Cited by 25

The DOI matches its Crossref record; 11 of the 11 references it cites were found in a registry or an index.

Cellular and Molecular Changes in Hippocampal Glutamate Signaling and Alterations in Learning, Attention, and Impulsivity Following Prenatal Nicotine Exposure

Polli, Filip S., Ipsen, Theis H., Caballero-Puntiverio, Maitane, Østerbøg, Tina Becher, Aznar, Susana, Andreasen, Jesper T., Kohlmeier, Kristi A.·2020·Molecular Neurobiology

Abstract

Over 70 million European pregnant women are smokers during their child-bearing years. Consumption of tobacco-containing products during pregnancy is associated with several negative behavioral outcomes for the offspring, including a higher susceptibility for the development of attention-deficit/hyperactive disorder (ADHD). In efforts to minimize fetal exposure to tobacco smoke, many women around the world switch to nicotine replacement therapies (NRTs) during the gestational period; however, prenatal nicotine exposure (PNE) in any form has been associated with alterations in cognitive processes, including learning, memory, and attention. These processes are controlled by glutamatergic signaling of hippocampal pyramidal neurons within the CA1 region, suggesting actions of nicotine on glutamatergic transmission in this region if present prenatally. Accordingly, we aimed to investigate hippocampal glutamatergic function following PNE treatment in NMRI mice employing molecular, cellular electrophysiology, and pharmacological approaches, as well as to evaluate cognition in the rodent continuous performance task (rCPT), a recently developed mouse task allowing assessment of learning, attention, and impulsivity. PNE induced increases in the expression levels of mRNA coding for different glutamate receptors and subunits within the hippocampus. Functional alterations in AMPA and NMDA receptors on CA1 pyramidal neurons of PNE mice were suggestive of higher GluA2-lacking and lower GluN2…

Overview

Integrity signals

Registry

Crossref · 10.1007/s12035-019-01854-9

Cites

11 of 11 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Show all 11 references

Research works printed but not linked: 118

  1. Fidler JA, West R (2009) Self-perceived smoking motives and their correlates in a general population sample. Nicotine Tob Res 11:1182–1188. https://doi.org/10.1093/ntr/ntp120 · DOI · Paper page
  2. Leventhal AM, Waters AJ, Boyd S, Moolchan ET, Lerman C, Pickworth WB (2007) Gender differences in acute tobacco withdrawal: effects on subjective , cognitive , and physiological measures. Exp Clin Psychopharmacol 15:21–36. https://doi.org/10.1037/1064-1297.15.1.21 · DOI
  3. Sieminska A, Jassem E (2014) The many faces of tobacco use among women. Med Sci Monit 20:153–162. https://doi.org/10.12659/MSM.889796 · DOI
  4. Royce JM, Corbett K, Sorensen G, Ockene J (1997) Gender, social pressure, and smoking cessations: the community intervention trial for smoking cessation (COMMIT) at baseline. Soc Sci Med 44:359–370 · DOI
  5. Benowitz NL, Lessov-Schlaggar CN, Swan GE, Jacob P (2006) Female sex and oral contraceptive use accelerate nicotine metabolism. Clin Pharmacol Ther 79:480–488. https://doi.org/10.1016/j.clpt.2006.01.008 · DOI · Paper page
  6. Tanner J-A (2015) The neurobiology and genetics of nicotine and tobacco. Springer
  7. Biederman J, Martelon M, Woodworth KY, Spencer TJ, Faraone SV (2017) Is maternal smoking during pregnancy a risk factor for cigarette smoking in offspring? A longitudinal controlled study of ADHD children grown up. J Atten Disord 21:975–985. https://doi.org/10.1177/1087054714557357 · DOI · Paper page
  8. Motlagh MG, Sukhodolsky DG, Landeros-weisenberger A et al (2011) Adverse effects of heavy prenatal maternal smoking on attentional control in children with ADHD. J Atten Disord 15:593–603. https://doi.org/10.1177/1087054710374576 · DOI · Paper page
  9. Schwenke E, Fasching PA, Faschingbauer F, Pretscher J, Kehl S, Peretz R, Keller A, Häberle L et al (2018) Predicting attention deficit hyperactivity disorder using pregnancy and birth characteristics. Arch Gynecol Obstet 298:889–895. https://doi.org/10.1007/s00404-018-4888-0 · DOI · Paper page
  10. Thakur GA, Sc B, Sengupta SM et al (2013) Maternal smoking during pregnancy and ADHD : a comprehensive clinical and neurocognitive characterization. Nicotine Tob Res 15:149–157. https://doi.org/10.1093/ntr/nts102 · DOI
  11. Ko T, Tsai L, Chu L, Yeh SJ, Leung C, Chen CY, Chou HC, Tsao PN et al (2014) Parental smoking during pregnancy and its association with low birth weight, small for gestational age, and preterm birth offspring: a birth cohort study. Pediatr Neonatol 55:20–27. https://doi.org/10.1016/j.pedneo.2013.05.005 · DOI
  12. Rogers JM (2009) Tobacco and pregnancy. Reprod Toxicol 28:152–160. https://doi.org/10.1016/j.reprotox.2009.03.012 · DOI
  13. Taylor JA, Sanderson M (1995) A reexamination of the risk factors for the sudden infant death syndrome. J Pediatr 126:887–891 · DOI
  14. Luck W, Nau H (1985) Nicotine and cotinine concentrations in serum and urine of infants exposed via passive smoking or milk from smoking mothers. J Pediatr 107:816–820 · DOI
  15. Alkam T, Kim H, Mamiya T et al (2013) Evaluation of cognitive behaviors in young offspring of C57BL / 6J mice after gestational nicotine exposure during different time-windows. Psychopharmacology 230:451–463. https://doi.org/10.1007/s00213-013-3175-9 · DOI
  16. Zhu J, Fan F, Mccarthy DM et al (2017) A prenatal nicotine exposure mouse model of methylphenidate responsive ADHD-associated cognitive phenotypes. Int J Dev Neurosci 58:26–34. https://doi.org/10.1016/j.ijdevneu.2017.01.014 · DOI · Paper page
  17. Zhang L, Spencer TJ, Biederman J, Bhide PG (2018) Attention and working memory deficits in a perinatal nicotine exposure mouse model. PLoS One 13:1–20. https://doi.org/10.1371/journal.pone.0198064 · DOI
  18. Roy TS, Sabherwal U (1998) Effects of gestational nicotine exposure on hippocampal morphology. Neurotoxicol Teratol 20:465–473. https://doi.org/10.1016/S0892-0362(97)00137-2 · DOI
  19. Roy TS, Seidler FJ, Slotkin TA (2002) Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J Pharmacol Exp Ther 300:124–133 · DOI
  20. Parameshwaran K, Buabeid MA, Karuppagounder SS (2012) Developmental nicotine exposure induced alterations in behavior and glutamate receptor function in hippocampus. Cell Mol Life Sci 69:829–841. https://doi.org/10.1007/s00018-011-0805-4 · DOI
  21. Vaglenova J, Parameshwaran K, Suppiramaniam V, Breese CR, Pandiella N, Birru S (2008) Long-lasting teratogenic effects of nicotine on cognition: gender specificity and role of AMPA receptor function. Neurobiol Learn Mem 90:527–536. https://doi.org/10.1016/j.nlm.2008.06.009 · DOI
  22. Jaiswal SJ, Pilarski JQ, Harrison CM, Fregosi RF (2013) Developmental nicotine exposure alters AMPA neurotransmission in the hypoglossal motor nucleus and pre-Botzinger complex of neonatal rats. J Neurosci 33:2616–2625. https://doi.org/10.1523/JNEUROSCI.3711-12.2013 · DOI
  23. Pilarski JQ, Wakefield HE, Fuglevand AJ, Levine RB, Fregosi RF (2011) Developmental nicotine exposure alters neurotransmission and excitability in hypoglossal motoneurons. J Neurophysiol 105:423–433. https://doi.org/10.1152/jn.00876.2010 · DOI
  24. Wang H, Dávila-García MI, Yarl W, Gondré-Lewis MC (2011) Gestational nicotine exposure regulates expression of AMPA and NMDA receptors and their signaling apparatus in developing and adult rat hippocampus. Neuroscience 188:168–181. https://doi.org/10.1016/j.neuroscience.2011.04.069 · DOI
  25. Ferbinteanu J, Kennedy PJ, Shapiro ML (2006) Episodic memory — from brain to mind. Hippocampus 16:691–703. https://doi.org/10.1002/hipo · DOI
  26. Smith DM, Mizumori SJY (2006) Hippocampal place cells, context, and episodic memory. Hippocampus 16:716–729. https://doi.org/10.1002/hipo · DOI
  27. Muzzio IA, Levita L, Kulkarni J, Monaco J, Kentros C, Stead M, Abbott LF, Kandel ER (2009) Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus. PLoS Biol 7:e1000140. https://doi.org/10.1371/journal.pbio.1000140 · DOI
  28. Stopford CL, Thompson JC, Neary D, Richardson AM, Snowden JS (2010) Working memory, attention, and executive function in Alzheimer’s disease and frontotemporal dementia. Cortex 48:429–446. https://doi.org/10.1016/j.cortex.2010.12.002 · DOI
  29. Perry RJ, Hodges JR (1999) Attention and executive deficits in Alzheimer’s disease: a critical review. Brain 122:383–404 · DOI
  30. Riccio CA, Reynolds CR, Lowe P, Moore JJ (2002) The continuous performance test: a window on the neural substrates for attention? Arch Clin Neurophysiol 17:235–272
  31. Riccio CA, Waldrop JJM, Reynolds CR, Lowe P (2001) Effects of stimulants on the continuous performance test ( CPT ): implications for CPT use and interpretation. J Neuropsychiatry Clin Neurosci 13:326–335 · DOI
  32. Kim CH, Hvoslef-eide M, Nilsson SRO et al (2015) The continuous performance test ( rCPT ) for mice : a novel operant touchscreen test of attentional function. Psychopharmacology 232:3947–3966. https://doi.org/10.1007/s00213-015-4081-0 · DOI
  33. Caballero-Puntiverio M, Lerdrup LS, Grupe M et al (2019) Effect of ADHD medication in male C57BL / 6J mice performing the rodent continuous performance test. Psychopharmacology. https://doi.org/10.1007/s00213-019-5167-x · DOI
  34. Schneider T, Ilott N, Brolese G, Bizarro L, Asherson PJ, Stolerman IP (2011) Prenatal exposure to nicotine impairs performance of the 5-choice serial reaction time task in adult rats. Neuropsychopharmacology 36:1114–1125. https://doi.org/10.1038/npp.2010.249 · DOI · Paper page
  35. Schneider T, Bizarro L, Asherson PJE, Stolerman IP (2012) Hyperactivity, increased nicotine consumption and impaired performance in the five-choice serial reaction time task in adolescent rats prenatally exposed to nicotine. Psychopharmacology 223:401–415. https://doi.org/10.1007/s00213-012-2728-7 · DOI
  36. Green D, Swets J (1966) Signal detection theory and psychophysics. Wiley, New York
  37. Polli FS, Kohlmeier KA (2018) Prenatal nicotine exposure alters postsynaptic AMPA receptors and glutamate neurotransmission within the laterodorsal tegmentum ( LDT ) of juvenile mice. Neuropharmacology 137:71–85. https://doi.org/10.1016/j.neuropharm.2018.04.024 · DOI
  38. Ipsen TH, Polli FS, Kohlmeier KA (2018) Calcium rises induced by AMPA and nicotine receptors in the ventral tegmental area show differences in mouse brain slices prenatally exposed to nicotine. Dev Neurobiol 78:1–21. https://doi.org/10.1002/dneu.22607 · DOI
  39. Polli FS, Kohlmeier KA (2019) Alterations in NMDAR-mediated signaling within the laterodorsal tegmental nucleus are associated with prenatal nicotine exposure. Neuropharmacology:158. https://doi.org/10.1016/j.neuropharm.2019.107744 · DOI
  40. Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG (2002) Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet 32:435–443 · DOI
  41. Peacock JL, Cook DG, Carey IM, Jarvis MJ, Bryant AE, Anderson HR, Bland JM (1998) Maternal cotinine level during pregnancy and birthweight for gestational age. Int J Epidemiol 27:647–656 · DOI
  42. Christensen MH, Nielsen ML, Kohlmeier KA (2015) Electrophysiological changes in laterodorsal tegmental neurons associated with prenatal nicotine exposure: Implications for heightened susceptibility to addict to drugs of abuse. J Dev Orig Health Dis 6:182–200. https://doi.org/10.1017/S204017441400049X · DOI · Paper page
  43. Lipton JW, Robie HC, Ling Z, Weese-Mayer DE, Carvey PM (1998) The magnitude of brain dopamine depletion from prenatal cocaine exposure is a function of uterine position. Neurotoxicol Teratol 20:373–382 · DOI
  44. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:45e–45e. https://doi.org/10.1093/nar/29.9.e45 · DOI · Paper page
  45. Neher E (1992) Correction for liquid junction potentials in pathc clamp experiments. Methods Enzymol 207:123–131. https://doi.org/10.1016/0076-6879(92)07008-C · DOI · Paper page
  46. Koike M, Iino M, Ozawa S (1997) Blocking effect of 1-naphthyl acetyl spermine on Ca+2-permeable AMPA receptors in cultured rat hippocampal neurons. Neurosci Res 29:27–36 · DOI
  47. Tsubokawa H, Oguro K, Masuzawa T, Nakaima T, Kawai N (1995) Effects of a spider toxin and its analogue on glutamate-activated currents in the hippocampal CA1 neuron after ischemia. J Neurophysiol 74:218–225 · DOI
  48. Lind GE, Mou TC, Tamborini L, Pomper MG, de Micheli C, Conti P, Pinto A, Hansen KB (2017) Structural basis of subunit selectivity for competitive NMDA receptor antagonists with preference for GluN2A over GluN2B subunits. Proc Natl Acad Sci U S A 114:E6942–E6951. https://doi.org/10.1073/pnas.1707752114 · DOI
  49. Wei X, Nishi T, Kondou S, Kimura H, Mody I (2019) Preferential enhancement of GluN2B-containing native NMDA receptors by the endogenous modulator 24S-hydroxycholesterol in hippocampal neurons. Neuropharmacology 148:11–20. https://doi.org/10.1016/j.neuropharm.2018.12.028 · DOI
  50. Aroniadou-Anderjaska V, Pidoplichko VI, Figueiredo TH, Braga MFM (2018) Oscillatory synchronous inhibition in the basolateral amygdala and its primary dependence on NR2A-containing NMDA receptors. Neuroscience 373:145–158. https://doi.org/10.1016/j.neuroscience.2018.01.021 · DOI
  51. Wu LJ, Xu H, Ren M, Cao X, Zhuo M (2007) Pharmacological isolation of postsynaptic currents mediated by NR2A- and NR2B-containing NMDA receptors in the anterior cingulate cortex. Mol Pain 3:1–6. https://doi.org/10.1186/1744-8069-3-11 · DOI
  52. Williams K (1993) Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44:851–859
  53. Tovar KR, Westbrook GL (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19:4180–4188 · DOI
  54. Tovar KR, Westbrook GL (2012) Amino-terminal ligands prolong NMDA receptor- mediated EPSCs. J Neurosci 32:8065–8073. https://doi.org/10.1523/JNEUROSCI.0538-12.2012 · DOI
  55. Eyo UB, Bispo A, Liu J, Sabu S, Wu R, DiBona VL, Zheng J, Murugan M et al (2018) The GluN2A subunit regulates neuronal NMDA receptor-induced microglia-neuron physical interactions. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-018-19205-4 · DOI
  56. Rosahl TW, Wingrove PB, Hunt V, Fradley RL, Lawrence JM, Heavens RP, Treacey P, Usala M et al (2006) A genetically modified mouse model probing the selective action of ifenprodil at the N-methyl-d-aspartate type 2B receptor. Mol Cell Neurosci 33:47–56. https://doi.org/10.1016/j.mcn.2006.06.006 · DOI
  57. Sanz-Clemente A, Matta JA, Isaac JTR, Roche KW (2010) Casein kinase 2 regulates the NR2 subunit composition of synaptic NMDA receptors. Neuron 67:984–996. https://doi.org/10.1016/j.neuron.2010.08.011 · DOI
  58. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304:1021–1024. https://doi.org/10.1126/science.1096615 · DOI
  59. Heeger D (1997) Signal detection theory:1–10. https://doi.org/10.1007/s00221-011-2557-7 · DOI
  60. Medin T, Jensen V, Skare Ø, Storm-Mathisen J, Hvalby Ø, Bergersen LH (2019) Altered α -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid ( AMPA ) receptor function and expression in hippocampus in a rat model of attention-deficit/hyperactivity disorder (ADHD). Behav Brain Res 360:209–215. https://doi.org/10.1016/j.bbr.2018.12.028 · DOI · Paper page
  61. Collingridge BYGL, Kehl SJ, Mclennan H (1983) Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334:33–46 · DOI · Paper page
  62. Jensen V, Rinholm JE, Johansen TJ, Medin T, Storm-Mathisen J, Sagvolden T, Hvalby O, Bergersen LH (2009) N-methyl-d-aspartate receptor subunit dysfunction at hippocampal glutamatergic synapses in an animal model of attention-deficit/hyperactivity disorder. Neuroscience 158:353–364. https://doi.org/10.1016/j.neuroscience.2008.05.016 · DOI
  63. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A et al (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17:7503–7522 · DOI · Paper page
  64. Poncer JC, Mckinney RA, Gähwiler BH, Thompson SM (2000) Differential control of GABA release at synapses from distinct interneurons in rat hippocampus. J Physiol 528:123–130 · DOI · Paper page
  65. Dietrich D, Kral T, Clusmann H, Friedl M, Schramm J (2002) Presynaptic group II metabotropic glutamate receptors reduce stimulated and spontaneous transmitter release in human dentate gyrus. Neuropharmacology 42:297–305 · DOI
  66. Losonczy A, Somogyi P, Nusser Z (2003) Reduction of excitatory postsynaptic responses by persistently active metabotropic glutamate receptors in the hippocampus. J Neurophysiol 89:1910–1919 · DOI
  67. Speed HE, Dobrunz LE (2009) Developmental changes in short-term facilitation are opposite at temporoammonic synapses compared to Schaffer collateral synapses onto CA1 pyramidal cells. Hippocampus 19:187–204. https://doi.org/10.1002/hipo.20496.Developmental · DOI
  68. Malinow R, Malenka RC (2002) Ampa rceptor tafficking and synaptic plasticity. Annu Rev Neurosci 25:103–126. https://doi.org/10.1146/annurev.neuro.25.112701.142758 · DOI · Paper page
  69. Traynelis SF, Wollmuth LP, Mcbain CJ et al (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405–496. https://doi.org/10.1124/pr.109.002451.405 · DOI
  70. Simeone TA, Sanchez RM, Rho JM (2004) Molecular biology and ontogeny of glutamate receptors in the mammalian central nervous system. J Child Neurol 19:343–360 · DOI
  71. Pandey SP, Rai R, Gaur P, Prasad S (2015) Development- and age-related alterations in the expression of AMPA receptor subunit GluR2 and its trafficking proteins in the hippocampus of male mouse brain. Biogerontology 16:317–328. https://doi.org/10.1007/s10522-014-9548-6 · DOI
  72. Ozawa S, Kamiya H, Tsuzuki K (1998) Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54:581–618. https://doi.org/10.1016/S0301-0082(97)00085-3 · DOI
  73. Alkam T, Kim HC, Hiramatsu M, Mamiya T, Aoyama Y, Nitta A, Yamada K, Nabeshima T (2013) Evaluation of emotional behaviors in young offspring of C57BL/6J mice after gestational and/or perinatal exposure to nicotine in six different time-windows. Behav Brain Res 239:80–89. https://doi.org/10.1016/j.bbr.2012.10.058 · DOI
  74. Pauly JR, Sparks JA, Hauser KF, Pauly TH (2004) In utero nicotine exposure causes persistent, gender-dependant changes in locomotor activity and sensitivity to nicotine in C57Bl/6 mice. Int J Dev Neurosci 22:329–337. https://doi.org/10.1016/j.ijdevneu.2004.05.009 · DOI
  75. Chater TE, Goda Y (2014) The role of AMPA receptors in postsynaptic mechanisms of synaptic plasticity. Front Cell Neurosci 8:1–14. https://doi.org/10.3389/fncel.2014.00401 · DOI
  76. Swanson GT, Kamboj SK, Cull-Candy SG (1997) Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17:58–69 · DOI
  77. Maier T, Schmidt A, Guell M et al (2011) Quantification of mRNA and protein and integration with protein turnover in a bacterium. Mol Syst Biol 7:1–12. https://doi.org/10.1038/msb.2011.38 · DOI · Paper page
  78. Greenbaum D, Colangelo C, Williams K et al (2003) Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4:117.1–117.8. https://doi.org/10.1186/gb-2003-4-9-117 · DOI · Paper page
  79. Sagvolden T (2000) Behavioral validation of the spontaneously hypertensive rat ( SHR ) as an animal model of attention-deficit / hyperactivity disorder ( AD / HD ). Neurosci Biobehav Rev 24:31–39 · DOI · Paper page
  80. Cheng J, Liu A, Shi MY, Yan Z (2017) Disrupted glutamatergic transmission in prefrontal cortex contributes to behavioral abnormality in an animal model of ADHD. Neuropsychopharmacology 42:2096–2104. https://doi.org/10.1038/npp.2017.30 · DOI
  81. Kumar SS, Bacci A, Kharazia V, Huguenard JR (2002) A developmental switch of AMPA receptor subunits in neocortical pyramidal neurons. J Neurosci 22:3005–3015 · DOI
  82. Bellone C, Mameli M (2011) In utero exposure to cocaine delays postnatal synaptic maturation of glutamatergic transmission in the VTA in utero exposure to cocaine delays postnatal synaptic maturation of glutamatergic transmission in the VTA. Nat Neurosci 14:1439–1446. https://doi.org/10.1038/nn.2930 · DOI
  83. Kullmann M (1994) Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: Implications for long-term potentiation. Neuron 12:1111–1120 · DOI
  84. Xia J, Meyers AM, Beeler JA (2017) Chronic nicotine alters corticostriatal plasticity in the striatopallidal pathway mediated by NR2B-containing silent synapses. Neuropsychopharmacology 42:2314–2324. https://doi.org/10.1038/npp.2017.87 · DOI
  85. Craven KMO, Downing PE, Kanwisher N (1999) fMRI evidence for objects as the units of attentional selection. Lett Nat 401:584–587 · DOI · Paper page
  86. Summerfield JJ, Gitelman DR, Mesulam MM, Nobre AC (2006) Orienting attention based on long-term memory experience. Neuron 49:905–916. https://doi.org/10.1016/j.neuron.2006.01.021 · DOI
  87. Li X, Chen W, Pan K, Li H, Pang P, Guo Y, Shu S, Cai Y et al (2018) Serotonin receptor 2c-expressing cells in the ventral CA1 control attention via innervation of the Edinger–Westphal nucleus. Nat Neurosci 21:1239–1250. https://doi.org/10.1038/s41593-018-0207-0 · DOI
  88. Cheung THC, Cardinal RN (2005) Hippocampal lesions facilitate instrumental learning with delayed reinforcement but induce impulsive choice in rats. BMC Neurosci 6:1–24. https://doi.org/10.1186/1471-2202-6-36 · DOI
  89. Mariano TY, Bannerman DM, McHugh SB, Preston TJ, Rudebeck PH, Rudebeck SR, Rawlins JN, Walton ME et al (2009) Impulsive choice in hippocampal but not orbitofrontal cortex-lesioned rats on a nonspatial decision-making maze task. Eur J Neurosci 30:472–484. https://doi.org/10.1111/j.1460-9568.2009.06837.x · DOI
  90. Pattij T, Vanderschuren LJMJ (2008) The neuropharmacology of impulsive behaviour. Trends Pharmacol Sci 29:192–199. https://doi.org/10.1016/j.tips.2008.01.002 · DOI
  91. Collingridge GL, Volianskis A, Bannister N, France G, Hanna L, Mercier M, Tidball P, Fang G et al (2013) The NMDA receptor as a target for cognitive enhancement. Neuropharmacology 64:13–26. https://doi.org/10.1016/j.neuropharm.2012.06.051 · DOI
  92. Dorval KM, Wigg KG, Crosbie J, Tannock R, Kennedy JL, Ickowicz A, Pathare T, Malone M et al (2007) Association of the glutamate receptor subunit gene GRIN2B with attention-deficit/hyperactivity disorder. Genes Brain Behav 6:444–452. https://doi.org/10.1111/j.1601-183X.2006.00273.x · DOI
  93. Turic D, Langley K, Mills S et al (2004) Follow-up of genetic linkage findings on chromosome 16p13 : evidence of association of N -methyl- D aspartate glutamate receptor 2A gene polymorphism with ADHD. Mol Psychiatry 13:169–173. https://doi.org/10.1038/sj.mp.4001387 · DOI
  94. Lynch G, Granger R, Ambros-ingerson J et al (1997) Evidence that a positive modulator of AMPA-type glutamate receptors improves delayed recall in aged humans. Exp Neurol 145:89–92 · DOI
  95. Ingvar M, Ambros-ingerson J, Davis M et al (1997) Enhancement by an ampakine of memory encoding in humans. Exp Neurol 146:553–559 · DOI
  96. Wezenberg E, Verkes RJ, Ruigt GSF, Hulstijn W, Sabbe BG (2007) Acute effects of the ampakine farampator on memory and information processing in healthy elderly volunteers. Neuropsychopharmacology 32:1272–1283. https://doi.org/10.1038/sj.npp.1301257 · DOI
  97. Adler LA, Kroon RA, Stein M et al (2012) A translational approach to evaluate the efficacy and safety of the novel AMPA receptor positive allosteric modulator org 26576 in adult attention-deficit/ hyperactivity disorder. Biol Psychiatry 72:971–977. https://doi.org/10.1016/j.biopsych.2012.05.012 · DOI
  98. Sakimura K, Kutsuwada T, Ito I et al (1995) Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor 1 subunit. Lett Nat 373:151–155 · DOI
  99. Ng D, Pitcher GM, Szilard RK et al (2009) Neto1 is a novel CUB-domain NMDA receptor – interacting protein required for synaptic plasticity and learning. PLoS Biol 7:e1000041. https://doi.org/10.1371/journal.pbio.1000041 · DOI
  100. Dragomir A, Akay YM, Zhang D, Akay M (2017) Ventral tegmental area dopamine neurons firing model reveals prenatal nicotine induced alterations. Trans Neural Syst Rehabil Eng 25:1387–1396 · DOI
  101. Muneoka K, Ogawa T, Kamei K et al (1997) Prenatal nicotine exposure affects the development of the central serotonergic system as well as the dopaminergic system in rat offspring : involvement of route of drug administrations. Dev Brain Res 102:117–126 · DOI
  102. Slotkin TA, Skavicus S, Card J, Stadler A, Levin ED, Seidler FJ (2015) Developmental neurotoxicity of tobacco smoke directed toward cholinergic and serotonergic systems: more than just nicotine. Toxicol Sci 147:178–189. https://doi.org/10.1093/toxsci/kfv123 · DOI · Paper page
  103. Ribary U, Lichtensteiger W (1989) Effects of acute and chronic prenatal nicotine treatment central catecholamine systems of male and female rat fetuses and offspring. Pharmacol Exp Ther 248:786–792
  104. Seidler FJ, Levin ED, Lappi SE, Slotkin TA (1992) Fetal nicotine exposure ablates the ability of postnatal nicotine challenge to release norepinephrine from rat brain regions. Decelopmental Brain Res 69:288–291 · DOI
  105. Dalley JW, Robbins TW (2017) Fractionating impulsivity : neuropsychiatric implications. Nat Publ Group 18:158–171. https://doi.org/10.1038/nrn.2017.8 · DOI · Paper page
  106. Chamberlain SR, Robbins TW (2013) Noradrenergic modulation of cognition : therapeutic implications. J Psychopharmacol 27:694–718. https://doi.org/10.1177/0269881113480988 · DOI
  107. Polli F, Kohlmeier K (2019) Prenatal nicotine exposure in rodents: why are there so many behavioral outcomes? Nicotine Tob Res. https://doi.org/10.1093/ntr/ntz196 · DOI
  108. Schneider T, Bizarro L, Asherson PJE, Stolerman IP (2010) Gestational exposure to nicotine in drinking water: teratogenic effects and methodological issues. Behav Pharmacol 21:206–216. https://doi.org/10.1097/FBP.0b013e32833a5bb5 · DOI
  109. Kohlmeier KA (2015) Nicotine during pregnancy: changes induced in neurotransmission, which could heighten proclivity to addict and induce maladaptive control of attention. J Dev Orig Health Dis 6:169–181. https://doi.org/10.1017/S2040174414000531 · DOI
  110. Vaglenova J, Birru S, Pandiella NM, Breese CR (2004) An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure. Behav Brain Res 150:159–170. https://doi.org/10.1016/j.bbr.2003.07.005 · DOI · Paper page
  111. Blot S, Bai J, Kemp A, Manahan-Vaughan D, Giros B, Tzavara E, Otani S (2015) Modulation of hippocampus-prefrontal cortex synaptic transmission and disruption of excecutive function cognitive fundtions by MK-801. Cereb Cortex 25(5):1348–1361. https://doi.org/10.1093/cercor/bht329 · DOI · Paper page
  112. Levin WA, Jones JP et al (1996) Prenatal nicotine effects on memory in rats : pharmacological and behavioral challenges. Dev Brain Res 97:207–215 · DOI · Paper page
  113. Levin ED, Briggs SJ, Christopher CN, Rose JE (1993) Prenatal nicotine exposure and cognitive performance in rats. Neurotroxicol Teratol 15:251–260 · DOI · Paper page
  114. Li J, Bo L, Zhang P, Gao Q, Li L, Tang J, Wu C, Li D et al (2015) Exposure to nicotine during pregnancy and altered learning and memory in the rat offspring. Nicotine Tob Res 17:661–666. https://doi.org/10.1093/ntr/ntu178 · DOI
  115. Shacka JJ, Fennell OB, Robinson SE (1997) Prenatal nicotine sex-dependently alters agonist-induced locomotion and stereotypy. Neurotoxicol Teratol 19:467–476 · DOI
  116. Franke RM, Park M, Belluzzi JD, Leslie FM (2008) Prenatal nicotine exposure changes natural and drug-induced reinforcement in adolescent male rats. Eur J Neurosci 27:2952–2961. https://doi.org/10.1111/j.1460-9568.2008.06253.x · DOI · Paper page
  117. Balsevich G, Poon A, Goldowitz D, Wilking JA (2014) The effects of pre- and post-natal nicotine exposure and genetic background on the striatum and behavioral phenotypes in the mouse. Behav Brain Res 266:7–18. https://doi.org/10.1016/j.bbr.2014.02.038 · DOI
  118. Gurwitz D (2001) Animal models and human genome diversity: the pitfalls of inbred mice. Drug Discov Today 6:766–768 · DOI

Metadata

Authors
Polli, F. S., Ipsen, T. H., Caballero-Puntiverio, M., Østerbøg, T. B., Aznar, S., Andreasen, J. T., & Kohlmeier, K. A.
Venue
Molecular Neurobiology
Published
2020-01-08
Volume
57
Issue
4
Pages
2002-2020
ISSN
  • 0893-7648
  • 1559-1182
Cited by
25
References
11
Language
en
Funders
  • Bispebjerg-Frederiksberg Hospital research funds (000000)
  • Philip Morris International (100197)
  • Brazilian National Council of Research (201542-2014/5)
  • Drug Design and Pharmacology Department at the University of Copenhagen (00000)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review