Effect of a supplement rich in linolenic acid, added to the diet of gestating and lactating goats, on the sensitivity to stress and learning ability of their offspring

Applied Animal Behaviour Science

Volumn 114, Issue 3-4, 2008, Pages 373-394

  Duvaux Ponter, Christine ^a   Rigalma, Karim ^a   Roussel Huchette, Sabine ^a   Schawlb, Yvonne ^a,b   Ponter, Andrew A ^b  

^a AGROPARISTECH   (France)

^b ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

Author keywords

Behaviour; Emotional reactivity; Fatty acid transfer; Fetus; Goat kids; Learning; Linolenic acid

Indexed keywords

BEHAVIORAL ECOLOGY; BLOOD; BRAIN; FATTY ACID; FOOD SUPPLEMENTATION; GOAT; HERB; LACTATION; LEARNING; MILK; NEONATE; PARTURITION; PREGNANCY; PSYCHOLOGY; SECRETION; VOCALIZATION;

BRASSICA NAPUS; CAPRA HIRCUS; RODENTIA;

EID: 52949130951     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2008.01.021     Document Type: Article

References (77)

1. AFZ-INRA Tables. Tables de composition et de valeur nutritive des matières premières destinées aux animaux d'élevage (2002), INRA Editions, Paris
2. Alessandri J.M., Guesnet P., Vancassel S., Astorg P., Denis I., Langelier B., Aid S., Poumes-Ballihaut C., Champeil-Potokar G., and Lavialle M. Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life. Reprod. Nutr. Dev. 44 (2004) 509-538
3. Archer J.E., and Blackman D.E. Prenatal psychological stress and offspring behaviour in rats and mice. Dev. Psychobiol. 43 (1970) 193-248
4. Beausoleil N.J., Stafford K.J., and Mellor D.J. Sheep show more aversion to a dog than to a human in an arena test. Appl. Anim. Behav. Sci. 91 (2005) 219-232
5. Bérubé L. Terminologie de neuropsychologie et de neurologie du comportement (1991), Les Éditions de la Chenelière Inc., Montréal
6. Boissy A., and Le Neindre P. Behavioral, cardiac and cortisol responses to brief peer separation and reunion in cattle. Physiol. Behav. 61 (1997) 693-699
7. Bourre J.M., Dumont O., Piciotti M., Clément M., Chaudière J., Bonneil M., Nalbone G., Lafont H., Pascal G., and Durand G. Essentiality of omega 3 fatty acids for brain structure and function. World Rev. Nutr. Diet. 66 (1991) 103-117
8. Bourre J.M., Francois M., Youyou A., Dumont O., Piciotti M., Pascal G., and Durand G. The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J. Nutr. 119 (1989) 1880-1892
9. Broom D.M., and Johnson K.G. Stress and Animal Welfare (1993), Chapman & Hall, London
10. Capper J.L., Wilkinson R.G., Mackenzie A.M., and Sinclair L.A. Polyunsaturated fatty acid supplementation during pregnancy alters neonatal behavior in sheep. J. Nutr. 136 (2006) 397-403
11. Carrié I., Clément M., de Javel D., Francès H., and Bourre J.M. Learning deficits in first generation OF1 mice deficient in (n - 3) polyunsaturated fatty acids do not result from visual alteration. Neurosci. Lett. 266 (1999) 69-72
12. Carrié I., Clément M., de Javel D., Francès H., and Bourre J.M. Phospholipid supplementation reverses behavioral and biochemical alterations induced by n - 3 polyunsaturated fatty acid deficiency in mice. J. Lipid Res. 41 (2000) 473-480
13. Chambaz J., Ravel D., Manier M.C., Pepin D., Mulliez N., and Bereziat G. Essential fatty-acids interconversion in the human-fetal liver. Biol. Neonate 47 (1985) 136-140
14. Chardigny J.M., Bonhomme B., Sébédio J.L., Juaneda P., Vatele J.M., Doly M., and Grandgirarda A. Effects of dietary n - 3 polyunsaturated fatty acids on the rat electroretinogram. Nutr. Res. 18 (1998) 1711-1721
15. Crawford M.A., Hassam A.G., and Williams G. Essential fatty acids and fetal brain growth. Lancet 1 (1976) 452-453
16. de la Presa Owens S., and Innis S.M. Docosahexaenoic and arachidonic acid prevent a decrease in dopaminergic and serotoninergic neurotransmitters in frontal cortex caused by a linoleic and alpha-linolenic acid deficient diet in formula-fed piglets. J. Nutr. 129 (1999) 2088-2093
17. de Passillé A.M., Rushen J., and Martin F. Interpreting the behaviour of calves in an open-field test: a factor analysis. Appl. Anim. Behav. Sci. 45 (1995) 201-213
18. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Hum. Dev. 3 (1979) 79-83
19. Dutta-Roy A.K. Transport mechanisms for long-chain polyunsaturated fatty acids in the human placenta. Am. J. Clin. Nutr. 71 (2000) 315S-322S
20. Duvaux-Ponter C., Roussel S., Tessier J., Sauvant D., Ficheux C., and Boissy A. Physiological effects of repeated transport in pregnant goats and their offspring. Anim. Res. 52 (2003) 553-566
21. Duvaux-Ponter C., Tournié M., Detrimont L., Clément F., Ficheux C., and Ponter A.A. A supplement of linolenic acid in the diet of mares modifies fatty acid composition of mammary secretions but does not improve the acquisition of passive immunity in the foal. Anim. Sci. 78 (2004) 399-407
22. Edelstone D.I., Rudolph A.M., and Heymann M.A. Liver and ductus venosus blood flows in fetal lambs in utero. Circ. Res. 42 (1978) 426-433
23. Farkas T., Kitajka K., Fodor E., Csengeri I., Lahdes E., Yeo Y.K., Krasznai Z., and Halver J.E. Docosahexaenoic acid-containing phospholipid molecular species in brains of vertebrates. Proc. Natl. Acad. Sci. 97 (2000) 6362-6366
24. Fisher A., and Matthews L. The social behaviour of sheep. In: Keeling L.J., and Gonyou H.W. (Eds). Social Behaviour in Farm Animals (2001), CABI Publishing, Wallingford 211-245
25. Francès H., Monier C., and Bourre J.M. Effects of dietary alpha-linolenic acid deficiency on neuromuscular and cognitive functions in mice. Life Sci. 57 (1995) 1935-1947
26. Francès H., Monier C., Clément M., Lecorsier A., Debray M., and Bourre J.M. Effect of dietary alpha-linolenic acid deficiency on habituation. Life Sci. 58 (1996) 1805-1816
27. Friend T.H., Gwazdauskas F.G., and Polan C.E. Change in adrenal response from free stall competition. J. Dairy Sci. 62 (1979) 768-771
28. Gamoh S., Hashimoto M., Sugioka K., Shahdat H.M., Hata N., Misawa Y., and Masumura S. Chronic administration of docosahexaenoic acid improves reference memory-related learning ability in young rats. Neuroscience 93 (1999) 237-241
29. Gentle K.L., Scott-Baird E., Pickard R.M., Beard A.P., Butler G., and Edwards S.A. Supplementation of pregnant ewe diets with docosahexaenoic acid reduces lamb suckling latency. Proceedings of the 40th International Congress of the ISAE. University of Bristol, August 8th-12th (2006) 130
30. Green P., and Yavin E. Elongation, desaturation, and esterification of essential fatty acids by fetal rat brain in vivo. J. Lipid Res. 34 (1993) 2099-2107
31. Hagen K., and Broom D.M. Cattle discriminate between individual familiar herd members in a learning experiment. Appl. Anim. Behav. Sci. 82 (2003) 13-28
32. Haggarty P. Effect of placental function on fatty acid requirements during pregnancy. Eur. J. Clin. Nutr. 58 (2004) 1559-1570
33. Hansen H.S., and Olsen S.F. Dietary (n - 3)-fatty acids, prostaglandins, and prolonged gestation in humans. Prog. Clin. Biol. Res. 282 (1988) 305-317
34. Heird J.C., Lokey C.E., and Cogan D.C. Repeatability and comparison of two maze tests to measure learning ability in horses. Appl. Anim. Behav. Sci. 16 (1986) 103-119
35. Ikemoto A., Ohishi M., Sato Y., Hata N., Misawa Y., Fujii Y., and Okuyama H. 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
36. INRA. Alimentation des Bovins, Ovins, Caprins (1988), INRA, Paris p. 471
37. Jainudeen M.R., and Hafez E.S.E. Gestation, prenatal physiology, and parturition. In: Hafez E.S.E. (Ed). Reproduction in Farm Animals (2000), Lippincott W. & Wilkins, Philadelphia 140-155
38. Lickliter R.E. Activity patterns and companion preferences of domestic goat kids. Appl. Anim. Behav. Sci. 19 (1987) 137-145
39. Lim S., and Suzuki H. Changes in maze behavior of mice occur after sufficient accumulation of docosahexaenoic acid in brain. J. Nutr. 131 (2001) 319-324
40. Mattos R., Staples C.R., and Thatcher W.W. Effects of dietary fatty acids on reproduction in ruminants. Rev. Reprod. 5 (2000) 38-45
41. Mendl M. Performing under pressure: stress and cognitive function. Appl. Anim. Behav. Sci. 65 (1999) 221-244
42. Moriguchi T., Greiner R.S., and Salem Jr. N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J. Neurochem. 75 (2000) 2563-2573
43. Murayama K., Yoneya S., Miyauchi O., Adachi-Usami E., and Nishikawa M. Fish oil (polyunsaturated fatty acid) prevents ischemic-induced injury in the mammalian retina. Exp. Eye Res. 74 (2002) 671-676
44. Noble R.C., Shand J.H., and Calvert D.T. The role of the placenta in the supply of essential fatty acids to the fetal sheep: studies of lipid compositions at term. Placenta 3 (1982) 287-295
45. Noble R.C., Shand J.H., and Christie W.W. Synthesis of C20 and C22 polyunsaturated fatty acids by the placenta of the sheep. Biol. Neonate 47 (1985) 333-338
46. Olsen S.F., Hansen H.S., Sorensen T.I.A., Jensen B., Secher N.J., Sommer S., and Knudsen L.B. Intake of marine fat, rich in (n - 3)-polyunsaturated fatty acids, may increase birth-weight by prolonging gestation. Lancet 2 (1986) 367-369
47. Osadchuk L.V., Braastad B.O., Hovland A.L., and Bakken M. Handling during pregnancy in the blue fox (Alopex lagopus): the influence on the fetal pituitary-adrenal axis. Gen. Comp. Endocrinol. 123 (2001) 100-110
48. Parrott R.F., Misson B.H., and de la Riva C.F. Differential stressor effects on the concentrations of cortisol, prolactin and catecholamines in the blood of sheep. Res. Vet. Sci. 56 (1994) 234-239
49. Ponter A.A., Douar C., Mialot J.P., Benoit-Valiergue H., and Grimard B. Effect of underfeeding post-partum Charolais beef cows on composition of plasma non-esterified fatty acids. Anim. Sci. 71 (2000) 243-252
50. Price E.O., and Thos J. Behavioral responses to short-term social isolation in sheep and goats. Appl. Anim. Ethol. 6 (1980) 331-339
51. Rajion M.A., McLean J.G., and Cahill R.N. Essential fatty acids in the fetal and newborn lamb. Aust. J. Biol. Sci. 38 (1985) 33-40
52. Redbo I. Relations between oral stereotypes, open-field behavior, and pituitary-adrenal system in growing dairy cattle. Physiol. Behav. 64 (1998) 273-278
53. Romeyer A., and Bouissou M.F. Assessment of fear reactions in domestic sheep, and influence of breed and rearing conditions. Appl. Anim. Behav. Sci. 34 (1992) 93-119
54. Roussel S., Boissy A., Montigny D., Hemsworth P.H., and Duvaux-Ponter C. Gender-specific effects of prenatal stress on emotional reactivity and stress physiology of goat kids. Horm. Behav. 47 (2005) 256-266
55. Ruiz-Miranda C.R., and Callard M. Effects of the presence of the mother on responses of domestic goat kids (Capra hircus) to novel inanimate objects and humans. Appl. Anim. Behav. Sci. 33 (1992) 277-285
56. Sanchez C. Stress-induced vocalisation in adult animals. A valid model of anxiety?. Eur. J. Pharmacol. 463 (2002) 133-143
57. Sandem A.I., Janczak A.M., and Braastad B.O. A short note on effects of exposure to a novel stimulus (umbrella) on behaviour and percentage of eye-white in cows. Appl. Anim. Behav. Sci. 89 (2004) 309-314
58. Shand J.H., and Noble R.C. Delta 9- and delta 6-desaturase activities of the ovine placenta and their role in the supply of fatty acids to the fetus. Biol. Neonate 36 (1979) 298-304
59. Sukhija P.S., and Palmquist D.L. Rapid method for determination of total fatty-acid content and composition of feedstuffs and feces. J. Agric. Food Chem. 36 (1988) 1202-1206
60. 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. Behav. Brain Res. 131 (2002) 193-203
61. Torres-Hernandez G., and Hohenboken W. An attempt to assess traits of emotionality in crossbred ewes. Appl. Anim. Ethol. 5 (1979) 71-83
62. Umezawa M., Kogishi K., Tojo H., Yoshimura S., Seriu N., Ohta A., Takeda T., and Hosokawa M. High-linoleate and high-alpha-linolenate diets affect learning ability and natural behavior in SAMR1 mice. J. Nutr. 129 (1999) 431-437
63. Vandenheede M., and Bouissou M.F. Sex differences in fear reactions in sheep. Appl. Anim. Behav. Sci. 37 (1993) 39-55
64. Veissier I., Boissy A., de Passillé A.M., Rushen J., van Reenen C.G., Roussel S., Andanson S., and Pradel P. Calves' responses to repeated social regrouping and relocation. J. Anim. Sci. 79 (2001) 2580-2593
65. Veissier I., and Stefanova I. Learning to suckle from an artificial teat within groups of lambs: influence of a knowledgeable partner. Behav. Process. 30 (1993) 75-82
66. Velzing-Aarts F.V., van der Klis F.R., van der Dijs F.P., and Muskiet F.A. Umbilical vessels of preeclamptic women have low contents of both n - 3 and n - 6 long-chain polyunsaturated fatty acids. Am. J. Clin. Nutr. 69 (1999) 293-298
67. Wainwright P.E., Xing H.C., Mutsaers L., McCutcheon D., and Kyle D. Arachidonic acid offsets the effects on mouse brain and behavior of a diet with a low (n - 6):(n - 3) ratio and very high levels of docosahexaenoic acid. J. Nutr. 127 (1997) 184-193
68. Wainwright P.E., Xing H.C., Ward G.R., Huang Y.S., Bobik E., Auestad N., and Montalto M. Water maze performance is unaffected in artificially reared rats fed diets supplemented with arachidonic acid and docosahexaenoic acid. J. Nutr. 129 (1999) 1079-1089
69. Walker C.D. Nutritional aspects modulating brain development and the responses to stress in early neonatal life. Prog. Neuropsychopharmacol. Biol. Psychiatry 29 (2005) 1249-1263
70. Yamamoto N., Hashimoto A., Takemoto Y., Okuyama H., Nomura M., Kitajima R., Togashi T., and Tamai Y. Effect of the dietary alpha-linolenate/linoleate balance on lipid compositions and learning ability of rats. II. Discrimination process, extinction process, and glycolipid compositions. J. Lipid Res. 29 (1988) 1013-1021
71. Yamamoto N., Saitoh M., Moriuchi A., Nomura M., and Okuyama H. Effect of dietary alpha-linolenate/linoleate balance on brain lipid compositions and learning ability of rats. J. Lipid Res. 28 (1987) 144-151
72. Yehuda S., and Carasso R.L. Modulation of learning, pain thresholds, and thermoregulation in the rat by preparations of free purified a-linolenic and linoleic acids: determination of the optimal w3-to-w6 ratio. Proc. Natl. Acad. Sci. 90 (1993) 10345-10349
73. Yehuda S., Rabinovitz S., Carasso R.L., and Mostofsky D.I. Fatty acid mixture counters stress changes in cortisol, cholesterol, and impair learning. Int. J. Neurosci. 101 (2000) 73-87
74. Yehuda S., Rabinovitz S., and Mostofsky D.I. Essential fatty acids are mediators of brain biochemistry and cognitive functions. J. Neurosci. Res. 56 (1999) 565-570
75. Yehuda S., Rabinovitz S., Mostofsky D.I., Huberman M., and Sredni B. Essential fatty acid preparation improves biochemical and cognitive functions in experimental allergic encephalomyelitis rats. Eur. J. Pharmacol. 328 (1997) 23-29
76. Yeom K.-H., Trierum G.V., Lee K.-W., and Beynen A.C. Influence of feeding a milk replacer deficient in [alpha]-linolenic acid on fatty acid composition of various tissues in goat kids. Small Ruminant Res. 48 (2003) 141-148
77. Zimmerman P.H., and Koene P. The effect of frustrative nonreward on vocalisations and behaviour in the laying hen, Gallus gallus domesticus. Behav. Process. 44 (1998) 73-79