Developmental sex differences in nicotinic currents of prefrontal layer VI neurons in mice and rats

PLoS ONE

Volumn 5, Issue 2, 2010, Pages

  Alves, Nyresa C ^a   Bailey, Craig D C ^a   Nashmi, Raad ^b   Lambe, Evelyn K ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CARBACHOL; MUSCARINIC RECEPTOR; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA4; NICOTINIC RECEPTOR ALPHA4BETA2; NICOTINIC ACETYLCHOLINE RECEPTOR ALPHA4 SUBUNIT; NICOTINIC AGENT; PHOTOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; BRAIN SLICE; CONTROLLED STUDY; FEMALE; LIMBIC CORTEX; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; POSTNATAL DEVELOPMENT; PREFRONTAL CORTEX; RAT; SCISEARCH; SEX DIFFERENCE; ANIMAL; C57BL MOUSE; CELL MEMBRANE POTENTIAL; CYTOLOGY; DRUG EFFECT; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; NERVE CELL; PATCH CLAMP; PHYSIOLOGY; SPECIES DIFFERENCE; SPRAGUE DAWLEY RAT; TIME;

MUS; RATTUS; RODENTIA;

ACETYLCHOLINE; ANIMALS; CARBACHOL; FEMALE; IMMUNOHISTOCHEMISTRY; LUMINESCENT PROTEINS; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; NEURONS; NICOTINE; NICOTINIC AGONISTS; PATCH-CLAMP TECHNIQUES; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC; SEX FACTORS; SPECIES SPECIFICITY; TIME FACTORS;

EID: 77949526459     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009261     Document Type: Article

References (57)

1. Brown RT, Freeman WS, Perrin JM, Stein MT, Amler RW, et al. (2001) Prevalence and assessment of attention-deficit/hyperactivity disorder in primary care settings. Pediatrics 107: E43.
2. Cuffe SP, Moore CG, McKeown RE (2005) Prevalence and correlates of ADHD symptoms in the national health interview survey. Journal of attention disorders 9: 392-401.
3. Smalley SL, McGough JJ, Moilanen IK, Loo SK, Taanila A, et al. (2007) Prevalence and psychiatric comorbidity of attention-deficit/hyperactivity disorder in an adolescent Finnish population. Journal of the American Academy of Child and Adolescent Psychiatry 46: 1575-1583.
4. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP, et al. (2007) Attentiondeficit/ hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci USA 104: 19649-19654.
5. Sullivan RM, Brake WG (2003) What the rodent prefrontal cortex can teach us about attention-deficit/hyperactivity disorder: the critical role of early developmental events on prefrontal function. Behav Brain Res 146: 43-55.
6. Krain AL, Castellanos FX (2006) Brain development and ADHD. Clinical psychology review 26: 433-444.
7. Fassbender C, Zhang H, Buzy WM, Cortes CR, Mizuiri D, et al. (2009) A lack of default network suppression is linked to increased distractibility in ADHD. Brain Res 1273: 114-128.
8. Sherman SM (2006) The neural substrates of cognition. Trends Neurosci 29: 295-297.
9. Kassam SM, Herman PM, Goodfellow NM, Alves NC, Lambe EK (2008) Developmental excitation of corticothalamic neurons by nicotinic acetylcholine receptors. Journal of Neuroscience 28: 8756-8764.
10. Romijn HJ, Hofman MA, Gramsbergen A (1991) At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum Dev 26: 61-67.
11. Watson RE, Desesso JM, Hurtt ME, Cappon GD (2006) Postnatal growth and morphological development of the brain: a species comparison. Birth Defects Res B Dev Reprod Toxicol 77: 471-484.
12. Ernst M, Moolchan ET, Robinson ML (2001) Behavioral and neural consequences of prenatal exposure to nicotine. Journal of the American Academy of Child and Adolescent Psychiatry 40: 630-641.
13. Langley K, Rice F, van den Bree MB, Thapar A (2005) Maternal smoking during pregnancy as an environmental risk factor for attention deficit hyperactivity disorder behaviour. A review. Minerva Pediatr 57: 359-371.
14. Jacobsen LK, Slotkin TA, Mencl WE, Frost SJ, Pugh KR (2007) Gender-specific effects of prenatal and adolescent exposure to tobacco smoke on auditory and visual attention. Neuropsychopharmacology 32: 2453-2464.
15. 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.
16. Todd RD, Lobos EA, Sun LW, Neuman RJ (2003) Mutational analysis of the nicotinic acetylcholine receptor alpha 4 subunit gene in attention deficit/hyperactivity disorder: evidence for association of an intronic polymorphism with attention problems. Mol Psychiatry 8: 103-108.
17. Rigbi A, Kanyas K, Yakir A, Greenbaum L, Pollak Y, et al. (2008) Why do young women smoke? V. Role of direct and interactive effects of nicotinic cholinergic receptor gene variation on neurocognitive function. Genes Brain Behav 7: 164-172.
18. Hatchell PC, Collins AC (1980) The influence of genotype and sex on behavioral sensitivity to nicotine in mice. Psychopharmacology 71: 45-49.
19. Kyerematen GA, Owens GF, Chattopadhyay B, deBethizy JD, Vesell ES (1988) Sexual dimorphism of nicotine metabolism and distribution in the rat. Studies in vivo and in vitro. Drug Metab Dispos 16: 823-828.
20. Paxinos G, J. Franklin K B (2001) The mouse brain in stereotaxic coordinates. Academic Press, San Diego USA.
21. Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, et al. (2007) Chronic nicotine cell specifically upregulates functional alpha 4* nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path. Journal of Neuroscience 27: 8202-8218.
22. Matamales M, Bertran-Gonzalez J, Salomon L, Degos B, Deniau JM, Valjent E, Hervé D, Girault JA (2009) Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice. PLoS ONE 4: e4770.
23. Kristt DA (1991) Organization and development of the cingulum: laminar arrangement of acetylcholinesterase-rich components in rat. Brain Res Bull 26: 789-798.
24. Das A, Dikshit M, Nath C (2001) Profile of acetylcholinesterase in brain areas of male and female rats of adult and old age. Life Sci 68: 1545-1555.
25. Henningfield JE, Stapleton JM, Benowitz NL, Grayson RF, London ED (1993) Higher levels of nicotine in arterial than in venous blood after cigarette smoking. Drug and alcohol dependence 33: 23-29.
26. Lambers DS, Clark KE (1996) The maternal and fetal physiologic effects of nicotine. Semin Perinatol 20: 115-126.
27. Gaimarri A, Moretti M, Riganti L, Zanardi A, Clementi F, et al. (2007) Regulation of neuronal nicotinic receptor traffic and expression. Brain research reviews 55: 134-143.
28. Shacka JJ, Robinson SE (1998) Postnatal developmental regulation of neuronal nicotinic receptor subunit alpha 7 and multiple alpha 4 and beta 2 mRNA species in the rat. Brain Res Dev Brain Res 109: 67-75.
29. Azam L, Chen Y, Leslie FM (2007) Developmental regulation of nicotinic acetylcholine receptors within midbrain dopamine neurons. Neuroscience 144: 1347-1360.
30. Winzer-Serhan U, Leslie F (2005) Expression of alpha5 nicotinic acetylcholine receptor subunit mRNA during hippocampal and cortical development. J Comp Neurol 481: 19-30.
31. Sallette J, Pons S, Devillers-Thiery A, Soudant M, Prado de Carvalho L, et al. (2005) Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 46: 595-607.
32. Jeanclos EM, Lin L, Treuil MW, Rao J, DeCoster MA, et al. (2001) The chaperone protein 14-3-3eta interacts with the nicotinic acetylcholine receptor alpha 4 subunit. Evidence for a dynamic role in subunit stabilization. J Biol Chem 276: 28281-28290.
33. Chen XQ, Liu S, Qin LY, Wang CR, Fung YW, et al. (2005) Selective regulation of 14-3-3eta in primary culture of cerebral cortical neurons and astrocytes during development. J Neurosci Res 79: 114-118.
34. Rezvani K, Teng Y, De Biasi M (2009) The Ubiquitin-Proteasome System Regulates the Stability of Neuronal Nicotinic Acetylcholine Receptors. J Mol Neurosci.
35. Bertrand D, Valera S, Bertrand S, Ballivet M, Rungger D (1991) Steroids inhibit nicotinic acetylcholine receptors. Neuroreport 2: 277-280.
36. Valera S, Ballivet M, Bertrand D (1992) Progesterone modulates a neuronal nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 89: 9949-9953.
37. Kohchi C, Ukena K, Tsutsui K (1998) Age- and region-specific expressions of the messenger RNAs encoding for steroidogenic enzymes p450scc, P450c17 and 3beta-HSD in the postnatal rat brain. Brain Res 801: 233-238.
38. Zwain IH, Yen SS (1999) Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 140: 3843-3852.
39. Shughrue PJ, Sar M, Stumpf WE (1992) Progestin target cell distribution in forebrain and midbrain regions of the 8-day postnatal mouse brain. Endocrinology 130: 3650-3659.
40. Shughrue PJ, Stumpf WE, Elger W, Schulze PE, Sar M (1991) Progestin receptor cells in mouse cerebral cortex during early postnatal development: a comparison with preoptic area and central hypothalamus using autoradiography with [125I]progestin. Brain Res Dev Brain Res 59: 143-155.
41. Kato J, Onouchi T, Okinaga S, Takamatsu M (1984) The ontogeny of cytosol and nuclear progestin receptors in male rat brain and its male-female differences. J Steroid Biochem 20: 147-152.
42. Nishimura A, Hohmann CF, Johnston MV, Blue ME (2002) Neonatal electrolytic lesions of the basal forebrain stunt plasticity in mouse barrel field cortex. Int J Dev Neurosci 20: 481-489.
43. Kuczewski N, Aztiria E, Leanza G, Domenici L (2005) Selective cholinergic immunolesioning affects synaptic plasticity in developing visual cortex. Eur J Neurosci 21: 1807-1814.
44. Robertson RT, Gallardo KA, Claytor KJ, Ha DH, Ku KH, et al. (1998) Neonatal treatment with 192 IgG-saporin produces long-term forebrain cholinergic deficits and reduces dendritic branching and spine density of neocortical pyramidal neurons. Cereb Cortex 8: 142-155.
45. Sherren N, Pappas BA (2005) Selective acetylcholine and dopamine lesions in neonatal rats produce distinct patterns of cortical dendritic atrophy in adulthood. Neuroscience 136: 445-456.
46. Couey JJ, Meredith RM, Spijker S, Poorthuis RB, Smit AB, et al. (2007) Distributed network actions by nicotine increase the threshold for spike-timingdependent plasticity in prefrontal cortex. Neuron 54: 73-87.
47. Zhang L, Jones EG (2004) Corticothalamic inhibition in the thalamic reticular nucleus. J Neurophysiol 91: 759-766.
48. Zikopoulos B, Barbas H (2006) Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. Journal of Neuroscience 26: 7348-61.
49. Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492: 145-77.
50. King SL, Marks MJ, Grady SR, Caldarone BJ, Koren AO, et al. (2003) Conditional expression in corticothalamic efferents reveals a developmental role for nicotinic acetylcholine receptors in modulation of passive avoidance behavior. Journal of Neuroscience 23: 3837-3843.
51. Heath CJ, Picciotto MR (2009) Nicotine-induced plasticity during development: modulation of the cholinergic system and long-term consequences for circuits involved in attention and sensory processing. Neuropharmacology 56 Suppl 1: 254-262.
52. Tun PA, Lachman ME (2008) Age differences in reaction time and attention in a national telephone sample of adults: education, sex, and task complexity matter. Developmental psychology 44: 1421-1429.
53. Schmitz M, Denardin D, Laufer Silva T, Pianca T, Hutz MH, et al. (2006) Smoking during pregnancy and attention-deficit/hyperactivity disorder, predominantly inattentive type: a case-control study. Journal of the American Academy of Child and Adolescent Psychiatry 45: 1338-1345.
54. Fung YK, Lau YS (1989) Effects of prenatal nicotine exposure on rat striatal dopaminergic and nicotinic systems. Pharmacol Biochem Behav 33: 1-6.
55. Ribary U, Lichtensteiger W (1989) Effects of acute and chronic prenatal nicotine treatment on central catecholamine systems of male and female rat fetuses and offspring. J Pharmacol Exp Ther 248: 786-792.
56. Gan WQ, Cohen SB, Man SF, Sin DD (2008) Sex-related differences in serum cotinine concentrations in daily cigarette smokers. Nicotine Tob Res 10: 1293-1300.
57. Rosecrans JA, Schechter MD (1972) Brain area nicotine levels in male and female rats of two strains. Archives internationales de pharmacodynamie et de thérapie 196: 46-54.