An n-3 Fatty Acid Deficiency Impairs Rat Spatial Learning in the Barnes Maze

Behavioral Neuroscience

Volumn 123, Issue 1, 2009, Pages 196-205

  Fedorova, Irina ^a   Hussein, Nahed ^a   Baumann, Michael H ^b   Di Martino, Carmine ^a   Salem Jr , Norman ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Barnes maze; DHA; docosahexaenoic acid; n 3 fatty acid deficiency; reversal learning

Indexed keywords

ANALYSIS OF VARIANCE; ANIMALS; BRAIN; BRAIN CHEMISTRY; DIETARY FATS; DOCOSAHEXAENOIC ACIDS; EXPLORATORY BEHAVIOR; FATTY ACIDS, OMEGA-3; FEMALE; MAZE LEARNING; NEUROTRANSMITTER AGENTS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, LONG-EVANS; REACTION TIME; SPATIAL BEHAVIOR;

EID: 60549090998     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/a0013801     Document Type: Article

References (63)

1. Aid S., Vancassel S., Poumes-Ballihaunt C., Chalon S., Guesnet P., and Lavialle M. Effect of a diet-induced n-3 PUFA depletion on cholinergic parameters in the rat hippocampus. Journal of Lipid Research 44 (2003) 1545-1551
2. Annett L.E., McGregor A., and Robbins T.W. The effects of ibotenic acid lesions of the nucleus accumbens on spatial learning and extinction in the rat. Behavioral Brain Research 31 (1989) 231-242
3. Arendash G.W., Jensen M.T., Salem Jr. N., Hussein N., Cracchiolo J., Dickson A., et al. A diet high in omega-3 fatty acids does not improve or protect cognitive performance in Alzheimer's transgenic mice. Neuroscience 149 (2007) 286-302
4. Bach M.E., Hawkins R.D., Osman M., Kandel E.R., and Mayford M. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell 81 (1995) 905-915
5. Barnes C.A. Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. Journal of Comparative Physiology 93 (1979) 74-104
6. Baumann M.H., Ayestas M.A., and Rothman R.B. Functional consequences of central serotonin depletion produced by repeated fenfluramine administration in rats. Journal of Neuroscience 18 (1998) 9069-9077
7. Block A.E., Dhanji H., Thompson-Tardif S.F., and Floresco S.B. Thalamic-prefrontal cortical-ventral striatal circuitry mediates dissociable component of strategy set-shifting. Cerebral Cortex 17 (2007) 1625-1636
8. Bourre J.M., Dumont O.S., Piciotti M.J., Pascal G.A., and Durand G.A. Dietary alpha-linolenic acid deficiency in adult rats for 7 months does not alter brain docosahexaenoic acid content, in contrast to liver, heart and testes. Biochimica et Biopysica Acta 1124 (1992) 119-122
9. Calon F., Lim G.P., Yang F., Morihara T., Teter B., Ubeda O., et al. Docosahesaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 43 (2004) 633-645
10. Catalan J., Moriguchi T., Slotnick B., Murthy M., Greiner R.S., and Salem Jr. N. Cognitive deficits in docosahexaenoic acid-deficient rats. Behavioral Neuroscience 116 (2002) 1022-1031
11. Chalon S. Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins, Leukotrienes and Essential Fatty Acids 75 (2006) 259-269
12. Clandinin M.T., Chappel J.E., Leong S., Heim T., Swyer P.R., and Chance G.W. Intrauterine fatty acid accretion rates in human brain: Implications for fatty acid requirements. Early Human Development 4 (1980) 121-129
13. Delion S., Chalon S., Guilloteau D., Besnard J.C., and Durand G. α-linolenic acid dietary deficiency alters age-related changes of dopaminergic and serotoninergic neurotransmission in the rat frontal cortex. Journal of Neurochemistry 66 (1996) 1582-1591
14. Delion S., Chalon S., Herault J., Guilloteau D., Besnard J.C., and Durand G. Chronic dietary alpha-linolenic acid deficiency alters dopaminergic and serotoninergic neurotransmission in rats. Journal of Nutrition 124 (1994) 2466-2476
15. Deutch A.Y., Tam S.-Y., and Roth R.H. Footshock and conditioned stress increase 3,4-dihydroxyphenylacetic acid (DOPAC) in the ventral tegmental area but not substantia nigra. Brain Research 333 (1985) 143-146
16. Fedorova I., and Salem Jr. N. Omega-3 fatty acids and rodent behavior. Prostaglandins, Leukotrienes and Essential Fatty Acids 75 (2006) 271-289
17. Folch J., Lees M., and Sloane-Stanley G. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226 (1957) 497-506
18. Frances H., Monier C., Clement M., Lecorsier A., Debray M., and Bourre J.M. Effect of dietary α-linolenic acid deficiency on habituation. Life Science 58 (1996) 1805-1816
19. Galli C., Trzeciak H.I., and Paoletti R. Effects of dietary fatty acids on the fatty acid composition of brain ethanolamine phosphoglyceride: Reciprocal replacement of n-6 and n-3 polyunsaturated fatty acids. Biochimica et Biopysica Acta 248 (1971) 449-454
20. Green P., and Yavin E. Modulation of fetal rat brain and liver phospholipid content by intraamniotic ethyl docosahexaenoate administration. Journal of Neurochemistry 65 (1995) 2555-2560
21. Greiner R.S., Catalan J.N., Moriguchi T., and Salem Jr. N. Docosapentaenoic acid does not completely replace DHA in n-3 FA-deficient rats during early development. Lipids 38 (2003) 431-435
22. Greiner R.S., Moriguchi T., Hutton A., Slotnik B., and Salem Jr. N. Rats with low levels of brain docosahexaenoic acid show impaired performance in olfactory-based and spatial learning tasks. Lipids 34 (1999) 239-243
23. Greiner R.S., Moriguchi T., Slotnick B.M., Hutton A., and Salem Jr. N. Olfactory discrimination deficits in n-3 fatty acid-deficient rats. Physiology & Behavior 72 (2001) 379-385
24. Havekes R., Timmer M., and Van der Zee E.A. Regional differences in hippocampal PKA immunoreactivity after training and reversal training in a spatial Y-maze task. Hippocampus 17 (2007) 338-348
25. Hussain R.J., Stumpo D.J., Blackshear P.J., Lenox R.H., Abel T., and McNamara R.K. Hippocampus 16 (2006) 495-503
26. Ikemoto S. Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Research Reviews 56 (2007) 27-78
27. Jarrard L.E. On the role of the hippocampus in learning and memory in the rat. Behavioral and Neural Biology 60 (1993) 9-26
28. Kalivas P.W., Churchill L., and Romanides A. Involvement of the pallidal-thalamocortical circuit in adaptive behavior. Annals of the New York Academy of Sciences 877 (1999) 64-70
29. Kesner R.P. Subregional analysis of mnemonic functions of the prefrontal cortex in the rat. Psychobiology 28 (2000) 219-228
30. Kodas E., Galineau L., Bodard S., Vancassel S., Guilloteau D., Besnard J.C., and Chalon S. Serotoninergic neurotransmission is affected by n-3 polyunsaturated fatty acids in the rat. Journal of Neurochemistry 89 (2004) 695-702
31. Kodas E., Page G., Zimmer L., Vancassel S., Guilloteau D., Durand G., and Chalon S. Neither the density nor the function of striatal dopamine transporters were influenced by chronic n-3 polyunsaturated fatty acid deficiency in rodents. Neuroscience Letters 321 (2002) 95-99
32. Kuperstein F., Yakubov E., Dinerman P., Gil S., Eylam R., Salem Jr. N., and Yavin E. Overexpression of dopamine receptor genes and their products in the postnatal rat brain following maternal n-3 fatty acid dietary deficiency. Journal of Neurochemistry 95 (2005) 1550-1562
33. Lim G.P., Calon F., Morihara T., Yang F., Teter B., Ubeda O., et al. A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. Journal of Neuroscience 25 (2005) 3032-3040
34. Lim S.-Y., Hoshiba J., Moriguchi T., and Salem Jr. N. n-3 fatty acid deficiency induced by a modified artificial rearing method leads to poorer performance in spatial learning tasks. Pediatric Research 58 (2005) 741-748
35. Lim S.-Y., Hoshiba J., and Salem Jr. N. An extraordinary degree of structural specificity is required in neural phospholipids for optimal brain function: N-6 docosapentaenoic acid substitution for docosahexaenoic acid leads to a loss in spatial task performance. Journal of Neurochemistry 95 (2005) 848-857
36. Louilot A., Taghzouti K., Simon H., and Le Moal M. Limbic system, basal ganglia, and dopaminergic neurons. Executive and regulatory neurons and their role in the organization of behavior. Brain, Behavior and Evolution 33 (1989) 157-161
37. Mannisto P.T. Aminergic regulation of neuroendocrine function: Theoretical background and clinical examples. Nuclear Medicine and Biology 65 (1987) 121-126
38. Martinez M. Tissue levels of polyunsaturated fatty acids during early human development. Journal of Pediatrics 120 (1992) S129-138
39. Mitchell D.C., Niu S.-L., and Litman B.J. DHA-rich phospholipids optimize G-protein-coupled signaling. Journal of Pediatrics 143 (2003) S80-S86
40. Mohrhauer H., and Holman R.T. Alteration of the fatty acid composition of brain lipids by varying levels of dietary essential fatty acids. Journal of Neurochemistry 10 (1963) 523-530
41. Moore K.E., Demarest K.T., and Lookingland K.J. Stress, prolactin and hypothalamic dopamine neurons. Neuropharmacology 26 (1987) 801-808
42. Moriguchi T., Greiner R.S., and Salem Jr. N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. Journal of Neurochemistry 75 (2000) 2563-2573
43. Moriguchi T., Lim S.-Y., Greiner R., Lefkowitz W., Loewke J., Hoshiba J., and Salem Jr. N. Effects of an n-3-deficient diet on brain, retina and liver fatty acyl composition in artificially reared rats. Journal of Lipid Research 45 (2004) 1437-1445
44. Moriguchi T., and Salem Jr. N. Recovery of brain docosahexaenoate leads to recovery of spatial task performance. Journal of Neurochemistry 87 (2003) 297-309
45. Niu S.L., Mitchell D.C., Lim S.-Y., Wen Z.M., Kim H.Y., Salem Jr. N., and Litman B.J. Reduced G protein-coupled signaling efficiency in retinal rod outer segments in response to n-3 fatty acid deficiency. Journal of Biological Chemistry 279 (2004) 31098-31104
46. Noguchi T., Yoshida Y., and Chiba S. Effects of psychological stress on monoamine systems in subregions of the frontal cortex and nucleus accumbens of the rat. Brain Research 916 (2001) 91-100
47. Okaniwa Y., Yuasa S., Yamamoto N., Watanabe S., Kobayashi T., Okuyama H., et al. A high linoleate and a high α-linolenate diet induced changes in learning behavior of rats. Effects of a shift in diets and reversal of training stimuli. Biological & Pharmaceutical Bulletin 19 (1996) 536-540
48. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (2005), Elsevier, New York
49. Roth R.H., Tam S.-Y., Ida Y., Yang J.-X., and Deutch A.Y. Stress and the mesocorticolimbic dopamine systems. Annals of the New York Academy of Sciences 537 (1988) 138-147
50. Rots N.Y., Cools A.R., Oitzl M.S., de Jong J., Sutanto W., and de Kloet E.R. Divergent prolation and pituitary-adrenal activity in rats bred selectively for different dopamine responsiveness. Endocrinology 137 (1996) 1678-1686
51. Salem Jr. N. Omega-3 fatty acids: Molecular and biochemical aspects. In: Spiller G.A., and Scala J. (Eds). Current topics in nutrition and disease: New protective roles for selected nutrients (1989), Alan R Liss, New York 109-228
52. Salem Jr. N., Kim H.-Y., and Yergey J.A. Docosahexaenoic acid: Membrane function and metabolism. In: Simopoulos A.P., Kifer R.R., and Martin R. (Eds). The health effects of polyunsaturates in seafood (1986), Academic Press, New York 263-317
53. Salem Jr. N., Moriguchi T., Greiner R.S., McBride K., Ahmad A., Catalan J.N., and Slotnik B. Alterations in brain function after loss of docosahexaenoate due to dietary restriction of n-3 fatty acids. Journal of Molecular Neuroscience 16 (2001) 299-307 317-321
54. Salem Jr. N., Reyzer M., and Karanian J. Losses of arachidonic acid in rat liver after alcohol inhalation. Lipids 31 (1996) S153-S156
55. Schultz W. Multiple dopamine functions at different time courses. Annual Review of Neuroscience 30 (2007) 259-288
56. Taghzouti K., Louilot A., Herman J.P., Moal M.L., and Simon H. Alternation behavior, spatial discrimination, and reversal disturbances following 6-hydroxydopamine lesions in the nucleus accumbens of the rat. Behavioral and Neural Biology 44 (1985) 354-363
57. Takeuchi T., Fukumoto Y., and Harada E. Influence of a dietary n-3 fatty acid deficiency on the cerebral catecholamine contents, EEG and learning ability in rat. Behavioral Brain Research 131 (2002) 193-203
58. Takeuchi T., Iwanaga M., and Harada E. Possible regulatory mechanism of DHA-induced anti-stress reaction in rats. Brain Research 964 (2003) 136-143
59. Tinoco J. Dietary requirements and functions of alpha-linolenic acid in animals. Progress in Lipid Research 21 (1982) 1-45
60. Weisinger H.S., Vingrys A.J., and Sinclair A.J. Effect of dietary n-3 deficiency on the electroretinogram in the guinea pig. Annals of Nutrition and Metabolism 40 (1996) 91-98
61. Zimmer L., Delion-Vancassel S., Durand G., Guilloteau D., Bodard S., Besnard J.C., and Chalon S. Modification of dopamine neurotransmission in the nucleus accumbens of rats deficient in n-3 polyunsaturated fatty acids. Journal of Lipid Research 41 (2000) 32-40
62. Zimmer L., Hembert S., Durand G., Breton P., Guilloteau D., Besnard J.C., and Chalon S. Chronic n-3 polyunsaturated fatty acid diet-deficiency acts on dopamine metabolism in the rat frontal cortex: A microdialysis study. Neuroscience Letters 240 (1998) 177-181
63. Zimmer L., Vancassel S., Cantagrel S., Breton P., Delamanche S., Guilloteau D., et al. The dopamine mesocorticolimbic pathway is affected by deficiency in n-3 polyunsaturated fatty acids. American Journal of Clinical Nutrition 75 (2002) 662-667