Paying more attention to attention: Towards more comprehensive cognitive translation using mouse models of Alzheimer's disease

Brain Research Bulletin

Volumn 92, Issue , 2013, Pages 49-55

  Romberg, Carola ^a   Bussey, Timothy J ^b,c   Saksida, Lisa M ^b,c  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b UK   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

5 Choice serial reaction time task; Alzheimer's disease; Animal behaviour; Attention; Cognition; Mouse models

Indexed keywords

ALZHEIMER DISEASE; ATTENTION; ATTENTION DEFICIT DISORDER; CHOLINERGIC NERVE CELL; COGNITION; DISEASE MODEL; EXECUTIVE FUNCTION; INHIBITION (PSYCHOLOGY); MENTAL TEST; NERVE CELL NETWORK; NONHUMAN; PARIETAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; SELECTIVE ATTENTION;

ALZHEIMER DISEASE; ANIMALS; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; COGNITION DISORDERS; COMPREHENSION; DISEASE MODELS, ANIMAL; HUMANS; MICE;

EID: 84875234023     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2012.02.007     Document Type: Review

References (111)

1. Alexander D.A. Attention dysfunction in senile dementia. Psychol. Rep. 1973, 32:229-230.
2. Artero S., Ritchie K. The detection of mild cognitive impairment in the general practice setting. Aging Ment. Health 2003, 7:251-258.
3. Baddeley A., Cocchini G., Della Sala S., Logie R.H., Spinnler H. Working memory and vigilance: evidence from normal aging and Alzheimer's disease. Brain Cogn. 1999, 41:87-108.
4. Baddeley A., Logie R., Bressi S., Della Sala S., Spinnler H. Dementia and working memory. Q. J. Exp. Psychol. A 1986, 38:603-618.
5. Baddeley A.D., Baddeley H.A., Bucks R.S., Wilcock G.K. Attentional control in Alzheimer's disease. Brain 2001, 124:1492-1508.
6. Bari A., Dalley J.W., Robbins T.W. The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat. Protoc. 2008, 3:759-767.
7. Baudic S., Barba G.D., Thibaudet M.C., Smagghe A., Remy P., Traykov L. Executive function deficits in early Alzheimer's disease and their relations with episodic memory. Arch. Clin. Neuropsychol. 2006, 21:15-21.
8. Beck L.H., Bransome E.D., Mirsky A.F., Rosvold H.E., Sarason I. A continuous performance test of brain damage. J. Consult. Psychol. 1956, 20:343-350.
9. Belleville S., Chertkow H., Gauthier S. Working memory and control of attention in persons with Alzheimer's disease and mild cognitive impairment. Neuropsychology 2007, 21:458-469.
10. Bentley P., Driver J., Dolan R.J. Cholinesterase inhibition modulates visual and attentional brain responses in Alzheimer's disease and health. Brain 2008, 131:409-424.
11. Bentley P., Vuilleumier P., Thiel C.M., Driver J., Dolan R.J. Cholinergic enhancement modulates neural correlates of selective attention and emotional processing. Neuroimage 2003, 20:58-70.
12. Berardi A.M., Parasuraman R., Haxby J.V. Sustained attention in mild Alzheimer's disease. Dev. Neuropsychol. 2005, 28:507-537.
13. Braak H., Braak E. Demonstration of amyloid deposits and neurofibrillary changes in whole brain sections. Brain Pathol. 1991, 1:213-216.
14. Brazzelli M., Cocchini G., Della Sala S., Spinnler H. Alzheimer patients show a sensitivity decrement over time on a tonic alertness task. J. Clin. Exp. Neuropsychol. 1994, 16:851-860.
15. Bushnell P.J. Behavioral approaches to the assessment of attention in animals. Psychopharmacology (Berl.) 1998, 138:231-259.
16. Bussey T.J., Holmes A., Lyon L., Mar A.C., McAllister K.A., Nithianantharajah J., Oomen C.A., Saksida L.M. New translational assays for preclinical modelling of cognition in schizophrenia: the touchscreen testing method for mice and rats. Neuropharmacology 2012, 62:1191-1203.
17. Bussey T.J., Padain T.L., Skillings E.A., Winters B.D., Morton A.J., Saksida L.M. The touchscreen cognitive testing method for rodents: how to get the best out of your rat. Learn. Mem. 2008, 15:516-523.
18. Bussey T.J., Saksida L.M., Rothblat L.A. Discrimination of computer-graphic stimuli by mice: a method for the behavioral characterization of transgenic and gene-knockout models. Behav. Neurosci. 2001, 115:957-960.
19. Caffarra P., Riggio L., Malvezzi L., Scaglioni A., Freedman M. Orienting of visual attention in Alzheimer's disease: its implication in favor of the interhemispheric balance. Neuropsychiatry Neuropsychol. Behav. Neurol. 1997, 10:90-95.
20. Carli M., Robbins T.W., Evenden J.L., Everitt B.J. Effects of lesions to ascending noradrenergic neurones on performance of a 5-choice serial reaction task in rats; implications for theories of dorsal noradrenergic bundle function based on selective attention and arousal. Behav. Brain Res. 1983, 9:361-380.
21. Chiba A.A., Bushnell P.J., Oshiro W.M., Gallagher M. Selective removal of cholinergic neurons in the basal forebrain alters cued target detection. Neuroreport 1999, 10:3119-3123.
22. Chu C.C., Tranel D., Damasio A.R., Van Hoesen G.W. The autonomic-related cortex: pathology in Alzheimer's disease. Cereb. Cortex 1997, 7:86-95.
23. Chudasama Y. Animal models of prefrontal-executive function. Behav. Neurosci. 2011, 125:327-343.
24. Chudasama Y., Passetti F., Rhodes S.E., Lopian D., Desai A., Robbins T.W. Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity and compulsivity. Behav. Brain Res. 2003, 146:105-119.
25. Collette F., Van der Linden M., Delrue G., Salmon E. Frontal hypometabolism does not explain inhibitory dysfunction in Alzheimer disease. Alzheimer Dis. Assoc. Disord. 2002, 16:228-238.
26. Corbetta M., Shulman G.L. Human cortical mechanisms of visual attention during orienting and search. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1998, 353:1353-1362.
27. Corbetta M., Shulman G.L., Miezin F.M., Petersen S.E. Superior parietal cortex activation during spatial attention shifts and visual feature conjunction. Science 1995, 270:802-805.
28. Coull J.T., Frith C.D., Frackowiak R.S., Grasby P.M. A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory. Neuropsychologia 1996, 34:1085-1095.
29. Cutuli D., Foti F., Mandolesi L., De Bartolo P., Gelfo F., Federico F., Petrosini L. Cognitive performances of cholinergically depleted rats following chronic donepezil administration. J. Alzheimers Dis. 2009, 17:161-176.
30. Dalley J.W., Theobald D.E., Bouger P., Chudasama Y., Cardinal R.N., Robbins T.W. Cortical cholinergic function and deficits in visual attentional performance in rats following 192 IgG-saporin-induced lesions of the medial prefrontal cortex. Cereb. Cortex 2004, 14:922-932.
31. Davies D.P.R. The Psychology of Vigilance 1982.
32. de Bruin N.M., Fransen F., Duytschaever H., Grantham C., Megens A.A. Attentional performance of (C57BL/6Jx129Sv)F2 mice in the five-choice serial reaction time task. Physiol. Behav. 2006, 89:692-703.
33. Dermaut B., Kumar-Singh S., Rademakers R., Theuns J., Cruts M., Van Broeckhoven C. Tau is central in the genetic Alzheimer-frontotemporal dementia spectrum. Trends Genet. 2005, 21:664-672.
34. Duncan J. EPS Mid-Career Award 2004: brain mechanisms of attention. Q. J. Exp. Psychol. (Colchester) 2006, 59:2-27.
35. Duyckaerts C., Potier M.C., Delatour B. Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol. 2008, 115:5-38.
36. Eriksen J.L., Janus C.G. Plaques, tangles, and memory loss in mouse models of neurodegeneration. Behav. Genet. 2007, 37:79-100.
37. Faust M.E., Balota D.A. Inhibition of return and visuospatial attention in healthy older adults and individuals with dementia of the Alzheimer type. Neuropsychology 1997, 11:13-29.
38. Ferris S., Schneider L., Farmer M., Kay G., Crook T. A double-blind, placebo-controlled trial of memantine in age-associated memory impairment (memantine in AAMI). Int. J. Geriatr. Psychiatry 2007, 22:448-455.
39. Foldi N.S., Schaefer L.A., White R.E., Johnson R., Berger J.T., Carney M.T., Macina L.O. Effects of graded levels of physical similarity and density on visual selective attention in patients with Alzheimer's disease. Neuropsychology 2005, 19:5-17.
40. Gallagher M., Holland P.C. The amygdala complex: multiple roles in associative learning and attention. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:11771-11776.
41. Gotz J., Ittner L.M. Animal models of Alzheimer's disease and frontotemporal dementia. Nat. Rev. Neurosci. 2008, 9:532-544.
42. Haass C. Presenilins: genes for life and death. Neuron 1997, 18:687-690.
43. Huff F.J., Becker J.T., Belle S.H., Nebes R.D., Holland A.L., Boller F. Cognitive deficits and clinical diagnosis of Alzheimer's disease. Neurology 1987, 37:1119-1124.
44. Humby T., Laird F.M., Davies W., Wilkinson L.S. Visuospatial attentional functioning in mice: interactions between cholinergic manipulations and genotype. Eur. J. Neurosci. 1999, 11:2813-2823.
45. Huntley J.D., Howard R.J. Working memory in early Alzheimer's disease: a neuropsychological review. Int. J. Geriatr. Psychiatry 2010, 25:121-132.
46. Jones D.N., Higgins G.A. Effect of scopolamine on visual attention in rats. Psychopharmacology (Berl.) 1995, 120:142-149.
47. Kastner S., Ungerleider L.G. Mechanisms of visual attention in the human cortex. Annu. Rev. Neurosci. 2000, 23:315-341.
48. Lambourne S.L., Humby T., Isles A.R., Emson P.C., Spillantini M.G., Wilkinson L.S. Impairments in impulse control in mice transgenic for the human FTDP-17 tauV337M mutation are exacerbated by age. Hum. Mol. Genet. 2007, 16:1708-1719.
49. Lee H.J., Youn J.M.M.J.O., Gallagher M., Holland P.C. Role of substantia nigra-amygdala connections in surprise-induced enhancement of attention. J. Neurosci. 2006, 26:6077-6081.
50. Levinoff E.J., Saumier D., Chertkow H. Focused attention deficits in patients with Alzheimer's disease and mild cognitive impairment. Brain Cogn. 2005, 57:127-130.
51. Lewin J.S., Friedman L., Wu D., Miller D.A., Thompson L.A., Klein S.K., Wise A.L., Hedera P., Buckley P., Meltzer H., Friedland R.P., Duerk J.L. Cortical localization of human sustained attention: detection with functional MR using a visual vigilance paradigm. J. Comput. Assist. Tomogr. 1996, 20:695-701.
52. Lichstein K.L., Riedel B.W., Richman S.L. The Mackworth Clock Test: a computerized version. J. Psychol. 2000, 134:153-161.
53. Lines C.R., Dawson C., Preston G.C., Reich S., Foster C., Traub M. Memory and attention in patients with senile dementia of the Alzheimer type and in normal elderly subjects. J. Clin. Exp. Neuropsychol. 1991, 13:691-702.
54. Mackworth N.H. The breakdown of vigilance during prolonged visual search. Q. J. Exp. Psychol. 1948, 1:6-21.
55. Manly T., Owen A.M., McAvinue L., Datta A., Lewis G.H., Scott S.K., Rorden C., Pickard J., Robertson I.H. Enhancing the sensitivity of a sustained attention task to frontal damage: convergent clinical and functional imaging evidence. Neurocase 2003, 9:340-349.
56. Martin L.A., Goldowitz D., Mittleman G. Sustained attention in the mouse: a study of the relationship with the cerebellum. Behav. Neurosci. 2006, 120:477-481.
57. Martin S.J., Clark R.E. The rodent hippocampus and spatial memory: from synapses to systems. Cell. Mol. Life Sci. 2007, 64:401-431.
58. Martin S.J., Morris R.G. New life in an old idea: the synaptic plasticity and memory hypothesis revisited. Hippocampus 2002, 12:609-636.
59. McGaughy J., Dalley J.W., Morrison C.H., Everitt B.J., Robbins T.W. Selective behavioral and neurochemical effects of cholinergic lesions produced by intrabasalis infusions of 192 IgG-saporin on attentional performance in a five-choice serial reaction time task. J. Neurosci. 2002, 22:1905-1913.
60. McGaughy J., Kaiser T., Sarter M. 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. 1996, 110:247-265.
61. McGaughy J., Sandstrom M., Ruland S., Bruno J.P., Sarter M. Lack of effects of lesions of the dorsal noradrenergic bundle on behavioral vigilance. Behav. Neurosci. 1997, 111:646-652.
62. McGaughy J., Sarter M. Behavioral vigilance in rats: task validation and effects of age amphetamine, and benzodiazepine receptor ligands. Psychopharmacology (Berl.) 1995, 117:340-357.
63. McGaughy J., Sarter M. Sustained attention performance in rats with intracortical infusions of 192 IgG-saporin-induced cortical cholinergic deafferentation: effects of physostigmine and FG 7142. Behav. Neurosci. 1998, 112:1519-1525.
64. McGuinness B., Barrett S.L., Craig D., Lawson J., Passmore A.P. Attention deficits in Alzheimer's disease and vascular dementia. J. Neurol. Neurosurg. Psychiatry 2010, 81:157-159.
65. McKhann G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984, 34:939-944.
66. Mirsky A.F., Anthony B.J., Duncan C.C., Ahearn M.B., Kellam S.G. Analysis of the elements of attention: a neuropsychological approach. Neuropsychol. Rev. 1991, 2:109-145.
67. Morton A.J., Skillings E., Bussey T.J., Saksida L.M. Measuring cognitive deficits in disabled mice using an automated interactive touchscreen system. Nat. Methods 2006, 3:767.
68. Muir J.L. Attention and stimulus processing in the rat. Brain Res. Cogn. Brain Res. 1996, 3:215-225.
69. Muir J.L. Acetylcholine, aging, and Alzheimer's disease. Pharmacol. Biochem. Behav. 1997, 56:687-696.
70. Muir J.L., Dunnett S.B., Robbins T.W., Everitt B.J. Attentional functions of the forebrain cholinergic systems: effects of intraventricular hemicholinium, physostigmine, basal forebrain lesions and intracortical grafts on a multiple-choice serial reaction time task. Exp. Brain Res. 1992, 89:611-622.
71. Muzzio I.A., Kentros C., Kandel E. What is remembered? Role of attention on the encoding and retrieval of hippocampal representations. J. Physiol. 2009, 587:2837-2854.
72. Muzzio I.A., Levita L., Kulkarni J., Monaco J., Kentros C., Stead M., Abbott L.F., Kandel E.R. Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus. PLoS Biol. 2009, 7:e1000140.
73. Nebes R.D., Brady C.B. Focused divided attention in Alzheimer's disease. Cortex 1989, 25:305-315.
74. Nebes R.D., Brady C.B. Phasic and tonic alertness in Alzheimer's disease. Cortex 1993, 29:77-90.
75. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003, 39:409-421.
76. Oken B.S., Kishiyama S.S., Kaye J.A., Howieson D.B. Attention deficit in Alzheimer's disease is not simulated by an anticholinergic/antihistaminergic drug and is distinct from deficits in healthy aging. Neurology 1994, 44:657-662.
77. Parasuraman R., Haxby J.V. Attention brain function in Alzheimer's disease: a review. Neuropsychology 1993, 7:242-272.
78. Patel S., Stolerman I.P., Asherson P., Sluyter F. Attentional performance of C57BL/6 and DBA/2 mice in the 5-choice serial reaction time task. Behav. Brain Res. 2006, 170:197-203.
79. Pattij T., Janssen M.C., Loos M., Smit A.B., Schoffelmeer A.N., van Gaalen M.M. Strain specificity and cholinergic modulation of visuospatial attention in three inbred mouse strains. Genes Brain Behav. 2007, 6:579-587.
80. Perry R.J., Hodges J.R. Attention and executive deficits in Alzheimer's disease. A critical review. Brain 1999, 122(Pt 3):383-404.
81. Perry R.J., Watson P., Hodges J.R. The nature and staging of attention dysfunction in early (minimal and mild) Alzheimer's disease: relationship to episodic and semantic memory impairment. Neuropsychologia 2000, 38:252-271.
82. Posner M.I. Measuring alertness. Ann. N. Y. Acad. Sci. 2008, 1129:193-199.
83. Posner M.I., Petersen S.E. The attention system of the human brain. Annu. Rev. Neurosci. 1990, 13:25-42.
84. Posner M.I., Snyder C.R., Davidson B.J. Attention and the detection of signals. J. Exp. Psychol. 1980, 109:160-174.
85. Raz A., Buhle J. Typologies of attentional networks. Nat. Rev. Neurosci. 2006, 7:367-379.
86. Reid W., Broe G., Creasey H., Grayson D., McCusker E., Bennett H., Longley W., Sulway M.R. Age at onset and pattern of neuropsychological impairment in mild early-stage Alzheimer disease. A study of a community-based population. Arch. Neurol. 1996, 53:1056-1061.
87. Riepe M.W., Adler G., Ibach B., Weinkauf B., Gunay I., Tracik F. Adding memantine to rivastigmine therapy in patients with mild-to-moderate Alzheimer's disease: results of a 12-week, open-label pilot study. Prim. Care Companion J. Clin. Psychiatry 2006, 8:258-263.
88. Robbins T.W. The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl.) 2002, 163:362-380.
89. Robbins T.W., James M., Owen A.M., Sahakian B.J., McInnes L., Rabbitt P. Cambridge Neuropsychological Test Automated Battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. Dementia 1994, 5:266-281.
90. Robbins T.W., Weinberger D., Taylor J.G., Morris R.G. Dissociating executive functions of the prefrontal cortex [and discussion]. Phil. Trans. R. Soc. Lond. B 1996, 351:1463-1471.
91. Romberg C., Mattson M.P., Mughal M.R., Bussey T.J., Saksida L.M. Impaired attention in the 3xTgAD mouse model of Alzheimer's disease: rescue by donepezil (Aricept). J. Neurosci. 2011, 31:3500-3507.
92. Rosner A.L., Mittleman G. Visuospatial attention in the rat and posterior parietal cortex lesions. Behav. Brain Res. 1996, 79:69-77.
93. Sahakian B., Jones G., Levy R., Gray J., Warburton D. The effects of nicotine on attention, information processing, and short-term memory in patients with dementia of the Alzheimer type. Br. J. Psychiatry 1989, 154:797-800.
94. Sahakian B.J., Coull J.T. Tetrahydroaminoacridine (THA) in Alzheimer's disease: an assessment of attentional and mnemonic function using CANTAB. Acta Neurol. Scand. Suppl. 1993, 149:29-35.
95. Sarter M., Bruno J.P. Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res. Brain Res. Rev. 1997, 23:28-46.
96. Sarter M., Bruno J.P., Givens B. Attentional functions of cortical cholinergic inputs: what does it mean for learning and memory?. Neurobiol. Learn. Mem. 2003, 80:245-256.
97. Sarter M., Givens B., Bruno J.P. The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res. Brain Res. Rev. 2001, 35:146-160.
98. Sarter M., Turchi J. Age- and dementia-associated impairments in divided attention: psychological constructs, animal models, and underlying neuronal mechanisms. Dement. Geriatr. Cogn. Disord. 2002, 13:46-58.
99. Selkoe D.J. The cell biology of beta-amyloid precursor protein and presenilin in Alzheimer's disease. Trends Cell Biol. 1998, 8:447-453.
100. Silveri M.C., Reali G., Jenner C., Puopolo M. Attention and memory in the preclinical stage of dementia. J. Geriatr. Psychiatry Neurol. 2007, 20:67-75.
101. Sohlberg M.M., Mateer C.A. Effectiveness of an attention-training program. J. Clin. Exp. Neuropsychol. 1987, 9:117-130.
102. St Peters .M., Cherian K.A., Bradshaw M., Sarter M. Sustained attention in mice: expanding the translational utility of the SAT by incorporating the Michigan Controlled Access Response Port (MICARP). Behav. Brain Res. 2011, 225:574-583.
103. Waldemar G., Dubois B., Emre M., Georges J., McKeith I.G., Rossor M., Scheltens P., Tariska P., Winblad B. Recommendations for the diagnosis and management of Alzheimer's disease and other disorders associated with dementia: EFNS guideline. Eur. J. Neurol. 2007, 14:e1-e26.
104. Ward N.M., Brown V.J. Covert orienting of attention in the rat and the role of striatal dopamine. J. Neurosci. 1996, 16:3082-3088.
105. Welsh K.A., Butters N., Hughes J.P., Mohs R.C., Heyman A. Detection and staging of dementia in Alzheimer's disease. Use of the neuropsychological measures developed for the Consortium to Establish a Registry for Alzheimer's Disease. Arch. Neurol. 1992, 49:448-452.
106. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., Delon M.R. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 1982, 215:1237-1239.
107. Wilkins A.J., Shallice T., McCarthy R. Frontal lesions and sustained attention. Neuropsychologia 1987, 25:359-365.
108. Wilkinson R.T. Interaction of noise with knowledge of results and sleep deprivation. J. Exp. Psychol. 1963, 66:332-337.
109. Winters B.D., Saksida L.M., Bussey T.J. Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci. Biobehav. Rev. 2008, 32:1055-1070.
110. Young J.W., Light G.A., Marston H.M., Sharp R., Geyer M.A. The 5-choice continuous performance test: evidence for a translational test of vigilance for mice. PLoS ONE 2009, 4:e4227.
111. Zahs K.R., Ashe K.H. 'Too much good news' - are Alzheimer mouse models trying to tell us how to prevent, not cure, Alzheimer's disease?. Trends Neurosci. 2010, 33:381-389.