794
136. J.T. Serences, S. Shomstein, A.B. Leber, X. Golay, H.E. Egeth, and S. Yantis Coordination of voluntary and stimulus-driven attentional control in human cortex Psychol. Sci. 16 2005 114 122 10.1111/j.0956-7976.2005.00791.x
137. J.K. Shirey, A.E. Brady, P.J. Jones, A.A. Davis, T.M. Bridges, J.P. Kennedy, S.B. Jadhav, U.N. Menon, Z. Xiang, M.L. Watson, E.P. Christian, J.J. Doherty, M.C. Quirk, D.H. Snyder, J.J. Lah, A.I. Levey, M.M. Nicolle, C.W. Lindsley, and P.J. Conn 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 2009 14271 14286 10.1523/JNEUROSCI.3930-09.2009
138. M.A. Silver, A. Shenhav, and M. D'Esposito Cholinergic enhancement reduces spatial spread of visual responses in human early visual cortex Neuron 60 2008 904 914 10.1016/j.neuron.2008.09.038
139. M. St. Peters, A. Koshy Cherian, M. Bradshaw, and M. Sarter Sustained attention in mice: expanding the translational utility of the SAT by incorporating the Michigan Controlled Access Response Port (MICARP) Behav. Brain Res. 225 2011 574 583 10.1016/j.bbr.2011.08.025
140. M. St. Peters, E. Demeter, C. Lustig, J.P. Bruno, and M. Sarter Enhanced control of attention by stimulating mesolimbic-corticopetal cholinergic circuitry J. Neurosci. 31 2011 9760 9771 10.1523/JNEUROSCI.1902-11.2011
141. T. Sunderland, P.N. Tariot, R.M. Cohen, H. Weingartner, E.A. Mueller, and D.L. Murphy Anticholinergic sensitivity in patients with dementia of the Alzheimer type and age-matched controls. A dose-response study Arch. Gen. Psychiatry 44 1987 418 426 10.1001/archpsyc.1987.01800170032006
142. T. Sunderland, P.N. Tariot, and P.A. Newhouse Differential responsivity of mood, behavior, and cognition to cholinergic agents in elderly neuropsychiatric populations Brain Res. 472 1988 371 389 10.1016/0165-0173(88) 90013-6
143. R. Tandon, and J. Greden Cholinergic hyperactivity and negative schizophrenic symptoms. A model of cholinergic/dopaminergic interactions in
144. Taylor, K.; Decker, M.W.; Sarter, M.; Parikh, V.; 2011. Viability of α4β2* nAChRs as a Target for Treating the Cognitive Symptoms of Schizophrenia in the Presence of Chronic Nicotine and Risperidone. Paper presented at the Society for Neuroscience Annual Meeting, Washington, DC.
145. C.M. Thiel, K. Zilles, and G.R. Fink Nicotine modulates reorienting of visuospatial attention and neural activity in human parietal cortex Neuropsychopharmacology 30 2005 810 820 10.1038/sj.npp.1300633
146. A.M. Treisman, and G. Gelade A feature-integration theory of attention Cogn. Psychol. 12 1980 97 136 10.1016/0010-0285(80)90005-5
147. J. Turchi, and M. Sarter Cortical acetylcholine and processing capacity: effects of cortical cholinergic deafferentation on crossmodal divided attention in rats Cogn. Brain Res. 6 1997 147 158 10.1016/S0926-6410(97)00027-X
148. J. Turchi, L.A. Holley, and M. Sarter Effects of nicotinic acetylcholine receptor ligands on behavioral vigilance in rats Psychopharmacology (Berl.) 118 1995 195 205 10.1007/BF02245840
149. S. Vangkilde, C. Bundesen, and J.T. Coull Prompt but inefficient: nicotine differentially modulates discrete components of attention Psychopharmacology 218 2011 667 680 10.1007/s00213-011-2361-x
150. S. Vossel, C.M. Thiel, and G.R. Fink Behavioral and neural effects of nicotine on visuospatial attentional reorienting in non-smoking subjects Neuropsychopharmacology 33 2008 731 738 10.1038/sj.npp.1301469
151. D.M. Warburton, and G. Mancuso Evaluation of the information processing and mood effects of a transdermal nicotine patch Psychopharmacology (Berl.) 135 1998 305 310 10.1007/s002130050514
152. K. Wesnes, and D.M. Warburton Effects of scopolamine and nicotine on human rapid information processing performance Psychopharmacology (Berl.) 82 1984 147 150 10.1007/BF00427761
153. J. Wess Molecular biology of muscarinic acetylcholine receptors Crit. Rev. Neurobiol. 10 1996 69 99
154. T.E. Wilens, and M.W. Decker Neuronal nicotinic receptor agonists for the treatment of attention-deficit/hyperactivity disorder: focus on cognition Biochem. Pharmacol. 74 2007 1212 1223 10.1016/j.biopsych.2005.10.029
155. T.E. Wilens, M.H. Verlinden, L.A. Adler, P.J. Wozniak, and S.A. West 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 2006 1065 1070 10.1016/j.biopsych.2005.10.029
156. T.E. Wilens, L.M. Gault, A. Childress, C.J. Kratochvil, L. Bensman, and C.M. Hall Safety and efficacy of ABT-089 in pediatric attention-deficit/ hyperactivity disorder: results from two randomized placebo-controlled clinical trials J. Am. Acad. Child Adolesc. Psychiatry 50 2011 73 84 10.1016/j.jaac.2010. 10.001
157. G.W. Wohlberg, and C. Kornetsky Sustained attention in remitted schizophrenics Arch. Gen. Psychiatry 28 1973 533 537
158. M. Yamada, K.G. Lamping, A. Duttaroy, W. Zhang, Y. Cui, F.P. Bymaster, D.L. McKinzie, C.C. Felder, C.X. Deng, F.M. Faraci, and J. Wess Cholinergic dilation of cerebral blood vessels is abolished in M(5) muscarinic acetylcholine receptor knockout mice Proc. Natl. Acad. Sci. U. S. A. 98 2001 14096 14101 10.1073/pnas.251542998
159. J.W. Young, K. Finlayson, C. Spratt, H.M. Marston, N. Crawford, and J.S. Kelly Nicotine improves sustained attention in mice: evidence for involvement of the α7 nicotinic acetylcholine receptor Neuropsychopharmacology 29 2004 891 900 10.1038/sj.npp.1300393
160. L. Zaborszky, and W.E. Cullinan Projections from the nucleus accumbens to cholinergic neurons of the ventral pallidum: a correlated light and electron microscopic double immunolabeling study in rat Brain Res. 570 1992 92 101 10.1016/0006-8993(92)90568-T
161. L. Zaborszky, and W.E. Cullinan Direct catecholaminergic-cholinergic interactions in the basal forebrain. I. Dopamine-betahydroxylase and tyrosine hydroxylase input to cholinergic neurons J. Comp. Neurol. 374 1996 535 554 10.1002/(SICI)1096-9861(19961028)374:4<535::AID-CNE>3.0.CO;2-2
162. L. Zaborszky, C. Leranth, and L. Heimer Ultrastructural evidence of amygdalofugal axons terminating on cholinergic cells of the rostral forebrain Neurosci. Lett. 52 1984 219 225 10.1016/0304-3940(84)90165-4
163. L. Zaborszky, L. Heimer, F. Eckenstein, and C. Leranth GABAergic input to cholinergic forebrain neurons: an ultrastructural study using retrograde tracing of HRP and double immunolabeling J. Comp. Neurol. 250 1986 282 295 10.1002/cne.902500303
164. L. Zaborszky, W.E. Cullinan, and V.N. Luine Catecholaminergic-cholinergic interaction in the basal forebrain Prog. Brain Res. 98 1993 31 49 10.1016/S0079-6123(08)62379-1
165. L. Zaborszky, R.P. Gaykema, D.J. Swanson, and W.E. Cullinan Cortical input to the basal forebrain Neuroscience 79 1997 1051 1078 10.1016/S0306- 4522(97)00049-3
166. L. Zaborszky, K. Pang, J. Somogyi, Z. Nadasdy, and I. Kallo The basal forebrain corticopetal system revisited Ann. N. Y. Acad. Sci. 877 1999 339 367 10.1111/j.1749-6632.1999.tb09276.x
167. L. Zaborszky, D.L. Buhl, S. Pobalashingham, J.G. Bjaalie, and Z. Nadasdy Three-dimensional chemoarchitecture of the basal forebrain: spatially specific association of cholinergic and calcium binding protein-containing neurons Neuroscience 136 2005 697 713 10.1016/j.neuroscience.2005.05.019
168. L. Zaborszky The modular organization of brain systems. Basal forebrain: the last frontier Prog. Brain Res. 136 2002 359 372 10.1016/S0079-6123(02)36030- 8
169. B. Zikopoulos, and H. Barbas Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms J. Neurosci. 26 2006 7348 7361 10.1523/JNEUROSCI.5511-05.2006