Both a nicotinic single nucleotide polymorphism (SNP) and a noradrenergic SNP modulate working memory performance when attention is manipulated

Journal of Cognitive Neuroscience

Volumn 21, Issue 11, 2009, Pages 2139-2153

  Greenwood, Pamela M ^a   Sundararajan, Ramya ^b   Lin, Ming Kuan ^b   Kumar, Reshma ^a   Fryxell, Karl J ^b   Parasuraman, Raja ^a  

^a GEORGE MASON UNIVERSITY   (United States)

^b GEORGE MASON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINIC RECEPTOR;

ACCURACY; ADULT; AGE DISTRIBUTION; AGED; ALLELE; ARTICLE; ATTENTION; CHOLINERGIC ACTIVITY; COGNITION; CONTROLLED STUDY; DEPTH PERCEPTION; FEMALE; GENE; HOMOZYGOTE; HUMAN; HUMAN EXPERIMENT; MALE; NEUROTRANSMISSION; NORADRENERGIC SYSTEM; NORMAL HUMAN; PERFORMANCE; PRIORITY JOURNAL; REACTION TIME; SINGLE NUCLEOTIDE POLYMORPHISM; WORKING MEMORY;

ADOLESCENT; AGED; AGING; ATTENTION; CUES; DISCRIMINATION (PSYCHOLOGY); DOPAMINE BETA-HYDROXYLASE; FEMALE; GENETIC VARIATION; HUMANS; MALE; MEMORY, SHORT-TERM; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, NICOTINIC; RECOGNITION (PSYCHOLOGY); REFERENCE VALUES; SPACE PERCEPTION; YOUNG ADULT;

EID: 70349245477     PISSN: 0898929X     EISSN: 15308898     Source Type: Journal    
DOI: 10.1162/jocn.2008.21164     Document Type: Article

References (86)

1. Abi-Dargham, A., Mawlawi, O., Lombardo, I., Gil, R., Martinez, D., Huang, Y., et al. (2002). Prefrontal dopamine D1 receptors and working memory in schizophrenia. Journal of Neuroscience, 22, 3708-3719. (Pubitemid 37465776)
2. Ammassari-Teule, M., Maho, C., & Sara, S. J. (1991). Clonidine reverses spatial learning deficits and reinstates theta frequencies in rats with partial fornix section. Behavioural Brain Research, 45, 1-8.
3. Avery, R. A., Franowicz, J. S., Studholme, C., van Dyck, C. H., & Arnsten, A. F. (2000). The alpha-2A-adrenoceptor agonist, guanfacine, increases regional cerebral blood f low in dorsolateral prefrontal cortex of monkeys performing a spatial working memory task. Neuropsychopharmacology, 23, 240-249. (Pubitemid 30609658)
4. Awh, E., & Jonides, J. (1998). Spatial working memory and spatial selective attention. In R. Parasuraman (Ed.), The attentive brain (pp. 353-380). Cambridge, MA: MIT Press.
5. Awh, E., Jonides, J., & Reuter-Lorenz, P. A. (1998). Rehearsal in spatial working memory. Journal of Experimental Psychology: Human Perception and Performance, 24, 780-790.
6. Awh, E., Vogel, E. K., & Oh, S. H. (2006). Interactions between attention and working memory. Neuroscience, 139, 201-208.
7. Baddeley, A. (1992). Working memory. Science, 255, 556-559.
8. Barnett, J. H., Jones, P. B., Robbins, T. W., & Muller, U. (2007). Effects of the catechol-O-methyltransferase Val158Met polymorphism on executive function: A meta-analysis of the Wisconsin Card Sort Test in schizophrenia and healthy controls. Molecular Psychiatry, 12, 502-509.
9. Bleckley, M. K., Durso, F. T., Crutchfield, J. M., Engle, R. W., & Khanna, M. M. (2003). Individual differences in working memory capacity predict visual attention allocation. Psychonomic Bulletin & Review, 10, 884-889. (Pubitemid 38483383)
10. Castner, S. A., Williams, G. V., & Goldman-Rakic, P. S. (2000). Reversal of antipsychotic-induced working memory deficits by short-term dopamine D1 receptor stimulation. Science, 287, 2020-2022.
11. Chudasama, Y., Dalley, J. W., Nathwani, F., Bouger, P., & Robbins, T. W. (2004). Cholinergic modulation of visual attention and working memory: Dissociable effects of basal forebrain 192-IgG-saporin lesions and intraprefrontal infusions of scopolamine. Learning and Memory, 11, 78-86. (Pubitemid 38167061)
12. Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum.
13. Conway, A. R., Cowan, N., & Bunting, M. F. (2001). The cocktail party phenomenon revisited: The importance of working memory capacity. Psychonomic Bulletin & Review, 8, 331-335. (Pubitemid 33604184)
14. Couey, J. J., Meredith, R. M., Spijker, S., Poorthuis, R. B., Smit, A. B., Brussaard, A. B., et al. (2007). Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron, 54, 73-87. (Pubitemid 46498688)
15. Cowan, N. (1988). Evolving conceptions of memory storage, selective attention, and their mutual constraints within the human information-processing system. Psychological Bulletin, 104, 163-191.
16. Cowan, N. (2001). The magical number 4 in short-term memory: A reconsideration of mental storage capacity. Behavioral and Brain Sciences, 24, 87-114; discussion 114-185.
17. Cubells, J. F., van Kammen, D. P., Kelley, M. E., Anderson, G. M., O'Connor, D. T., Price, L. H., et al. (1998). Dopamine beta-hydroxylase: Two polymorphisms in linkage disequilibrium at the structural gene DBH associate with biochemical phenotypic variation. Human Genetics, 102, 533-540.
18. Curtis, C. E., & D'Esposito, M. (2003). Persistent activity in the prefrontal cortex during working memory. Trends in Cognitive Sciences, 7, 415-423. (Pubitemid 37083479)
19. Dani, J. A., & Bertrand, D. (2007). Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annual Review of Pharmacology and Toxicology, 47, 699-729. (Pubitemid 46272144)
20. Devauges, V., & Sara, S. J. (1990). Activation of the noradrenergic system facilitates an attentional shift in the rat. Behavioural Brain Research, 39, 19-28. (Pubitemid 20182169)
21. Dyon-Laurent, C., Herve, A., & Sara, S. J. (1994). Noradrenergic hyperactivity in hippocampus after partial denervation: Pharmacological, behavioral, and electrophysiological studies. Experimental Brain Research, 99, 259-266. (Pubitemid 24169596)
22. Engle, R. W., Kane, M. J., & Tuholski, S. W. (Eds.) (1999). Individual differences in working memory capacity and what they tell us about controlled attention, general f luid intelligence, and functions of the prefrontal cortex. Cambridge: Cambridge University Press.
23. Eriksen, C. W., & St James, J. D. (1986). Visual attention within and around the field of focal attention: A zoom lens model. Perception & Psychophysics, 40, 225-240.
24. Espeseth, T., Endestad, T., Rootwelt, H., & Reinvang, I. (2007). Nicotine receptor gene CHRNA4 modulates early event-related potentials in auditory and visual oddball target detection tasks. Neuroscience, 147, 974-985.
25. Espeseth, T., Greenwood, P. M., Reinvang, I., Fjell, A. M., Walhovd, K. B., Westlye, L. T., et al. (2006). Interactive effects of APOE and CHRNA4 on attention and white matter volume in healthy middle-aged and older adults. Cognitive, Affective, & Behavioral Neuroscience, 6, 31-43.
26. Everitt, B. J., & Robbins, T. W. (1997). Central cholinergic systems and cognition. Annual Review of Psychology, 48, 649-684.
27. Feng, Y., Niu, T., Xing, H., Xu, X., Chen, C., Peng, S., et al. (2004). A common haplotype of the nicotine acetylcholine receptor alpha 4 subunit gene is associated with vulnerability to nicotine addiction in men. American Journal of Human Genetics, 75, 112-121. (Pubitemid 38801907)
28. Flores, C. M., DeCamp, R. M., Kilo, S., Rogers, S. W., & Hargreaves, K. M. (1996). Neuronal nicotinic receptor expression in sensory neurons of the rat trigeminal ganglion: Demonstration of alpha3beta4, a novel subtype in the mammalian nervous system. Journal of Neuroscience, 16, 7892-7901. (Pubitemid 26405052)
29. Flores, C. M., Rogers, S. W., Pabreza, L. A., Wolfe, B. B., & Kellar, K. J. (1992). A subtype of nicotinic cholinergic receptor in rat brain is composed of alpha 4 and beta 2 subunits and is up-regulated by chronic nicotine treatment. Molecular Pharmacology, 41, 31-37.
30. Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). "Mini-mental state" - A practical method for grading the cognitive state of patients for the clinician. Journal of Current Psychiatric Research, 12, 189-198.
31. Fossella, J., Sommer, T., Fan, J., Wu, Y., Swanson, J. M., Pfaff, D. W., et al. (2002). Assessing the molecular genetics of attention networks. BMC Neuroscience, 3, 14. (Pubitemid 38729133)
32. Fossella, J. A., & Casey, B. J. (2006). Genes, brain, and behavior: Bridging disciplines. Cognitive, Affective & Behavioral Neuroscience, 6, 1-8.
33. Foxe, J. J., & Simpson, G. V. (2002). Flow of activation from V1 to frontal cortex in humans. A framework for defining "early" visual processing. Experimental Brain Research, 142, 139-150.
34. Franowicz, J. S., & Arnsten, A. F. (2002). Actions of alpha-2 noradrenergic agonists on spatial working memory and blood pressure in rhesus monkeys appear to be mediated by the same receptor subtype. Psychopharmacology (Berlin), 162, 304-312.
35. Furey, M. L., Pietrini, P., & Haxby, J. V. (2000). Cholinergic enhancement and increased selectivity of perceptual processing during working memory. Science, 290, 2315-2319. (Pubitemid 32041576)
36. Furey, M. L., Pietrini, P., Haxby, J. V., & Drevets, W. C. (2008). Selective effects of cholinergic modulation on task performance during selective attention. Neuropsychopharmacology, 33, 913-923. (Pubitemid 351252696)
37. Goldberg, T. E., & Weinberger, D. R. (2004). Genes and the parsing of cognitive processes. Trends in Cognitive Sciences, 8, 325-335.
38. Greenwood, P., Kumar, R., Sundararajan, R., Fryxell, K. J., Lin, M., & Parasuraman, R. (2006). Effects of attention on working memory are modulated by a nicotinic SNP (CHRNA4) but not a noradrenergic SNP (DBH). Paper presented at the Society for Neuroscience, Atlanta, Georgia.
39. Greenwood, P. M., Fossella, J. A., & Parasuraman, R. (2005). Specificity of the effect of a nicotinic receptor polymorphism on individual differences in visuospatial attention. Journal of Cognitive Neuroscience, 17, 1611-1620.
40. Greenwood, P. M., Lambert, C., Sunderland, T., & Parasuraman, R. (2005). Effects of apolipoprotein E genotype on spatial attention, working memory, and their interaction in healthy, middle-aged adults: Results from the National Institute of Mental Health's BIOCARD study. Neuropsychology, 19, 199-211. (Pubitemid 40381656)
41. Greenwood, P. M., & Parasuraman, R. (1999). Scale of attentional focus in visual search. Perception & Psychophysics, 61, 837-859.
42. Greenwood, P. M., & Parasuraman, R. (2003). Normal genetic variation, cognition, and aging. Behavioral and Cognitive Neuroscience Reviews, 2, 278-306.
43. Greenwood, P. M., & Parasuraman, R. (2004). The scaling of spatial attention in visual search and its modification in healthy aging. Perception & Psychophysics, 66, 3-22.
44. Greenwood, P. M., Sunderland, T., Putnam, K., Levy, J., & Parasuraman, R. (2005). Scaling of visuospatial attention undergoes differential longitudinal change as a function of APOE genotype prior to old age: Results from the NIMH BIOCARD study. Neuropsychology, 19, 830-840. (Pubitemid 41803530)
45. Griffin, I. C., & Nobre, A. C. (2003). Orienting attention to locations in internal representations. Journal of Cognitive Neuroscience, 15, 1176-1194.
46. Gu, Q. (2002). Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience, 111, 815-835. (Pubitemid 34603251)
47. Hare, M. P., & Palumbi, S. R. (1999). The accuracy of heterozygous base calling from diploid sequence and resolution of haplotypes using allele-specific sequencing. Molecular Ecology, 8, 1750-1752.
48. Hasselmo, M. E., Linster, C., Patil, M., Ma, D., & Cekic, M. (1997). Noradrenergic suppression of synaptic transmission may influence cortical signal-to-noise ratio. Journal of Neurophysiology, 77, 3326-3339. (Pubitemid 27290897)
49. Kent, L., Middle, F., Hawi, Z., Fitzgerald, M., Gill, M., Feehan, C., et al. (2001). Nicotinic acetylcholine receptor alpha4 subunit gene polymorphism and attention deficit hyperactivity disorder. Psychiatric Genetics, 11, 37-40. (Pubitemid 32499861)
50. Levin, E. D., Kaplan, S., & Boardman, A. (1997). Acute nicotine interactions with nicotinic and muscarinic antagonists: Working and reference memory effects in the 16-arm radial maze. Behavioural Pharmacology, 8, 236-242. (Pubitemid 27303918)
51. Levin, E. D., McClernon, F. J., & Rezvani, A. H. (2006). Nicotinic effects on cognitive function: Behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berlin), 184, 523-539.
52. Levin, E. D., & Simon, B. B. (1998). Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology (Berlin), 138, 217-230.
53. Mao, Z. M., Arnsten, A. F., & Li, B. M. (1999). Local infusion of an alpha-1 adrenergic agonist into the prefrontal cortex impairs spatial working memory performance in monkeys. Biological Psychiatry, 46, 1259-1265.
54. Matsukura, M., Luck, S. J., & Vecera, S. P. (2007). Attention effects during visual short-term memory maintenance: Protection or prioritization? Perception & Psychophysics, 69, 1422-1434.
55. Noesselt, T., Hillyard, S. A., Woldorff, M. G., Schoenfeld, A., Hagner, T., Jancke, L., et al. (2002). Delayed striate cortical activation during spatial attention. Neuron, 35, 575-587. (Pubitemid 34879955)
56. Parasuraman, R., & Greenwood, P. M. (2004). Molecular genetics of visuospatial attention and working memory. In M. I. Posner (Ed.), Cognitive neuroscience of attention (pp. 245-259). New York: Guilford.
57. Parasuraman, R., Greenwood, P. M., Haxby, J. V., & Grady, C. L. (1992). Visuospatial attention in dementia of the Alzheimer type. Brain, 115, 711-733.
58. Parasuraman, R., Greenwood, P. M., Kumar, R., & Fossella, J. (2005). Beyond heritability: Neurotransmitter genes differentially modulate visuospatial attention and working memory. Psychological Science, 16, 200-207. (Pubitemid 40451209)
59. Phillips, J. M., McAlonan, K., Robb, W. G., & Brown, V. J. (2000). Cholinergic neurotransmission influences covert orientation of visuospatial attention in the rat. Psychopharmacology (Berlin), 150, 112-116. (Pubitemid 30350820)
60. Posner, M. I., Rothbart, M. K., & Sheese, B. E. (2007). Attention genes. Developmental Science, 10, 24-29.
61. Postle, B. R. (2006). Working memory as an emergent property of the mind and brain. Neuroscience, 139, 23-38.
62. Ranganath, C. (2006). Working memory for visual objects: Complementary roles of inferior temporal, medial temporal, and prefrontal cortex. Neuroscience, 139, 277-289.
63. Rezvani, A. H., Bushnell, P. J., & Levin, E. D. (2002). Effects of nicotine and mecamylamine on choice accuracy in an operant visual signal detection task in female rats. Psychopharmacology (Berlin), 164, 369-375.
64. Robbins, T. W., Everitt, B. J., Marston, H. M., Wilkinson, J., Jones, G. H., & Page, K. J. (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. Behavioural Brain Research, 35, 221-240. (Pubitemid 20004659)
65. Robbins, T. W., Semple, J., Kumar, R., Truman, M. I., 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 of dementia. Psychopharmacology (Berlin), 134, 95-106. (Pubitemid 27485554)
66. Sahakian, B., Jones, G., Levy, R., Gray, J., & Warburton, D. (1989). The effects of nicotine on attention, information processing, and short-term memory in patients with dementia of the Alzheimer type. British Journal of Psychiatry, 154, 797-800. (Pubitemid 19172212)
67. Sara, S. J. (1989). Noradrenergic-cholinergic interaction: Its possible role in memory dysfunction associated with senile dementia. Archives of Gerontology and Geriatrics: Supplement, 1, 99-108.
68. Sarter, M., & Bruno, J. P. (2004). Developmental origins of the age-related decline in cortical cholinergic function and associated cognitive abilities. Neurobiology of Aging, 25, 1127-1139. (Pubitemid 39099262)
69. Shirtcliff, E. A., & Marrocco, R. T. (2003). Salivary cotinine levels in human tobacco smokers predict the attentional validity effect size during smoking abstinence. Psychopharmacology (Berlin), 166, 11-18.
70. Steinlein, O. K., Deckert, J., Nothen, M. M., Franke, P., Maier, W., Beckmann, H., et al. (1997). Neuronal nicotinic acetylcholine receptor alpha 4 subunit (CHRNA4) and panic disorder: An association study. American Journal of Medical Genetics, 74, 199-201. (Pubitemid 27187653)
71. Super, H., Spekreijse, H., & Lamme, V. A. (2001). A neural correlate of working memory in the monkey primary visual cortex. Science, 293, 120-124. (Pubitemid 32625508)
72. Thiel, C. M., Zilles, K., & Fink, G. R. (2005). Nicotine modulates reorienting of visuospatial attention and neural activity in human parietal cortex. Neuropsychopharmacology, 30, 810-820. (Pubitemid 40397088)
73. Vogel, E. K., & Machizawa, M. G. (2004). Neural activity predicts individual differences in visual working memory capacity. Nature, 428, 748-751. (Pubitemid 38508284)
74. Vogel, E. K., McCollough, A. W., & Machizawa, M. G. (2005). Neural measures reveal individual differences in controlling access to working memory. Nature, 438, 500-503.
75. Voytko, M. L. (1996). Cognitive functions of the basal forebrain cholinergic system in monkeys: Memory or attention? Behavioural Brain Research, 75, 13-25.
76. Voytko, M. L., Olton, D. S., Richardson, R. T., Gorman, L. K., Tobin, J. R., & Price, D. L. (1994). Basal forebrain lesions in monkeys disrupt attention but not learning and memory. Journal of Neuroscience, 14, 167-186.
77. Wang, J., Chuang, K., Ahluwalia, M., Patel, S., Umblas, N., Mirel, D., et al. (2005). High-throughput SNP genotyping by single-tube PCR with Tm-shift primers. BioTechniques, 39, 885-893.
78. Wechsler, D. (1981). Wechsler Adult Intelligence Scale - revised: Manual. New York: Psychological Corporation.
79. Wechsler, D. (1987). Wechsler Memory Scale - revised: Manual. New York: Psychological Corporation.
80. White, H. K., & Levin, E. D. (2004). Chronic transdermal nicotine patch treatment effects on cognitive performance in age-associated memory impairment. Psychopharmacology (Berlin), 171, 465-471.
81. Winterer, G., Musso, F., Konrad, A., Vucurevic, G., Stoeter, P., Sander, T., et al. (2007). Association of attentional network function with exon 5 variations of the CHRNA4 gene. Human Molecular Genetics, 16, 2165-2174. (Pubitemid 47354899)
82. Witte, E. A., Davidson, M. C., & Marrocco, R. T. (1997). Effects of altering brain cholinergic activity on covert orienting of attention: Comparison of monkey and human performance. Psychopharmacology (Berlin), 132, 324-334.
83. Witte, E. A., & Marrocco, R. T. (1997). Alteration of brain noradrenergic activity in rhesus monkeys affects the alerting component of covert orienting. Psychopharmacology (Berlin), 132, 315-323.
84. Wood, J. G., Joyce, P. R., Miller, A. L., Mulder, R. T., & Kennedy, M. A. (2002). A polymorphism in the dopamine beta-hydroxylase gene is associated with "paranoid ideation" in patients with major depression. Biological Psychiatry, 51, 365-369.
85. Yago, E., Duarte, A., Wong, T., Barcelo, F., & Knight, R. T. (2004). Temporal kinetics of prefrontal modulation of the extrastriate cortex during visual attention. Cognitive, Affective & Behavioral Neuroscience, 4, 609-617.
86. Yu, A. J., & Dayan, P. (2005). Uncertainty, neuromodulation, and attention. Neuron, 46, 681-692.