Impact of dietary n-3 polyunsaturated fatty acids on cognition, motor skills and hippocampal neurogenesis in developing C57BL/6J mice

被引:73
作者
Janssen, Carola I. F. [1 ]
Zerbi, Valerio [1 ]
Mutsaers, Martina P. C. [1 ]
de Jong, Bas S. W. [1 ]
Wiesmann, Maximilian [1 ,2 ]
Arnoldussen, Ilse A. C. [1 ]
Geenen, Bram [1 ]
Heerschap, Arend [3 ]
Muskiet, Frits A. J. [4 ]
Jouni, Zeina E. [5 ]
van Tol, Eric A. F. [5 ]
Gross, Gabriele [5 ]
Homberg, Judith R. [6 ]
Berg, Brian M. [5 ]
Kiliaan, Amanda J. [1 ]
机构
[1] Radboud Univ Nijmegen, Med Ctr, Donders Inst Brain Cognit & Behav, Dept Anat, NL-6500 HB Nijmegen, Netherlands
[2] Radboud Univ Nijmegen, Med Ctr, Donders Inst Brain Cognit & Behav, Dept Geriatr, NL-6500 HB Nijmegen, Netherlands
[3] Radboud Univ Nijmegen, Med Ctr, Donders Inst Brain Cognit & Behav, Dept Radiol, NL-6500 HB Nijmegen, Netherlands
[4] Univ Groningen, Univ Med Ctr Groningen, Lab Med, Groningen, Netherlands
[5] Mead Johnson Pediat Nutr Inst, Nijmegen, Netherlands
[6] Radboud Univ Nijmegen, Med Ctr, Donders Inst Brain Cognit & Behav, Dept Cognit Neurosci, NL-6500 HB Nijmegen, Netherlands
关键词
Brain development; Animal models; Omega-3 fatty acid supplementation; Cognition; Neurohistology; Phosphorus magnetic resonance imaging; BRAIN DOCOSAHEXAENOIC ACID; FISH-OIL SUPPLEMENTATION; INFANT VISUAL-ACUITY; ALPHA-LINOLENIC ACID; DOUBLE-BLIND; TERM INFANTS; MATERNAL SUPPLEMENTATION; EICOSAPENTAENOIC ACID; PREPULSE INHIBITION; DHA SUPPLEMENTATION;
D O I
10.1016/j.jnutbio.2014.08.002
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Maternal intake of omega-3 polyunsaturated fatty acids (n-3 PUFA) is critical during perinatal development of the brain. Docosahexaenoic acid (DHA) is the most abundant n-3 PUFA in the brain and influences neuronal membrane function and neuroprotection. The present study aims to assess the effect of dietary n-3 PUFA availability during the gestational and postnatal period on cognition, brain metabolism and neurohistology in C57BL/6J mice. Female wild-type C57BL/6J mice at day 0 of gestation were randomly assigned to either an n-3 PUFA deficient diet (0.05% of total fatty acids) or an n-3 PUFA adequate diet (3.83% of total fatty acids) containing preformed DHA and its precursor a-linolenic acid. Male offspring remained on diet and performed cognitive tests during puberty and adulthood. In adulthood, animals underwent P-31 magnetic resonance spectroscopy to assess brain energy metabolites. Thereafter, biochemical and immunohistochemical analyses were performed assessing inflammation, neurogenesis and synaptic plasticity. Compared to the n-3 PUFA deficient group, pubertal n-3 PUFA adequate fed mice demonstrated increased motor coordination. Adult n-3 PUFA adequate fed mice exhibited increased exploratory behavior, sensorimotor integration and spatial memory, while neurogenesis in the hippocampus was decreased. Selected brain regions of n-3 PUFA adequate fed mice contained significantly lower levels of arachidonic acid and higher levels of DHA and dihomo-gamma-linolenic acid. Our data suggest that dietary n-3 PUFA can modify neural maturation and enhance brain functioning in healthy C57BL/6J mice. This indicates that availability of n-3 PUFA in infant diet during early development may have a significant impact on brain development. (C) 2015 Elsevier Inc. All rights reserved.
引用
收藏
页码:24 / 35
页数:12
相关论文
共 88 条
[1]   Temporal changes in dietary fats:: Role of n-6 polyunsaturated fatty acids in excessive adipose tissue development and relationship to obesity [J].
Ailhaud, Gerard ;
Massiera, Florence ;
Weill, Pierre ;
Legrand, Philippe ;
Alessandri, Jean-Marc ;
Guesnet, Philippe .
PROGRESS IN LIPID RESEARCH, 2006, 45 (03) :203-236
[2]   Age dependence of strain determinant on mice motor coordination [J].
Bearzatto, B ;
Servais, L ;
Cheron, G ;
Schiffmann, SN .
BRAIN RESEARCH, 2005, 1039 (1-2) :37-42
[3]   Ethyl-eicosapentaenoic acid in first-episode psychosis. A 1H-MRS study [J].
Berger, Gregor E. ;
Wood, Stephen J. ;
Wellard, R. Mark ;
Proffitt, Tina M. ;
McConchie, Mirabel ;
Amminger, G. Paul ;
Jackson, Graeme D. ;
Velakoulis, Dennis ;
Pantelis, Christos ;
McGorry, Patrick D. .
NEUROPSYCHOPHARMACOLOGY, 2008, 33 (10) :2467-2473
[4]   A randomized controlled trial of early dietary supply of long-chain polyunsaturated fatty acids and mental development in term infants [J].
Birch, EE ;
Garfield, S ;
Hoffman, DR ;
Uauy, R ;
Birch, DG .
DEVELOPMENTAL MEDICINE AND CHILD NEUROLOGY, 2000, 42 (03) :174-181
[5]   Visual acuity and cognitive outcomes at 4 years of age in a double-blind, randomized trial of long-chain polyunsaturated fatty acid-supplemented infant formula [J].
Birch, Eileen E. ;
Garfield, Sharon ;
Castaneda, Yolanda ;
Hughbanks-Wheaton, Dianna ;
Uauy, Ricardo ;
Hoffman, Dennis .
EARLY HUMAN DEVELOPMENT, 2007, 83 (05) :279-284
[6]   The DIAMOND (DHA Intake And Measurement Of Neural Development) Study: a double-masked, randomized controlled clinical trial of the maturation of infant visual acuity as a function of the dietary level of docosahexaenoic acid [J].
Birch, Eileen E. ;
Carlson, Susan E. ;
Hoffman, Dennis R. ;
Fitzgerald-Gustafson, Kathleen M. ;
Fu, Valeria L. N. ;
Drover, James R. ;
Castaneda, Yolanda S. ;
Minns, Laura ;
Wheaton, Dianna K. H. ;
Mundy, David ;
Marunycz, John ;
Diersen-Schade, Deborah A. .
AMERICAN JOURNAL OF CLINICAL NUTRITION, 2010, 91 (04) :848-859
[7]   Relationship between umbilical cord essential fatty acid content and the quality of general movements of healthy term infants at 3 months [J].
Bouwstra, H ;
Dijck-Brouwer, DJ ;
Decsi, T ;
Boehm, G ;
Boersma, ER ;
Muskiet, FA ;
Hadders-Algra, M .
PEDIATRIC RESEARCH, 2006, 59 (05) :717-722
[8]   Animal studies of the functional consequences of suboptimal polyunsaturated fatty acid status during pregnancy, lactation and early post-natal life [J].
Brenna, J. Thomas .
MATERNAL AND CHILD NUTRITION, 2011, 7 :59-79
[9]   α-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans [J].
Brenna, J. Thomas ;
Salem, Norman, Jr. ;
Sinclair, Andrew J. ;
Cunnane, Stephen C. .
PROSTAGLANDINS LEUKOTRIENES AND ESSENTIAL FATTY ACIDS, 2009, 80 (2-3) :85-91
[10]   Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function [J].
Cao, Dehua ;
Kevala, Karl ;
Kim, Jeffrey ;
Moon, Hyun-Seuk ;
Jun, Sang Beom ;
Lovinger, David ;
Kim, Hee-Yong .
JOURNAL OF NEUROCHEMISTRY, 2009, 111 (02) :510-521