Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on sleep in brain health

LIVE: Thursday 2nd May 2024, 18:00-19:30 (CEST)

Quality sleep is essential for health. But what happens to our brains when sleep patterns are disturbed? Join our experts to explore the interplay between sleep disruption and neurological diseases, and the questions that you need to be asking your patients to help you prevent the harmful effects of sleep deprivation.
ADVANCED SEARCH
Log in
Top
Behavioral and Brain Functions
Published in: Behavioral and Brain Functions 1/2014

Open Access 01-12-2014 | Research

Behavioral changes following PCB 153 exposure in the Spontaneously Hypertensive rat – an animal model of Attention-Deficit/Hyperactivity disorder

Authors: Espen Borgå Johansen, Frode Fonnum, Per L Lausund, S Ivar Walaas, Nora Elise Bærland, Grete Wøien, Terje Sagvolden

Published in: Behavioral and Brain Functions | Issue 1/2014

Login to get access

Abstract

Background

Attention-Deficit/Hyperactivity Disorder (ADHD) is a behavioral disorder affecting 3-5% of children. Although ADHD is highly heritable, environmental factors like exposure during early development to various toxic substances like polychlorinated biphenyls (PCBs) may contribute to the prevalence. PCBs are a group of chemical industrial compounds with adverse effects on neurobiological and cognitive functioning, and may produce behavioral impairments that share significant similarities with ADHD. The present study examined the relation between exposure to PCB 153 and changes in ADHD-like behavior in an animal model of ADHD, the spontaneously hypertensive rats (SHR/NCrl), and in Wistar Kyoto (WKY/NHsd) controls.

Methods

SHR/NCrl and WKY/NHsd, males and females, were orally given PCB 153 dissolved in corn oil at around postnatal day (PND) 8, 14, and 20 at a dosage of 1, 3 or 6 mg/kg bodyweight at each exposure. The control groups were orally administered corn oil only. The animals were behaviorally tested for exposure effects from PND 37 to 64 using an operant procedure.

Results

Exposure to PCB 153 was associated with pronounced and long-lasting behavioral changes in SHR/NCrl. Exposure effects in the SHR/NCrl depended on dose, where 1 mg/kg tended to reduce ADHD-like behaviors and produce opposite behavioral effects compared to 3 mg/kg and 6 mg/kg, especially in the females. In the WKY/NHsd controls and for the three doses tested, PCB 153 exposure produced a few specific behavioral changes only in males. The data suggest that PCB 153 exposure interacts with strain and sex, and also indicate a non-linear dose–response relation for the behaviors observed.

Conclusions

Exposure to PCB 153 seems to interact with several variables including strain, sex, dose, and time of testing. To the extent that the present findings can be generalized to humans, exposure effects of PCB 153 on ADHD behavior depends on amount of exposure, where high doses may aggravate ADHD symptoms in genetically vulnerable individuals. In normal controls, exposure may not constitute an environmental risk factor for developing the full range of ADHD symptoms, but can produce specific behavioral changes.
Appendix
Available only for authorised users
Literature
1.
American Psychiatric Association: Diagnostic and statistical manual of mental disorders. Text revision (DSM-IV-TR), 4 edn. 2000, Washington DC: America Psychiatric AssociationCrossRef
2.
Biederman J: Attention-deficit/hyperactivity disorder: a selective overview. Biol Psychiatry. 2005, 57: 1215-1220. 10.1016/j.biopsych.2004.10.020.PubMedCrossRef
3.
Genro JP, Kieling C, Rohde LA, Hutz MH: Attention-deficit/hyperactivity disorder and the dopaminergic hypotheses. Expert Rev Neurother. 2010, 10: 587-601. 10.1586/ern.10.17.PubMedCrossRef
4.
Faraone SV, Perlis RH, Doyle AE, Smoller JW, Goralnick JJ, Holmgren MA, Sklar P: Molecular genetics of attention-deficit/hyperactivity disorder. Biol Psychiatry. 2005, 57: 1313-1323. 10.1016/j.biopsych.2004.11.024.PubMedCrossRef
5.
Rutter M, Moffitt TE, Caspi A: Gene-environment interplay and psychopathology: multiple varieties but real effects. J Child Psychol Psychiatry. 2006, 47: 226-261. 10.1111/j.1469-7610.2005.01557.x.PubMedCrossRef
6.
Snowling M: Editorial: Multiple perspectives on ADHD: implications for future research. J Child Psychol Psychiatry. 2009, 50: 1039-1041. 10.1111/j.1469-7610.2009.02145.x.PubMedCrossRef
7.
Caspi A, Moffitt TE: Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat Rev Neurosci. 2006, 7: 583-590.PubMedCrossRef
8.
Linnet KM, Dalsgaard S, Obel C, Wisborg K, Henriksen TB, Rodriguez A, Kotimaa A, Moilanen I, Thomsen PH, Olsen J, Jarvelin MR: Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am J Psychiatry. 2003, 160: 1028-1040. 10.1176/appi.ajp.160.6.1028.PubMedCrossRef
9.
Mick E, Biederman J, Prince J, Fischer MJ, Faraone SV: Impact of low birth weight on attention-deficit hyperactivity disorder. J Dev Behav Pediatr. 2002, 23: 16-22. 10.1097/00004703-200202000-00004.PubMedCrossRef
10.
Williams JH, Ross L: Consequences of prenatal toxin exposure for mental health in children and adolescents: a systematic review. Eur Child Adolesc Psychiatry. 2007, 16: 243-253. 10.1007/s00787-006-0596-6.PubMedCrossRef
11.
Nigg JT: What causes ADHD?: Understanding what goes wrong and why. 2009, New York, NY: Guilford Publications
12.
Rice DC: Parallels between attention deficit hyperactivity disorder and behavioral deficits produced by neurotoxic exposure in monkeys. Environ Health Perspect. 2000, 108: 405-408.PubMedCentralPubMedCrossRef
13.
Sagiv SK, Thurston SW, Bellinger DC, Tolbert PE, Altshul LM, Korrick SA: Prenatal organochlorine exposure and behaviors associated with attention deficit hyperactivity disorder in school-aged children. Am J Epidemiol. 2010, 171: 593-601. 10.1093/aje/kwp427.PubMedCentralPubMedCrossRef
14.
DasBanerjee T, Middleton FA, Berger DF, Lombardo JP, Sagvolden T, Faraone SV: A comparison of molecular alterations in environmental and genetic rat models of ADHD: A pilot study. Am J Med Genet B Neuropsychiatr Genet. 2008, 147B: 1554-1563. 10.1002/ajmg.b.30877.PubMedCentralPubMedCrossRef
15.
Eubig PA, Aguiar A, Schantz SL: Lead and PCBs as risk factors for attention deficit/hyperactivity disorder. Environ Health Perspect. 2010, 118: 1654-1667. 10.1289/ehp.0901852.PubMedCentralPubMedCrossRef
16.
Mariussen E, Fonnum F: Neurochemical targets and behavioral effects of organohalogen compounds: an update. Crit Rev Toxicol. 2006, 36: 253-289. 10.1080/10408440500534164.PubMedCrossRef
17.
Fonnum F, Mariussen E: Mechanisms involved in the neurotoxic effects of environmental toxicants such as polychlorinated biphenyls and brominated flame retardants. J Neurochem. 2009, 111: 1327-1347. 10.1111/j.1471-4159.2009.06427.x.PubMedCrossRef
18.
Breivik K, Sweetman A, Pacyna JM, Jones KC: Towards a global historical emission inventory for selected PCB congeners–a mass balance approach. 2. Emissions. Sci Total Environ. 2002, 290: 199-224. 10.1016/S0048-9697(01)01076-2.PubMedCrossRef
19.
Safe S: Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit Rev Toxicol. 1990, 21: 51-88. 10.3109/10408449009089873.PubMedCrossRef
20.
Bushnell PJ, Moser VC, MacPhail RC, Oshiro WM, Derr-Yellin EC, Phillips PM, Kodavanti PR: Neurobehavioral assessments of rats perinatally exposed to a commercial mixture of polychlorinated biphenyls. Toxicol Sci. 2002, 68: 109-120. 10.1093/toxsci/68.1.109.PubMedCrossRef
21.
Schantz SL: Developmental neurotoxicity of PCBs in humans: what do we know and where do we go from here?. Neurotoxicol Teratol. 1996, 18: 217-227. 10.1016/S0892-0362(96)90001-X.PubMedCrossRef
22.
Stewart P, Reihman J, Gump B, Lonky E, Darvill T, Pagano J: Response inhibition at 8 and 9 1/2 years of age in children prenatally exposed to PCBs. Neurotoxicol Teratol. 2005, 27: 771-780. 10.1016/j.ntt.2005.07.003.PubMedCrossRef
23.
Stewart P, Fitzgerald S, Reihman J, Gump B, Lonky E, Darvill T, Pagano J, Hauser P: Prenatal PCB exposure, the corpus callosum, and response inhibition. Environ Health Perspect. 2003, 111: 1670-1677. 10.1289/ehp.6173.PubMedCentralPubMedCrossRef
24.
Grandjean P, Weihe P, Burse VW, Needham LL, Storr-Hansen E, Heinzow B, Debes F, Murata K, Simonsen H, Ellefsen P, Budtz-Jorgensen E, Keiding N, White RF: Neurobehavioral deficits associated with PCB in 7-year-old children prenatally exposed to seafood neurotoxicants. Neurotoxicol Teratol. 2001, 23: 305-317. 10.1016/S0892-0362(01)00155-6.PubMedCrossRef
25.
Jacobson JL, Jacobson SW: Intellectual impairment in children exposed to polychlorinated biphenyls in utero. N Engl J Med. 1996, 335: 783-789. 10.1056/NEJM199609123351104.PubMedCrossRef
26.
Jacobson JL, Jacobson SW: Dose–response in perinatal exposure to polychlorinated biphenyls (PCBs): The Michigan and North Carolina cohort studies. Toxicol Ind Health. 1996, 12: 435-445. 10.1177/074823379601200315.PubMedCrossRef
27.
Patandin S, Lanting CI, Mulder PG, Boersma ER, Sauer PJ, Weisglas-Kuperus N: Effects of environmental exposure to polychlorinated biphenyls and dioxins on cognitive abilities in Dutch children at 42 months of age. J Pediatr. 1999, 134: 33-41. 10.1016/S0022-3476(99)70369-0.PubMedCrossRef
28.
Vreugdenhil HJ, Mulder PG, Emmen HH, Weisglas-Kuperus N: Effects of perinatal exposure to PCBs on neuropsychological functions in the Rotterdam cohort at 9 years of age. Neuropsychology. 2004, 18: 185-193.PubMedCrossRef
29.
Heinzel S, Dresler T, Baehne CG, Heine M, Boreatti-Hummer A, Jacob CP: COMT × DRD4 epistasis impacts prefrontal cortex function underlying response control. Cereb Cortex. 2013, 23: 1453-1462. 10.1093/cercor/bhs132.PubMedCrossRef
30.
Sagvolden T, Johansen EB, Aase H, Russell VA: A dynamic developmental theory of Attention-Deficit/Hyperactivity Disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behav Brain Sci. 2005, 28: 397-419.PubMedCrossRef
31.
Haenlein M, Caul WF: Attention deficit disorder with hyperactivity: a specific hypothesis of reward dysfunction. J Am Acad Child Adolesc Psychiatry. 1987, 26: 356-362. 10.1097/00004583-198705000-00014.PubMedCrossRef
32.
Wender PH: Minimal brain dysfunction in children. 1971, New York: Wiley
33.
Wender PH: The minimal brain dysfunction syndrome in children. I. The syndrome and its relevance for psychiatry. II. A psychological and biochemical model for the syndrome. J Nerv Ment Dis. 1972, 155: 55-71. 10.1097/00005053-197207000-00007.PubMedCrossRef
34.
Wender PH: Some speculations concerning a possible biochemical basis of minimal brain dysfunction. Life Sci. 1974, 14: 1605-1621. 10.1016/0024-3205(74)90263-X.PubMedCrossRef
35.
Douglas VI, Parry PA: Effects of reward on delayed reaction time task performance of hyperactive children. J Abnorm Child Psychol. 1983, 11: 313-326. 10.1007/BF00912094.PubMedCrossRef
36.
Freibergs V, Douglas VI: Concept learning in hyperactive and normal children. J Abnorm Psychol. 1969, 74: 388-395.PubMedCrossRef
37.
Sonuga-Barke EJ, Taylor E, Sembi S, Smith J: Hyperactivity and delay aversion–I. The effect of delay on choice. J Child Psychol Psychiatry. 1992, 33: 387-398. 10.1111/j.1469-7610.1992.tb00874.x.PubMedCrossRef
38.
Sagvolden T, Archer T: Future perspectives on ADD research -- An irresistible challenge. Attention deficit disorder: clinical and basic research. Edited by: Sagvolden T, Hillsdale AT. 1989, N.J: Lawrence Erlbaum Associates, 369-389.
39.
Johansen EB, Aase H, Meyer A, Sagvolden T: Attention-deficit/hyperactivity disorder (ADHD) behaviour explained by dysfunctioning reinforcement and extinction processes. Behav Brain Res. 2002, 130: 37-45. 10.1016/S0166-4328(01)00434-X.PubMedCrossRef
40.
Sagvolden T, Wultz B, Moser EI, Moser M-B, Mørkrid L: Results from a comparative neuropsychological research program indicate altered reinforcement mechanisms in children with ADD. Attention deficit disorder: clinical and basic research. Edited by: Sagvolden T, Hillsdale AT. 1989, N.J: Lawrence Erlbaum Associates, 261-286.
41.
Johansen EB, Killeen PR, Russell VA, Tripp G, Wickens JR, Tannock R, Williams J, Sagvolden T: Origins of altered reinforcement effects in ADHD. Behav Brain Funct. 2009, 5: 7-10.1186/1744-9081-5-7.PubMedCentralPubMedCrossRef
42.
43.
Johansen EB, Knoff M, Fonnum F, Lausund PL, Walaas SI, Woien G: Postnatal exposure to PCB 153 and PCB 180, but not to PCB 52, produces changes in activity level and stimulus control in outbred male Wistar Kyoto rats. Behav Brain Funct. 2011, 7: 18-10.1186/1744-9081-7-18.PubMedCentralPubMedCrossRef
44.
Sagvolden T, Aase H, Zeiner P, Berger D: Altered reinforcement mechanisms in attention-deficit/hyperactivity disorder. Behav Brain Res. 1998, 94: 61-71. 10.1016/S0166-4328(97)00170-8.PubMedCrossRef
45.
46.
Aase H, Meyer A, Sagvolden T: Moment-to-moment dynamics of ADHD behaviour in South African children. Behav Brain Funct. 2006, 2: 11-10.1186/1744-9081-2-11.PubMedCentralPubMedCrossRef
47.
Sagvolden T: Behavioral validation of the spontaneously hypertensive rat (SHR) as an animal model of attention-deficit/hyperactivity disorder (AD/HD). Neurosci Biobehav Rev. 2000, 24: 31-39. 10.1016/S0149-7634(99)00058-5.PubMedCrossRef
48.
49.
Sagvolden T, Russell VA, Aase H, Johansen EB, Farshbaf M: Rodent models of attention-deficit/hyperactivity disorder. Biol Psychiatry. 2005, 57: 1239-1247. 10.1016/j.biopsych.2005.02.002.PubMedCrossRef
50.
Sagvolden T, Johansen EB, Woien G, Walaas SI, Storm-Mathisen J, Bergersen LH, Hvalby O, Jensen V, Aase H, Russell VA, Killeen PR, DasBanerjee T, Middleton FA, Faraone SV: The spontaneously hypertensive rat model of ADHD - The importance of selecting the appropriate reference strain. Neuropharmacology. 2009, 57: 619-626. 10.1016/j.neuropharm.2009.08.004.PubMedCentralPubMedCrossRef
51.
Sagvolden T, Johansen EB: Rat Models of ADHD. Behavioral neuroscience of attention deficit hyperactivity disorder and its treatment. Edited by: Stanford C, Tannock R. 2012, Berlin: Springer Berlin Heidelberg, 301-315.
52.
Fonnum F, Mariussen E, Reistad T: Molecular mechanisms involved in the toxic effects of polychlorinated biphenyls (PCBs) and brominated flame retardants (BFRs). J Toxicol Environ Health A. 2006, 69: 21-35. 10.1080/15287390500259020.PubMedCrossRef
53.
Russell V, Allie S, Wiggins T: Increased noradrenergic activity in prefrontal cortex slices of an animal model for attention-deficit hyperactivity disorder–the spontaneously hypertensive rat. Behav Brain Res. 2000, 117: 69-74. 10.1016/S0166-4328(00)00291-6.PubMedCrossRef
54.
Russell VA: Hypodopaminergic and hypernoradrenergic activity in prefrontal cortex slices of an animal model for attention-deficit hyperactivity disorder – the spontaneously hypertensive rat. Behav Brain Res. 2002, 130: 191-196. 10.1016/S0166-4328(01)00425-9.PubMedCrossRef
55.
Russell VA: Dopamine hypofunction possibly results from a defect in glutamate-stimulated release of dopamine in the nucleus accumbens shell of a rat model for attention deficit hyperactivity disorder–the spontaneously hypertensive rat. Neurosci Biobehav Rev. 2003, 27: 671-682. 10.1016/j.neubiorev.2003.08.010.PubMedCrossRef
56.
Miller EM, Pomerleau F, Huettl P, Russell VA, Gerhardt GA, Glaser PE: The spontaneously hypertensive and Wistar Kyoto rat models of ADHD exhibit sub-regional differences in dopamine release and uptake in the striatum and nucleus accumbens. Neuropharmacology. 2012, 63: 1327-1334. 10.1016/j.neuropharm.2012.08.020.PubMedCentralPubMedCrossRef
57.
Lee DW, Notter SA, Thiruchelvam M, Dever DP, Fitzpatrick R, Kostyniak PJ, Cory-Slechta DA, Opanashuk LA: Subchronic polychlorinated biphenyl (Aroclor 1254) exposure produces oxidative damage and neuronal death of ventral midbrain dopaminergic systems. Toxicol Sci. 2012, 125: 496-508. 10.1093/toxsci/kfr313.PubMedCentralPubMedCrossRef
58.
Beck V, Roelens SA, Darras VM: Exposure to PCB 77 induces tissue-dependent changes in iodothyronine deiodinase activity patterns in the embryonic chicken. Gen Comp Endocrinol. 2006, 148: 327-335. 10.1016/j.ygcen.2006.04.003.PubMedCrossRef
59.
Dobbing J, Sands J: Comparative aspects of the brain growth spurt. Early Hum Dev. 1979, 3: 79-83. 10.1016/0378-3782(79)90022-7.PubMedCrossRef
60.
Sagvolden T, Xu T: l-Amphetamine improves poor sustained attention while d-amphetamine reduces overactivity and impulsiveness as well as improves sustained attention in an animal model of Attention-Deficit/Hyperactivity Disorder (ADHD). Behav Brain Funct. 2008, 4: 3-10.1186/1744-9081-4-3.PubMedCentralPubMedCrossRef
61.
Sagiv SK, Thurston SW, Bellinger DC, Altshul LM, Korrick SA: Neuropsychological measures of attention and impulse control among 8-year-old children exposed prenatally to organochlorines. Environ Health Perspect. 2012, 120: 904-909. 10.1289/ehp.1104372.PubMedCentralPubMedCrossRef
62.
De JW, Linthorst AC, Versteeg HG: The nigrostriatal dopamine system and the development of hypertension in the spontaneously hypertensive rat. Arch Mal Coeur Vaiss. 1995, 88: 1193-1196.
63.
National Instruments: LabVIEW (Version 7.1). 2004, Texas, USA: Austin
64.
Catania AC: Learning. 1998, Prentice Hall: N.J., Englewoods Cliffs, 4
65.
Reilly MP: Variable interval generator 1.2. 2001
66.
Catania AC, Reynolds GS: A quantitative analysis of the responding maintained by interval schedules of reinforcement. J Exp Anal Behav. 1968, 11: Suppl-83-10.1901/jeab.1968.11-83.CrossRef
67.
Jensenius AR, Godoey RI, Wanderley MM: Developing tools for studying musical gestures within the MAX/MSP/Jitter environment. Proceedings of the 2005 International Computer Music Conference. 2005, 282-285.
68.
StatSoft: Statistica for windows. 2005, Tulsa, OK: StatSoft, Inc
69.
Myers JL, Well AD: Research design and statistical analysis. 2003, Mahwah: Lawrence Erlbaum Associates, 2
70.
Dervola KS, Roberg BA, Woien G, Bogen IL, Sandvik TH, Sagvolden T, Drevon CA, Johansen EB, Walaas SI: Marine omega-3 polyunsaturated fatty acids induce sex-specific changes in reinforcer-controlled behaviour and neurotransmitter metabolism in a spontaneously hypertensive rat model of ADHD. Behav Brain Funct. 2012, 8: 56-10.1186/1744-9081-8-56.PubMedCentralPubMedCrossRef
71.
72.
Johansen EB, Killeen PR, Sagvolden T: Behavioral variability, elimination of responses, and delay-of-reinforcement gradients in SHR and WKY rats. Behav Brain Funct. 2007, 3: 60-10.1186/1744-9081-3-60.PubMedCentralPubMedCrossRef
73.
Holene E, Nafstad I, Skaare JU, Sagvolden T: Behavioural hyperactivity in rats following postnatal exposure to sub- toxic doses of polychlorinated biphenyl congeners 153 and 126. Behav Brain Res. 1998, 94: 213-224. 10.1016/S0166-4328(97)00181-2.PubMedCrossRef
74.
Holene E, Nafstad I, Skaare JU, Krogh H, Sagvolden T: Behavioural effects in female rats of postnatal exposure to sub-toxic doses of polychlorinated biphenyl congener 153. Acta Paediatr Suppl. 1999, 88: 55-63.PubMedCrossRef
75.
Berger DF, Lombardo JP, Jeffers PM, Hunt AE, Bush B, Casey A, Quimby F: Hyperactivity and impulsiveness in rats fed diets supplemented with either Aroclor 1248 or PCB-contaminated St. Lawrence river fish. Behav Brain Res. 2001, 126: 1-11. 10.1016/S0166-4328(01)00244-3.PubMedCrossRef
76.
Fink JS, Smith GP: Mesolimbic and mesocortical dopaminergic neurons are necessary for normal exploratory behavior in rats. Neurosci Lett. 1980, 17: 61-65. 10.1016/0304-3940(80)90062-2.PubMedCrossRef
77.
Granger R, Staubli U, Davis M, Perez Y, Nilsson L, Rogers GA, Lynch G: A drug that facilitates glutamatergic transmission reduces exploratory activity and improves performance in a learning-dependent task. Synapse. 1993, 15: 326-329. 10.1002/syn.890150409.PubMedCrossRef
78.
Sazonova NA, DasBanerjee T, Middleton FA, Gowtham S, Schuckers S, Faraone SV: Transcriptome-wide gene expression in a rat model of attention deficit hyperactivity disorder symptoms: Rats developmentally exposed to polychlorinated biphenyls. Am J Med Genet B Neuropsychiatr Genet. 2011, 156: 898-912. 10.1002/ajmg.b.31230.CrossRef
79.
Piedrafita B, Erceg S, Cauli O, Monfort P, Felipo V: Developmental exposure to polychlorinated biphenyls PCB153 or PCB126 impairs learning ability in young but not in adult rats. Eur J Neurosci. 2008, 27: 177-182. 10.1111/j.1460-9568.2007.05988.x.PubMedCrossRef
80.
Cauli O, Piedrafita B, Llansola M, Felipo V: Gender differential effects of developmental exposure to methyl-mercury, polychlorinated biphenyls 126 or 153, or its combinations on motor activity and coordination. Toxicology. 2013, 311: 61-68. 10.1016/j.tox.2012.11.016.PubMedCrossRef
81.
Ferguson SA, Gray EP, Cada AM: Early behavioral development in the spontaneously hypertensive rat: a comparison with the Wistar-Kyoto and Sprague–Dawley strains. Behav Neurosci. 2003, 117: 263-270.PubMedCrossRef
82.
Pinilla L, Castellano JM, Romero M, Tena-Sempere M, Gaytan F, Aguilar E: Delayed puberty in spontaneously hypertensive rats involves a primary ovarian failure independent of the hypothalamic KiSS-1/GPR54/GnRH system. Endocrinology. 2009, 150: 2889-2897. 10.1210/en.2008-1381.PubMedCrossRef
83.
Berberich S, Punnakkal P, Jensen V, Pawlak V, Seeburg PH, Hvalby O, Kohr G: Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. J Neurosci. 2005, 25: 6907-6910. 10.1523/JNEUROSCI.1905-05.2005.PubMedCrossRef
84.
Bliss TV, Lomo T: Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973, 232: 331-356.PubMedCentralPubMedCrossRef
85.
Dickerson SM, Cunningham SL, Gore AC: Prenatal PCBs disrupt early neuroendocrine development of the rat hypothalamus. Toxicol Appl Pharmacol. 2011, 252: 36-46. 10.1016/j.taap.2011.01.012.PubMedCentralPubMedCrossRef
86.
Hilgier W, Lazarewicz JW, Struzynska L, Frontczak-Baniewicz M, Albrecht J: Repeated exposure of adult rats to Aroclor 1254 induces neuronal injury and impairs the neurochemical manifestations of the NMDA receptor-mediated intracellular signaling in the hippocampus. Neurotoxicology. 2012, 33: 16-22. 10.1016/j.neuro.2011.10.005.PubMedCrossRef
87.
Boix J, Cauli O, Felipo V: Developmental exposure to polychlorinated biphenyls 52, 138 or 180 affects differentially learning or motor coordination in adult rats. Mechanisms involved. Neuroscience. 2010, 167: 994-1003. 10.1016/j.neuroscience.2010.02.068.PubMedCrossRef
88.
Niemi WD, Audi J, Bush B, Carpenter DO: PCBs reduce long-term potentiation in the CA1 region of rat hippocampus. Exp Neurol. 1998, 151: 26-34. 10.1006/exnr.1998.6793.PubMedCrossRef
89.
Ozcan M, Yilmaz B, King WM, Carpenter DO: Hippocampal long-term potentiation (LTP) is reduced by a coplanar PCB congener. Neurotoxicology. 2004, 25: 981-988. 10.1016/j.neuro.2004.03.014.PubMedCrossRef
90.
Hussain RJ, Gyori J, DeCaprio AP, Carpenter DO: In vivo and in vitro exposure to PCB 153 reduces long-term potentiation. Environ Health Perspect. 2000, 108: 827-831. 10.1289/ehp.00108827.PubMedCentralPubMedCrossRef
91.
Hollmann M, Heinemann S: Cloned glutamate receptors. Annu Rev Neurosci. 1994, 17: 31-108. 10.1146/annurev.ne.17.030194.000335.PubMedCrossRef
92.
Dingledine R, Borges K, Bowie D, Traynelis SF: The glutamate receptor ion channels. Pharmacol Rev. 1999, 51: 7-61.PubMed
93.
Erreger K, Dravid SM, Banke TG, Wyllie DJ, Traynelis SF: Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. J Physiol. 2005, 563: 345-358. 10.1113/jphysiol.2004.080028.PubMedCentralPubMedCrossRef
94.
Lehohla M, Kellaway L, Russell V: NMDA receptor function in the prefrontal cortex of a rat model for attention-deficit hyperactivity disorder. Metab Brain Dis. 2004, 19: 35-42.PubMedCrossRef
95.
Jensen V, Rinholm JE, Johansen TJ, Medin T, Storm-Mathisen J, Sagvolden T, Hvalby O, Bergersen LH: N-methyl-d-aspartate receptor subunit dysfunction at hippocampal glutamatergic synapses in an animal model of attention-deficit/hyperactivity disorder. Neuroscience. 2009, 158: 353-364. 10.1016/j.neuroscience.2008.05.016.PubMedCrossRef
96.
Smith AG, Gangolli SD: Organochlorine chemicals in seafood: occurrence and health concerns. Food Chem Toxicol. 2002, 40: 767-779. 10.1016/S0278-6915(02)00046-7.PubMedCrossRef
97.
Castoldi AF, Blandini F, Randine G, Samuele A, Manzo L, Coccini T: Brain monoaminergic neurotransmission parameters in weanling rats after perinatal exposure to methylmercury and 2,2′,4,4′,5,5′-hexachlorobiphenyl (PCB153). Brain Res. 2006, 1112: 91-98. 10.1016/j.brainres.2006.07.022.PubMedCrossRef
98.
Schantz SL, Moshtaghian J, Ness DK: Spatial learning deficits in adult rats exposed to ortho-substituted PCB congeners during gestation and lactation. Fundam Appl Toxicol. 1995, 26: 117-126. 10.1006/faat.1995.1081.PubMedCrossRef
99.
Widholm JJ, Clarkson GB, Strupp BJ, Crofton KM, Seegal RF, Schantz SL: Spatial reversal learning in Aroclor 1254-exposed rats: sex-specific deficits in associative ability and inhibitory control. Toxicol Appl Pharmacol. 2001, 174: 188-198. 10.1006/taap.2001.9199.PubMedCrossRef
100.
Roegge CS, Seo BW, Crofton KM, Schantz SL: Gestational-lactational exposure to Aroclor 1254 impairs radial-arm maze performance in male rats. Toxicol Sci. 2000, 57: 121-130. 10.1093/toxsci/57.1.121.PubMedCrossRef
101.
Geller AM, Oshiro WM, Haykal-Coates N, Kodavanti PR, Bushnell PJ: Gender-dependent behavioral and sensory effects of a commercial mixture of polychlorinated biphenyls (Aroclor 1254) in rats. Toxicol Sci. 2001, 59: 268-277. 10.1093/toxsci/59.2.268.PubMedCrossRef
102.
Hatcher-Martin JM, Gearing M, Steenland K, Levey AI, Miller GW, Pennell KD: Association between polychlorinated biphenyls and Parkinson’s disease neuropathology. Neurotoxicology. 2012, 33: 1298-1304. 10.1016/j.neuro.2012.08.002.PubMedCentralPubMedCrossRef
103.
Nishida N, Farmer JD, Kodavanti PR, Tilson HA, MacPhail RC: Effects of acute and repeated exposures to Aroclor 1254 in adult rats: motor activity and flavor aversion conditioning. Fundam Appl Toxicol. 1997, 40: 68-74. 10.1006/faat.1997.2352.PubMedCrossRef
104.
Kodavanti PR, Ward TR, Derr-Yellin EC, Mundy WR, Casey AC, Bush B, Tilson HA: Congener-specific distribution of polychlorinated biphenyls in brain regions, blood, liver, and fat of adult rats following repeated exposure to Aroclor 1254. Toxicol Appl Pharmacol. 1998, 153: 199-210. 10.1006/taap.1998.8534.PubMedCrossRef
105.
Yang D, Kim KH, Phimister A, Bachstetter AD, Ward TR, Stackman RW, Mervis RF, Wisniewski AB, Klein SL, Kodavanti PR, Anderson KA, Wayman G, Pessah IN, Lein PJ: Developmental exposure to polychlorinated biphenyls interferes with experience-dependent dendritic plasticity and ryanodine receptor expression in weanling rats. Environ Health Perspect. 2009, 117: 426-435.PubMedCentralPubMedCrossRef
106.
Eriksson P, Fischer C, Fredriksson A: Polybrominated diphenyl ethers, a group of brominated flame retardants, can interact with polychlorinated biphenyls in enhancing developmental neurobehavioral defects. Toxicol Sci. 2006, 94: 302-309. 10.1093/toxsci/kfl109.PubMedCrossRef
107.
Andersen ME, Yang RS, French CT, Chubb LS, Dennison JE: Molecular circuits, biological switches, and nonlinear dose–response relationships. Environ Health Perspect. 2002, 110 (Suppl 6): 971-978.PubMedCentralPubMedCrossRef
108.
Phillips KP, Foster WG, Leiss W, Sahni V, Karyakina N, Turner MC, Kacew S, Krewski D: Assessing and managing risks arising from exposure to endocrine-active chemicals. J Toxicol Environ Health B Crit Rev. 2008, 11: 351-372. 10.1080/10937400701876657.PubMedCrossRef
109.
Metadata
Title
Behavioral changes following PCB 153 exposure in the Spontaneously Hypertensive rat – an animal model of Attention-Deficit/Hyperactivity disorder
Authors
Espen Borgå Johansen
Frode Fonnum
Per L Lausund
S Ivar Walaas
Nora Elise Bærland
Grete Wøien
Terje Sagvolden
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Behavioral and Brain Functions / Issue 1/2014
Electronic ISSN: 1744-9081
DOI
https://doi.org/10.1186/1744-9081-10-1

Other articles of this Issue 1/2014

Behavioral and Brain Functions 1/2014 Go to the issue

Research

A common haplotype of KIAA0319 contributes to the phonological awareness skill in Chinese children

Research

Does IQ influence Associations between ADHD Symptoms and other Cognitive Functions in young Preschoolers?

Research

Multilevel analysis of facial expressions of emotion and script: self-report (arousal and valence) and psychophysiological correlates

Research

Right and left amygdalae activation in patients with major depression receiving antidepressant treatment, as revealed by fMRI

Research

Age-dependent effect of high cholesterol diets on anxiety-like behavior in elevated plus maze test in rats

Research

Fat-mass and obesity-associated gene polymorphisms and weight gain after risperidone treatment in first episode schizophrenia