Synergistic effects of genetic variation in nicotinic and muscarinic receptors on visual attention but not working memory

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 9, 2009, Pages 3633-3638

  Greenwood, P M ^a   Lin, M K ^b   Sundararajan, R ^b   Fryxell, K J ^b   Parasuraman, R ^a  

^a GEORGE MASON UNIVERSITY   (United States)

^b GEORGE MASON UNIVERSITY   (United States)

Author keywords

Cholinergic; Cognition; Genetics; Synergism

Indexed keywords

MUSCARINIC M2 RECEPTOR; NICOTINIC RECEPTOR ALPHA4;

ADULT; AGED; ARTICLE; ASSOCIATION; ATTENTION; CHOLINERGIC ACTIVITY; COGNITION; CONTROLLED STUDY; FEMALE; GENE INTERACTION; GENETIC VARIABILITY; HOMOZYGOSITY; HUMAN; HUMAN EXPERIMENT; MALE; NEUROPSYCHOLOGICAL TEST; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; ORIENTATION; PRIORITY JOURNAL; REACTION TIME; SINGLE NUCLEOTIDE POLYMORPHISM; VISUAL STIMULATION; WORKING MEMORY;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ATTENTION; GENOTYPE; HUMANS; MEMORY; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, MUSCARINIC; RECEPTORS, NICOTINIC; VISUAL PERCEPTION;

EID: 62549140640     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0807891106     Document Type: Article

References (68)

1. Everitt BJ, Robbins TW (1997) Central cholinergic systems and cognition. Annu Rev Psychol 48:649-684.
2. Shirtcliff EA, Marrocco RT (2003) Salivary cotinine levels in human tobacco smokers predict the attentional validity effect size during smoking abstinence. Psychopharmacology 166:11-18.
3. Abi-Dargham A, et al. (2002) Prefrontal dopamine D1 receptors and working memory in schizophrenia. J Neurosci 22:3708-3719.
4. Sarter M, Bruno JP (2004) Developmental origins of the age-related decline in cortical cholinergic function and associated cognitive abilities. Neurobiol Aging 25:1127-1139.
5. Gu Q (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815-835.
6. Yu AJ, Dayan P (2005) Uncertainty, neuromodulation, and attention. Neuron 46:681-692.
7. Posner MI (1980) Orienting of attention. Q J Exp Psychol 32:3-25.
8. Phillips JM, McAlonan K, Robb WG, Brown VJ (2000) Cholinergic neurotransmission influences covert orientation of visuospatial attention in the rat. Psychopharmacology 150:112-116.
9. Witte EA, Davidson MC, Marrocco RT (1997) Effects of altering brain cholinergic activity on covert orienting of attention: Comparison of monkey and human performance. Psychopharmacology 132:324-334.
10. Davidson MC, Marrocco RT (2000) Local infusion of scopolamine into intraparietal cortex slows covert orienting in rhesus monkeys. J Neurophysiol 83:1536-1549.
11. Furey ML, Ricciardi E, Schapiro MB, Rapoport SI, Pietrini P (2008) Cholinergic enhancement eliminates modulation of neural activity by task difficulty in the prefrontal cortex during working memory. J Cognit Neurosci 20:1342-1353.
12. Furey ML, Pietrini P, Haxby JV, Drevets WC (2008) Selective effects of cholinergic modulation on task performance during selective attention. Neuropsychopharmacology 33:913-923.
13. Mentis MJ, et al. (2001) Muscarinic versus nicotinic modulation of a visual task: A pet study using drug probes. Neuropsychopharmacology 25:555-564.
14. Erskine FF, et al. (2004) Evidence for synergistic modulation of early information processing by nicotinic and muscarinic receptors in humans. Hum Psychopharmacol 19:503-509.
15. Green A, et al. (2005) Muscarinic and nicotinic receptor modulation of object and spatial n-back working memory in humans. Pharmacol Biochem Behav 81:575-584.
16. Ellis JR, et al. (2006) Muscarinic and nicotinic receptors synergistically modulate working memory and attention in humans. Int J Neuropsychopharmacol 9:175-189.
17. 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.
18. Flores CM, et al. (1992) A subtype of nicotinic cholinergic receptor in rat brain is composed of α4 and β2 subunits and is up-regulated by chronic nicotine treatment. Mol Pharmacol 41:31-37.
19. Greenwood PM, Parasuraman R (2003) Normal genetic variation, cognition, and aging. Behav Cognit Neurosci Rev 2:278-306.
20. Goldberg TE, Weinberger DR (2004) Genes and the parsing of cognitive processes. Trends Cognit Sci 8:325-335.
21. Hariri AR, et al. (2003) Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J Neurosci 23:6690-6694.
22. Mattay VS, et al. (2003) Catechol O-methyltransferase val158-met genotype and individual variation in the brain response to amphetamine. Proc Natl Acad Sci USA 100:6186-6191.
23. Flores CM, Rogers SW, Pabreza LA, Wolfe BB, Kellar KJ (1996) Neuronal nicotinic receptor expression in sensory neurons of the rat trigeminal ganglion: Demonstration of α3β4, a novel subtype in the mammalian nervous system. J Neurosci 16:7892-7901.
24. 2+ dependence of the α4β2 acetylcholine response. J Physiol (London) 550:11-24.
25. Steinlein OK, et al. (1997) Neuronal nicotinic acetylcholine receptor α4 subunit (CHRNA4) and panic disorder: An association study. Am J Med Genet 74:199-201.
26. Feng Y, et al. (2004) A common haplotype of the nicotine acetylcholine receptor α4 subunit gene is associated with vulnerability to nicotine addiction in men. Am J Hum Genet 75:112-121.
27. Greenwood PM, Fossella JA, Parasuraman R (2005) Specificity of the effect of a nicotinic receptor polymorphism on individual differences in visuospatial attention. J Cognit Neurosci 17:1611-1620.
28. Parasuraman R, Greenwood PM, Kumar R, Fossella J (2005) Beyond heritability: Neurotransmitter genes differentially modulate visuospatial attention and working memory. Psychol Sci 16:200-207.
29. Posner MI, Snyder CR, Davidson BJ (1980) Attention and the detection of signals. J Exp Psychol 109:160-174.
30. Eriksen CW, St James JD (1986) Visual attention within and around the field of focal attention: A zoom lens model. Percept Psychophys 40:225-240.
31. Winterer G, et al. (2007) Association of attentional network function with exon 5 variations of the CHRNA4 gene. Hum Mol Genet 16:2165-2174.
32. 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.
33. Rypma B, et al. (2006) Neural correlates of cognitive efficiency. NeuroImage 33:969-979.
34. Dick DM, et al. (2006) Linkage analyses of IQ in the collaborative study on the genetics of alcoholism (COGA) sample. Behav Genet 36:77-86.
35. Dick DM, et al. (2007) Association of CHRM2 with IQ: Converging evidence for a gene influencing intelligence. Behav Genet 37:265-272.
36. Luciano M, et al. (2006) Genomewide scan of IQ finds significant linkage to a quantitative trait locus on 2q. Behav Genet 36:45-55.
37. Comings DE, et al. (2002) Association of the muscarinic cholinergic 2 receptor (CHRM2) gene with major depression in women. Am J Med Genet 114:527-529.
38. Comings DE, et al. (2003) Role of the cholinergic muscarinic 2 receptor (CHRM2) gene in cognition. Mol Psychiatry 8:10-11.
39. Jones KA, et al. (2004) Linkage and linkage disequilibrium of evoked EEG oscillations with CHRM2 receptor gene polymorphisms: Implications for human brain dynamics and cognition. Int J Psychophysiol 53:75-90.
40. Greenwood PM, Parasuraman R (1999) Scale of attentional focus in visual search. Percept Psychophys 61:837-859.
41. Greenwood PM, Parasuraman R (2004) The scaling of spatial attention in visual search and its modification in healthy aging. Percept Psychophys 66:3-22.
42. Brazhnik E, Borgnis R, Muller RU, Fox SE (2004) The effects on place cells of local scopolamine dialysis are mimicked by amixture of two specific muscarinic antagonists. J Neurosci 24:9313-9323.
43. Fan J, et al. (2002)Testing the efficiency and independence of attentional networks. J Cognit Neurosci 14:340-347.
44. Voytko ML (1996) Cognitive functions of the basal forebrain cholinergic system in monkeys: Memory or attention? Behav Brain Res 75:13-25.
45. Dunnett SB, Rogers DC, Jones GH (1989) Effects of nucleus basalis magnocellularis lesions in rats on delayed matching and nonmatching to position tasks. Eur J Neurosci 1:395-406.
46. Robbins TW, et al. (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.
47. Levin ED (2002) Nicotinic receptor subtypes and cognitive function. J Neurobiol 53:633-640.
48. Chudasama Y, et al. (2004) Cholinergic modulation of visual attention and working memory: Dissociable effects of basal forebrain 192-IgG-saporin lesions and intraprefrontal infusions of scopolamine. Learn Mem 11:78-86.
49. Greenwood PM, et al. (2009) Both a nicotinic SNP and a noradrenergic SNP modulate working memory performance when attention is manipulated. J Cognit Neurosci, in press.
50. Bertrand D (2002) Neuronal nicotinic acetylcholine receptors and epilepsy. Epilepsy Curr 2:191-193.
51. Kimchi-Sarfaty C, et al. (2007) A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science 315:525-528.
52. Haier RJ, et al. (1992) Regional glucose metabolic changes after learning a complex visuospatial/motor task: A positron emission tomographic study. Brain Res 570:134-143.
53. Espeseth T, et al. (2006) Interactive effects of APOE and CHRNA4 on attention and white matter volume in healthy middle-aged and older adults. Cognit Affect Behav Neurosci 6:31-43.
54. Voytko ML, et al. (1994) Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J Neurosci 14:167-186.
55. Hasselmo M (2005) Expecting the unexpected: Modeling of neuromodulation. Neuron 46:526-528.
56. Parasuraman R, Greenwood PM, Haxby JV, Grady CL (1992) Visuospatial attention in dementia of the Alzheimer type. Brain 115:711-733.
57. Hasselmo ME, Cekic M (1996) Suppression of synaptic transmission may allow combination of associative feedback and self-organizing feed-forward connections in the neocortex. Behav Brain Res 79:153-161.
58. Gil Z, Connors BW, Amitai Y (1997) Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679-686.
59. Zhang W, et al. (2002) Characterization of central inhibitory muscarinic autoreceptors by the use of muscarinic acetylcholine receptor knockout mice. J Neurosci 22:1709-1717.
60. Mrzljak L, Levey AI, Belcher S, Goldman-Rakic PS (1998) Localization of the m2 muscarinic acetylcholine receptor protein and mRNA in cortical neurons of the normal and cholinergically deafferented rhesus monkey. J Comp Neurol 390:112-132.
61. Rouse ST, Gilmor ML, Levey AI (1998) Differential presynaptic and postsynaptic expression of m1-m4 muscarinic acetylcholine receptors at the perforant pathway/granule cell synapse. Neuroscience 86:221-232.
62. Alcantara AA, et al. (2001) Muscarinic m1 and m2 receptor proteins in local circuit and projection neurons of the primate striatum: Anatomical evidence for cholinergic modulation of glutamatergic prefronto-striatal pathways. J Comp Neurol 434:445-460.
63. Parikh V, et al. (2004) Rapid assessment of in vivo cholinergic transmission by amperometric detection of changes in extracellular choline levels. Eur J Neurosci 20:1545-1554.
64. Briand LA, et al. (2007) Modulators in concert for cognition: Modulator interactions in the prefrontal cortex. Prog Neurobiol 83:69-91.
65. Alkondon M, Pereira EF, Eisenberg HM, Albuquerque EX (2000) Nicotinic receptor activation in human cerebral cortical interneurons: A mechanism for inhibition and disinhibition of neuronal networks. J Neurosci 20:66-75.
66. Wechsler D (1981) Wechsler Adult Intelligence Scale-Revised Manual (Psychological Corporation, New York).
67. Wechsler D (1987) Wechsler Memory Scale- Revised Manual (Psychological Corporation, New York).
68. Greenwood PM, 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.