AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (1.3 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Alterations of attention and impulsivity in the rat following a transgenerational decrease in dietary omega-3 fatty acids

Joachim HauserEwelina StollbergAndreas ReissmannIvo KaunzingerKlaus W. Lange( )
Department of Experimental Psychology, University of Regensburg, 93040 Regensburg, Germany

Peer review under responsibility of KeAi Communications Co., Ltd.

Show Author Information

Abstract

Polyunsaturated fatty acids (PUFAs), particularly the omega-3 PUFAs, are thought to be involved in neuronal processes, to play a role in neurodevelopmental disorders and to be important for the integrity of central nervous system functioning. The present study investigated the effects of nutritional omega-3 PUFAs on attentional functions and impulsive behavior in Wistar rats. For this purpose, female Wistar rats were fed an omega-3 deficient diet over several generations, and the dams of the seventh generation were randomly assigned to two diet groups and fed an omega-3 deficient or an omega-3 sufficient diet. In addition, a group of previously untreated dams was fed an omega-3 sufficient diet. The male offspring of these three diet groups were tested using an established paradigm for the assessment of attention and impulsive behavior, i.e. a modified version of the five-choice-serial-reaction-time task (5CSRTT). The present data show that the deficiency of omega-3 PUFAs over generations led to substantial changes in attentional processes and impulsive behaviors. The impairments associated with an omega-3 deficiency were partly corrected by treatment with the omega-3 sufficient diet in the last generation of the omega-3 deficient group which showed substantial improvements in attention parameters. While there were no significant effects of dietary modifications on psychomotor activity levels, there was some evidence for changes in impulsive behavior. In conclusion, transgenerational dietary changes in the availability of omega-3 PUFAs led to changes in attentional processes and impulsive behavior in rats, supporting the hypothesis that omega-3 PUFAs play a role in cognitive and behavioral processes. The present findings offer a promising approach in the investigation of the role of omega-3 PUFAs in a variety of cognitive and behavioral domains.

References

[1]

J.P. Schuchardt, M. Huss, M. Stauss-Grabo, A. Hahn, Significance of long-chain polyunsaturated fatty acids (PUFAs) for the development and behaviour of children, Eur. J. Pediatr. 169 (2010) 149–164, http://dx.doi.org/10.1007/s00431-009-1035-8.

[2]

P.E. Wainwright, Dietary essential fatty acids and brain function: a developmental perspective on mechanisms, Proc. Nutr. Soc. 61 (2002) 61–69 https://www.ncbi.nlm.nih.gov/pubmed/12002796.

[3]

M.G. Morgese, L. Trabace, Maternal Malnutrition in the Etiopathogenesis of Psychiatric Diseases: Role of Polyunsaturated Fatty Acids, Brain Sci. 6 (2016), http://dx.doi.org/10.3390/brainsci6030024.

[4]

L. Stevens, W. Zhang, L. Peck, T. Kuczek, N. Grevstad, A. Mahon, S.S. Zentall, L.E. Arnold, J.R. Burgess, EFA supplementation in children with inattention, hyperactivity, and other disruptive behaviors, Lipids 38 (2003) 1007–1021.

[5]

J.J. Liu, P. Green, J. John Mann, S.I. Rapoport, M.E. Sublette, Pathways of polyunsaturated fatty acid utilization: implications for brain function in neuropsychiatric health and disease, Brain Res. 1597 (2015) 220–246,http://dx.doi.org/10.1016/j.brainres.2014.11.059.

[6]

N. Sinn, C. Milte, P.R.C. Howe, Oiling the brain: a review of randomized controlled trials of omega-3 fatty acids in psychopathology across the lifespan, Nutrients 2 (2010) 128–170, http://dx.doi.org/10.3390/nu2020128.

[7]

M.T. Clandinin, J.E. Chappell, S. Leong, T. Heim, P.R. Swyer, G.W. Chance, Extrauterine fatty acid accretion in infant brain: implications for fatty acid requirements, Early Hum. Dev. 4 (1980) 131–138.

[8]

B. Koletzko, E. Lien, C. Agostoni, H. Böhles, C. Campoy, I. Cetin, T. Decsi, J.W. Dudenhausen, C. Dupont, S. Forsyth, I. Hoesli, W. Holzgreve, A. Lapillonne, G. Putet, N.J. Secher, M. Symonds, H. Szajewska, P. Willatts, R. Uauy, The roles of long-chain polyunsaturated fatty acids in pregnancy, lactation and infancy: review of current knowledge and consensus recommendations, J. Perinat. Med. 36 (2008) 5–14,http://dx.doi.org/10.1515/jpm.2008.001.

[9]

B. Levant, T.J. Zarcone, S.C. Fowler, Developmental effects of dietary n-3 fatty acids on activity and response to novelty, Physiol. Behav. 101 (2010) 176–183, http://dx.doi.org/10.1016/j.physbeh.2010.04.038.

[10]

M. Martinez, Tissue levels of polyunsaturated fatty acids during early human development, J. Pediatr. 120 (1992) S129–138.

[11]

M. Martinez, Polyunsaturated fatty acids in the developing human brain, red cells and plasma: influence of nutrition and peroxisomal disease, World Rev. Nutr. Diet. 75 (1994) 70–78.

[12]

R.G. Jensen, Lipids in human milk, Lipids 34 (1999) 1243–1271.

[13]

B. Koletzko, I. Thiel, P.O. Abiodun, The fatty acid composition of human milk in Europe and Africa, J. Pediatr. 120 (1992) S62–70.

[14]

T. Moriguchi, R.S. Greiner, N. Salem, Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration, J. Neurochem. 75 (2000) 2563–2573.

[15]

J.P. Schuchardt, M. Huss, M. Stauss-Grabo, A. Hahn, Significance of long-chain polyunsaturated fatty acids (PUFAs) for the development and behaviour of children, Eur. J. Pediatr. 169 (2010) 149–164, http://dx.doi.org/10.1007/s00431-009-1035-8.

[16]

S.M. Innis, Dietary omega 3 fatty acids and the developing brain, Brain Res. 1237 (2008) 35–43, http://dx.doi.org/10.1016/j.brainres.2008.08.078.

[17]

S.E. Carlson, P.G. Rhodes, M.G. Ferguson, Docosahexaenoic acid status of preterm infants at birth and following feeding with human milk or formula, Am. J. Clin. Nutr. 44 (1986) 798–804.

[18]

J. Farquharson, F. Cockburn, W.A. Patrick, E.C. Jamieson, R.W. Logan, Infant cerebral cortex phospholipid fatty-acid composition and diet, Lancet 340 (1992) 810–813.

[19]

J. Farquharson, E.C. Jamieson, K.A. Abbasi, W.J. Patrick, R.W. Logan, F. Cockburn, Effect of diet on the fatty acid composition of the major phospholipids of infant cerebral cortex, Arch. Dis. Child. 72 (1995) 198–203.

[20]

S.E. Carlson, S.H. Werkman, A randomized trial of visual attention of preterm infants fed docosahexaenoic acid until two months, Lipids 31 (1996) 85–90.

[21]

S.E. Carlson, S.H. Werkman, P.G. Rhodes, E.A. Tolley, Visual-acuity development in healthy preterm infants: effect of marine-oil supplementation, Am. J. Clin. Nutr. 58 (1993) 35–42.

[22]

M.T. Clandinin, J.E. van Aerde, K.L. Merkel, C.L. Harris, M.A. Springer, J.W. Hansen, D.A. Diersen-Schade, Growth and development of preterm infants fed infant formulas containing docosahexaenoic acid and arachidonic acid, J. Pediatr. 146 (2005) 461–468, http://dx.doi.org/10.1016/j.jpeds.2004.11.030.

[23]

I.B. Helland, L. Smith, K. Saarem, O.D. Saugstad, C.A. Drevon, Maternal supplementation with very-long-chain n-3 fatty acids during pregnancy and lactation augments children’s IQ at 4 years of age, Pediatrics 111 (2003) e39–44.

[24]

R. Uauy, E. Birch, D. Birch, P. Peirano, Visual and brain function measurements in studies of n-3 fatty acid requirements of infants, J. Pediatr. 120 (1992) S168–180.

[25]

S.H. Werkman, S.E. Carlson, A randomized trial of visual attention of preterm infants fed docosahexaenoic acid until nine months, Lipids. 31 (1996) 91–97.

[26]

P. Willatts, J.S. Forsyth, M.K. DiModugno, S. Varma, M. Colvin, Effect of long-chain polyunsaturated fatty acids in infant formula on problem solving at 10 months of age, Lancet (London England) 352 (1998) 688–691.

[27]

C. Dullemeijer, J. Durga, I.A. Brouwer, O. van de Rest, F.J. Kok, R.-J.M. Brummer, M.P. van Boxtel, P. Verhoef, n 3 fatty acid proportions in plasma and cognitive performance in older adults, Am. J. Clin. Nutr. 86 (2007) 1479–1485.

[28]

S. Kalmijn, M.P.J. van Boxtel, M. Ocké, W.M.M. Verschuren, D. Kromhout, L.J. Launer, Dietary intake of fatty acids and fish in relation to cognitive performance at middle age, Neurology 62 (2004) 275–280.

[29]

M.C. Morris, D.A. Evans, J.L. Bienias, C.C. Tangney, D.A. Bennett, R.S. Wilson, N. Aggarwal, J. Schneider, Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease, Arch. Neurol. 60 (2003) 940–946,http://dx.doi.org/10.1001/archneur.60.7.940.

[30]

L. Schaeffer, H. Gohlke, M. Müller, I.M. Heid, L.J. Palmer, I. Kompauer, H. Demmelmair, T. Illig, B. Koletzko, J. Heinrich, Common genetic variants of the FADS1 FADS2 gene cluster and their reconstructed haplotypes are associated with the fatty acid composition in phospholipids, Hum. Mol. Genet. 15 (2006) 1745–1756, http://dx.doi.org/10.1093/hmg/ddl117.

[31]

L.J. Stevens, S.S. Zentall, M.L. Abate, T. Kuczek, J.R. Burgess, Omega-3 fatty acids in boys with behavior learning, and health problems, Physiol. Behav. 59 (1996) 915–920.

[32]

R.E. Cooper, C. Tye, J. Kuntsi, E. Vassos, P. Asherson, Omega-3 polyunsaturated fatty acid supplementation and cognition: A systematic review and meta-analysis, J. Psychopharmacol. 29 (2015) 753–763, http://dx.doi.org/10.1177/0269881115587958.

[33]

J. Jiao, Q. Li, J. Chu, W. Zeng, M. Yang, S. Zhu, Effect of n-3 PUFA supplementation on cognitive function throughout the life span from infancy to old age: a systematic review and meta-analysis of randomized controlled trials, Am. J. Clin. Nutr. 100 (2014) 1422–1436, http://dx.doi.org/10.3945/ajcn.114.095315.

[34]

S. Delion, S. Chalon, J. Hérault, D. Guilloteau, J.C. Besnard, G. Durand, Chronic dietary alpha-linolenic acid deficiency alters dopaminergic and serotoninergic neurotransmission in rats, J. Nutr. 124 (1994) 2466–2476.

[35]

S. Chalon, S. Vancassel, L. Zimmer, D. Guilloteau, G. Durand, Polyunsaturated fatty acids and cerebral function: focus on monoaminergic neurotransmission, Lipids 36 (2001) 937–944.

[36]

S. Chalon, Omega-3 fatty acids and monoamine neurotransmission, Prostaglandins. Leukot. Essent. Fatty Acids. 75 (2006) 259–269,http://dx.doi.org/10.1016/j.plefa.2006.07.005.

[37]

C. Transler, S. Mitchell, A. Eilander, Could polyunsaturated fatty acids deficiency explain some dysfunctions found in ADHD? Hypotheses from animal research, J. Atten. Disord. 17 (2013) 20–28, http://dx.doi.org/10.1177/1087054711401345.

[38]

H. Frances, C. Monier, M. Clement, A. Lecorsier, M. Debray, J.M. Bourre, Effect of dietary alpha-linolenic acid deficiency on habituation, Life Sci. 58 (1996) 1805–1816.

[39]

A.S. de Souza, L. da C. Pacheco, P. da S. Castro, J.N. Hokoç, M.S. Rocha, M. das G.T. do Carmo, Brain fatty acid profiles and spatial learning in malnourished rats: effects of nutritional intervention, Nutr. Neurosci. 11 (2008) 119–127, http://dx.doi.org/10.1179/147683008x301504.

[40]

I. Fedorova, N. Hussein, M.H. Baumann, C. Di Martino, N. Salem, An n-3 fatty acid deficiency impairs rat spatial learning in the Barnes maze, Behav. Neurosci. 123 (2009) 196–205, http://dx.doi.org/10.1037/a0013801.

[41]

P.E. Wainwright, E. Jalali, L.M. Mutsaers, R. Bell, S. Cvitkovic, An imbalance of dietary essential fatty acids retards behavioral development in mice, Physiol. Behav. 66 (1999) 833–839.

[42]

R.S. Greiner, T. Moriguchi, B.M. Slotnick, A. Hutton, N. Salem, Olfactory discrimination deficits in n-3 fatty acid-deficient rats, Physiol. Behav. 72 (2001) 379–385.

[43]

J.C. DeMar, K. Ma, J.M. Bell, M. Igarashi, D. Greenstein, S.I. Rapoport, One generation of n-3 polyunsaturated fatty acid deprivation increases depression and aggression test scores in rats, J. Lipid Res. 47 (2006) 172–180, http://dx.doi.org/10.1194/jlr.M500362-JLR200.

[44]

M. Enslen, H. Milon, A. Malnoë, Effect of low intake of n-3 fatty acids during development on brain phospholipid fatty acid composition and exploratory behavior in rats, Lipids 26 (1991) 203–208.

[45]

C.J. Antalis, L.J. Stevens, M. Campbell, R. Pazdro, K. Ericson, J.R. Burgess, Omega-3 fatty acid status in attention-deficit/hyperactivity disorder, Prostaglandins. Leukot. Essent. Fatty Acids. 75 (2006) 299–308, http://dx.doi.org/10.1016/j.plefa.2006.07.004.

[46]

J.-R. Chen, S.-F. Hsu, C.-D. Hsu, L.-H. Hwang, S.-C. Yang, Dietary patterns and blood fatty acid composition in children with attention-deficit hyperactivity disorder in Taiwan, J. Nutr. Biochem. 15 (2004) 467–472,http://dx.doi.org/10.1016/j.jnutbio.2004.01.008.

[47]

I. Colquhoun, S. Bunday, A lack of essential fatty acids as a possible cause of hyperactivity in children, Med. Hypotheses. 7 (1981) 673–679.

[48]

A.L. Colter, C. Cutler, K.A. Meckling, Fatty acid status and behavioural symptoms of attention deficit hyperactivity disorder in adolescents: a case-control study, Nutr. J. 7 (2008) 8, http://dx.doi.org/10.1186/1475-2891-7-8.

[49]

E.A. Mitchell, M.G. Aman, S.H. Turbott, M. Manku, Clinical characteristics and serum essential fatty acid levels in hyperactive children, Clin. Pediatr. (Phila) 26 (1987) 406–411,http://dx.doi.org/10.1177/000992288702600805.

[50]

L.J. Stevens, S.S. Zentall, J.L. Deck, M.L. Abate, B.A. Watkins, S.R. Lipp, J.R. Burgess, Essential fatty acid metabolism in boys with attention-deficit hyperactivity disorder, Am. J. Clin. Nutr. 62 (1995) 761–768.

[51]

S. Chalon, S. Delion-Vancassel, C. Belzung, D. Guilloteau, A.M. Leguisquet, J.C. Besnard, G. Durand, Dietary fish oil affects monoaminergic neurotransmission and behavior in rats, J. Nutr. 128 (1998) 2512–2519.

[52]

M. Carli, T.W. Robbins, J.L. Evenden, B.J. Everitt, Effects of lesions to ascending noradrenergic neurones on performance of a 5-choice serial reaction task in rats; implications for theories of dorsal noradrenergic bundle function based on selective attention and arousal, Behav. Brain Res. 9 (1983) 361–380.

[53]

T.W. Robbins, The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry, Psychopharmacol. 163 (2002) 362–380.

[54]

M.F. Bear, Homosynaptic long-term depression: a mechanism for memory? Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 9457–9458.

[55]

V. Deroche, M. Marinelli, S. Maccari, M. Le Moal, H. Simon, P.V. Piazza, Stress-induced sensitization and glucocorticoids. I. Sensitization of dopamine-dependent locomotor effects of amphetamine and morphine depends on stress-induced corticosterone secretion, J. Neurosci. 15 (1995) 7181–7188.

[56]

E.N. Pothos, L. Hernandez, B.G. Hoebel, Chronic food deprivation decreases extracellular dopamine in the nucleus accumbens: implications for a possible neurochemical link between weight loss and drug abuse, Obes. Res. 3 (Suppl. 4) (1995) 525S-529S.

[57]

I. Carrié, M. Clément, D. de Javel, H. Francès, J.M. Bourre, Phospholipid supplementation reverses behavioral and biochemical alterations induced by n-3 polyunsaturated fatty acid deficiency in mice, J. Lipid Res. 41 (2000) 473–480.

[58]

A. Ikemoto, M. Ohishi, Y. Sato, N. Hata, Y. Misawa, Y. Fujii, H. Okuyama, Reversibility of n-3 fatty acid deficiency-induced alterations of learning behavior in the rat: level of n-6 fatty acids as another critical factor, J. Lipid Res. 42 (2001) 1655–1663.

[59]

T. Moriguchi, N. Salem, Recovery of brain docosahexaenoate leads to recovery of spatial task performance, J. Neurochem. 87 (2003) 297–309.

[60]

T. Takeuchi, Y. Fukumoto, E. Harada, Influence of a dietary n-3 fatty acid deficiency on the cerebral catecholamine contents, EEG and learning ability in rat, Behav. Brain Res. 131 (2002) 193–203.

[61]

K.S. Dervola, B.A. Roberg, G. Wøien, I.L. Bogen, T.H. Sandvik, T. Sagvolden, C.A. Drevon, E.B. Johansen, S.I. Walaas, Marine Ο-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. 8 (2012) 56, http://dx.doi.org/10.1186/1744-9081-8-56.

[62]

J.-M. Alessandri, P. Guesnet, S. Vancassel, P. Astorg, I. Denis, B. Langelier, S. Aïd, C. Poumès-Ballihaut, G. Champeil-Potokar, M. Lavialle, Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life, Reprod. Nutr. Dev. 44 (2004) 509–538.

[63]

A. Lee, Membrane structure, Curr. Biol. 11 (2001) R811–814.

[64]

S. Yehuda, S. Rabinovitz, D.I. Mostofsky, Essential fatty acids are mediators of brain biochemistry and cognitive functions, J. Neurosci. Res. 56 (1999) 565–570,http://dx.doi.org/10.1002/(sici)1097-4547(19990615)56:6<565:aid-jnr2>3.0.co;2-h.

[65]

S.O. Ahmad, J.-H. Park, J.D. Radel, B. Levant, Reduced numbers of dopamine neurons in the substantia nigra pars compacta and ventral tegmental area of rats fed an n-3 polyunsaturated fatty acid-deficient diet: a stereological study, Neurosci. Lett. 438 (2008) 303–307, http://dx.doi.org/10.1016/j.neulet.2008.04.073.

[66]

S. Delion, S. Chalon, D. Guilloteau, J.C. Besnard, G. Durand, alpha-Linolenic acid dietary deficiency alters age-related changes of dopaminergic and serotoninergic neurotransmission in the rat frontal cortex, J. Neurochem. 66 (1996) 1582–1591.

[67]

J.C. McCann, B.N. Ames, Is docosahexaenoic acid an n-3 long-chain polyunsaturated fatty acid, required for development of normal brain function? An overview of evidence from cognitive and behavioral tests in humans and animals, Am. J. Clin. Nutr. 82 (2005) 281–295.

[68]

M. Neuringer, W.E. Connor, n-3 fatty acids in the brain and retina: evidence for their essentiality, Nutr. Rev. 44 (1986) 285–294.

[69]

E. Stollberg, J. Hauser, A. Reissmann, I. Kaunzinger, K.W. Lange, Transgenerational reduction of dietary polyunsaturated fatty acids and cognition in Wistar rats, Mov. Nutr. Health Dis. 2 (2018) 11–21, http://dx.doi.org/10.5283/mnhd.7.

[70]

E.S.J. Robinson, D.M. Eagle, D. Economidou, D.E.H. Theobald, A.C. Mar, E.R. Murphy, T.W. Robbins, J.W. Dalley, Behavioural characterisation of high impulsivity on the 5-choice serial reaction time task: specific deficits in waiting versus stopping, Behav. Brain Res. 196 (2009) 310–316, http://dx.doi.org/10.1016/j.bbr.2008.09.021.

[71]

T. Koskinen, A. Haapalinna, J. Sirviö, Alpha-adrenoceptor-mediated modulation of 5-HT2 receptor agonist induced impulsive responding in a 5-choice serial reaction time task, Pharmacol. Toxicol. 92 (2003) 214–225.

[72]

J. Catalan, T. Moriguchi, B. Slotnick, M. Murthy, R.S. Greiner, N. Salem, Cognitive deficits in docosahexaenoic acid-deficient rats, Behav. Neurosci. 116 (2002) 1022–1031.

[73]

I. Fedorova, N. Salem, Omega-3 fatty acids and rodent behavior, Prostaglandins. Leukot. Essent. Fatty Acids. 75 (2006) 271–289, http://dx.doi.org/10.1016/j.plefa.2006.07.006.

Food Science and Human Wellness
Pages 49-56
Cite this article:
Hauser J, Stollberg E, Reissmann A, et al. Alterations of attention and impulsivity in the rat following a transgenerational decrease in dietary omega-3 fatty acids. Food Science and Human Wellness, 2018, 7(1): 49-56. https://doi.org/10.1016/j.fshw.2017.12.004

337

Views

7

Downloads

3

Crossref

N/A

Web of Science

3

Scopus

0

CSCD

Altmetrics

Received: 10 August 2017
Revised: 19 December 2017
Accepted: 22 December 2017
Published: 15 February 2018
© 2018 “Society information”.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return