Difference between revisions of "Effect of Diet on Behaviour"

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==Overview==
 
==Overview==
 
Several aspects of feeding can have an effect on behaviour:
 
Several aspects of feeding can have an effect on behaviour:
−
* Dietary composition: Nutrient composition, palatability, method of preservation (raw, dried, moist).
+
* Dietary composition: Nutrient composition, palatability, method of preservation (raw, dried, moist)
−
* Timing of access: Meal-feeding, on demand feeding, ad-lib feeding.
+
* Timing of access: Meal-feeding, on demand feeding, ad-lib feeding
 
* Type of access: Bowl, simulated foraging (activity feeding)
 
* Type of access: Bowl, simulated foraging (activity feeding)
  
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It is particularly important to ensure appropriate timing and type of access that satisfies species-specific time and energy allocation; cats and dogs would normally spent large parts of the day on foraging behaviour. A lack of opportunity to do this can lead to welfare and behaviour problems.
 
It is particularly important to ensure appropriate timing and type of access that satisfies species-specific time and energy allocation; cats and dogs would normally spent large parts of the day on foraging behaviour. A lack of opportunity to do this can lead to welfare and behaviour problems.
  
−
* Feral and wild cats allocate 6-8 hours every day on foraging (searching for prey and hunting). They eat 10-20 small meals each day, and return to hunting dirtily after consuming a meal. Frequency of hunting is not affected by satiation; cats will hunt whether hungry or not, but latency to kill-bite delivery is reduced when cats are hungry.
+
* Feral and wild cats allocate 6-8 hours every day on foraging (searching for prey and hunting). They eat 10-20 small meals each day, and return to [[Feline Predatory Behaviour|hunting]] after consuming a meal. Frequency of hunting is not affected by satiation; cats will hunt whether hungry or not, but latency to kill-bite delivery is reduced when cats are hungry.
 
* Feral dogs and wolves hunt more sporadically, as opportunities arise, but also spend several hours each day foraging (often searching for carrion and non-meat food).
 
* Feral dogs and wolves hunt more sporadically, as opportunities arise, but also spend several hours each day foraging (often searching for carrion and non-meat food).
  
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====Protein, Tryptophan and Carbohydrate====
 
====Protein, Tryptophan and Carbohydrate====
−
l-Tryptophan is large neutral amino acid (LNAA) which acts as a precursor for serotonin. l-Tryptophan is actively transported across the blood brain barrier by the L1 carrier<ref>Hawkins, R.A., O’Kane, R.L., Simpson, I.A., Vin ̃az, J.R. (2006) Structure of the Blood–Brain Barrier and Its Role in the Transport of Amino Acids. J. Nutr. 136: 218S–226S.</ref>. l-Tryptophan is therefore in competition for this carrier with other LNAAs (such as leucine, valine, methionine, histidine, isoleucine, tyrosine, phenylalanine, and threonine) leading to theories that l-tryptophan supplementation might increase serotoinin availability and therefore alter mood and behaviour. However, l-tryptophan is converted to kynurenine by the enzyme indoleamine 2,3,-dioygenase (IDO), which is activated by cortisol or pro-inflammatory cytokines<ref>Oxenkrug, G.F. (2010) Tryptophan–Kynurenine Metabolism as a Common Mediator of Genetic and Environmental Impacts in Major Depressive Disorder: The Serotonin Hypothesis Revisited 40 Years Later. Isr J Psychiatry Relat Sci. 47(1): 56–63.</ref>. Activation of IDO leads to depletion of l-tryptophan, and therefore of serotonin, which indicates a significant role in anxiety and depression<ref> Wichers, M.C., Maes, M. (2004) The role of indoleamine 2,3-dioxygenase (IDO) in the pathophysiology of interferon-α-induced depression. J Psychiatry Neurosci. 29(1):11-7.</ref> <ref>Elovainio, M., Hurme, M., Jokela, M., Pulkki-Råback, L., Kivimäki, M., Hintsanen, M., Hintsa, T., Lehtimäki, T., Viikari, J., Raitakari, O.T., Keltikangas-Järvinen, L. (2012) Indoleamine 2,3-dioxygenase activation and depressive symptoms: results from the Young Finns Study.Psychosom Med. 74(7):675-81.</ref>. Through IDO there is therefore an interaction between stress hormones (e.g. cortisol), inflammation and serotonin production. Supplementation of l-tryptophan in stressed individuals might therefore be expected to have variable effects. Supplementation with 5-hydroxytrptophan, which is converted directly to serotonin and bypasses IDO, might be expected to circumvent this problem. However, despite a large number of trials, evidence of the clinical effect of l-tryptophan supplementation in humans is weak, with a Cochrane Report concluding that evidence for effect above placebo was positive but of insufficient quality to be conclusive both for l-tryptophan and 5-hydroxytryptophan <ref>Shaw, K.A., Turner, J., Del Mar, C. (2008) Tryptophan and 5-Hydroxytryptophan for depressions.The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.</ref>.  
+
L-Tryptophan is large neutral amino acid (LNAA) which acts as a precursor for serotonin. L-Tryptophan is actively transported across the blood brain barrier by the L1 carrier<ref>Hawkins, R.A., O’Kane, R.L., Simpson, I.A., Vin ̃az, J.R. (2006) Structure of the Blood–Brain Barrier and Its Role in the Transport of Amino Acids. J. Nutr. 136: 218S–226S.</ref>. It is therefore in competition for this carrier with other LNAAs (such as leucine, valine, methionine, histidine, isoleucine, tyrosine, phenylalanine, and threonine) leading to theories that l-tryptophan supplementation might increase serotonin availability and therefore alter mood and behaviour. However, l-tryptophan is converted to kynurenine by the enzyme indoleamine 2,3,-dioygenase (IDO), which is activated by cortisol or pro-inflammatory cytokines<ref>Oxenkrug, G.F. (2010) Tryptophan–Kynurenine Metabolism as a Common Mediator of Genetic and Environmental Impacts in Major Depressive Disorder: The Serotonin Hypothesis Revisited 40 Years Later. Isr J Psychiatry Relat Sci. 47(1): 56–63.</ref>. Activation of IDO leads to depletion of l-tryptophan, and therefore of serotonin, which indicates a significant role in anxiety and depression<ref> Wichers, M.C., Maes, M. (2004) The role of indoleamine 2,3-dioxygenase (IDO) in the pathophysiology of interferon-α-induced depression. J Psychiatry Neurosci. 29(1):11-7.</ref> <ref>Elovainio, M., Hurme, M., Jokela, M., Pulkki-Råback, L., Kivimäki, M., Hintsanen, M., Hintsa, T., Lehtimäki, T., Viikari, J., Raitakari, O.T., Keltikangas-Järvinen, L. (2012) Indoleamine 2,3-dioxygenase activation and depressive symptoms: results from the Young Finns Study. Psychosom Med. 74(7):675-81.</ref>. Through IDO there is therefore an interaction between stress hormones (e.g. cortisol), inflammation and serotonin production. Supplementation of l-tryptophan in stressed individuals might therefore be expected to have variable effects. Supplementation with 5-hydroxytryptophan, which is converted directly to serotonin and bypasses IDO, might be expected to circumvent this problem. However, despite a large number of trials, evidence of the clinical effect of l-tryptophan supplementation in humans is weak, with a Cochrane Report concluding that evidence for effect above placebo was positive but of insufficient quality to be conclusive both for l-tryptophan and 5-hydroxytryptophan <ref>Shaw, K.A., Turner, J., Del Mar, C. (2008) Tryptophan and 5-Hydroxytryptophan for depressions.The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.</ref>.  
  
 
Dysfunction of the serotonergic neurotransmitter system in dogs has been linked to a number of problems, including aggression<ref>Rosado, B., Garcia-Belenguer, S., Leon, M., et al. Blood concentrations of serotonin, cortisol, and dehydroepiandrosterone in aggressive dogs. Appl Anim Behav Sci 2010; 123:124-30</ref>. However, evidence for the efficacy of l-tryptophan supplemented diets is as equivocal and unreliable as in humans.
 
Dysfunction of the serotonergic neurotransmitter system in dogs has been linked to a number of problems, including aggression<ref>Rosado, B., Garcia-Belenguer, S., Leon, M., et al. Blood concentrations of serotonin, cortisol, and dehydroepiandrosterone in aggressive dogs. Appl Anim Behav Sci 2010; 123:124-30</ref>. However, evidence for the efficacy of l-tryptophan supplemented diets is as equivocal and unreliable as in humans.
  
−
In both dogs and cats fed a L-tryptophan supplement, lower levels of behaviours related to stress and fewer signs of anxiety were seen in one study, but this was not in a peer-reviewed journal<ref>Da Graca Pereira, G., Fragoso, S., L-tryptophan supplementation and its effect of multi-housed cats and working dogs. Proceedings of the 2010 European Veterinary Behaviour Meeting. Hamburg, 2010, 30-35</ref>. In another study, an axiolytic effect was fond, but the diet contained alpha-casozepine as well as l-tryptophan, so any effect cannot be ascribed to amino acid acid supplementation alone<ref name="Kato">Kato, M., Miyaji, K., Ohtani, N., et al. (2012) Effects of prescription diet on dealing with stressful situations and performance of anxiety-related behaviours in privately owned anxious dogs. Journal of Veterinary Behavior: Clinical Applications and Research. 7(1). 21–26.</ref>. A randomised double-blinded, placebo-controlled study showed no effect of an l-tryptophan enriched diet on behaviour or salivary cortisol in dogs, despite measurable increases in plasma levels of the amino acid<ref name="Kato">Kato, M., Miyaji, K., Ohtani, N., et al. (2012) Effects of prescription diet on dealing with stressful situations and performance of anxiety-related behaviours in privately owned anxious dogs. Journal of Veterinary Behavior: Clinical Applications and Research. 7(1). 21–26.</ref>Bosch, G., Beerda, B., Beynen, A.C., van der Borg, J.A.M.,  b, van der Poel, A.F.B., Hendriks, W.H.,  (2009) Dietary tryptophan supplementation in privately owned mildly anxious dogs. Applied Animal Behaviour Science. 121. 197–205</ref>.
+
In both dogs and cats fed a l-tryptophan supplement, lower levels of behaviours related to stress and fewer signs of anxiety were seen in one study, but this was not in a peer-reviewed journal<ref>Da Graca Pereira, G., Fragoso, S., L-tryptophan supplementation and its effect of multi-housed cats and working dogs. Proceedings of the 2010 European Veterinary Behaviour Meeting. Hamburg, 2010, 30-35</ref>. In another study, an axiolytic effect was found, but the diet contained alpha-casozepine as well as l-tryptophan, so any effect cannot be ascribed to amino acid acid supplementation alone<ref name="Kato">Kato, M., Miyaji, K., Ohtani, N., et al. (2012) Effects of prescription diet on dealing with stressful situations and performance of anxiety-related behaviours in privately owned anxious dogs. Journal of Veterinary Behavior: Clinical Applications and Research. 7(1). 21–26.</ref>. A randomised double-blinded, placebo-controlled study showed no effect of an l-tryptophan enriched diet on behaviour or salivary cortisol in dogs, despite measurable increases in plasma levels of the amino acid<ref name="Kato">Kato, M., Miyaji, K., Ohtani, N., et al. (2012) Effects of prescription diet on dealing with stressful situations and performance of anxiety-related behaviours in privately owned anxious dogs. Journal of Veterinary Behavior: Clinical Applications and Research. 7(1). 21–26.</ref><ref>Bosch, G., Beerda, B., Beynen, A.C., van der Borg, J.A.M.,  b, van der Poel, A.F.B., Hendriks, W.H.,  (2009) Dietary tryptophan supplementation in privately owned mildly anxious dogs. Applied Animal Behaviour Science. 121. 197–205</ref>.
  
−
The effect of dietary protein content is also uncertain. In one study feeding dogs a diet with a lower protein content decreased territorial aggression (territorial aggression that had a fearful underlying motivation)<ref>Dodman, N.H., Reisner, I., Shuster, L., et al. Effect of dietary protein content on behaviour of dogs. J Am Vet Med Assoc 1996; 208:376-9</ref>, although other types of aggression seemed to be uninfluenced. In another, protein content and relative level to l-tryptophan were found to affect different forms of aggression<ref>DeNapoli, J.S., Dodman, N.H., Shuster, L., Rand, W.M., Gross, K.L. (2000) Effect of dietary protein content and tryptophan supplementation on dominance aggression, territorial aggression, and hyperactivity in dogs.J Am Vet Med Assoc. 217(4):504-8.</ref>.
+
The effect of dietary protein content is also uncertain. In one study feeding dogs a diet with a lower protein content decreased territorial aggression (territorial aggression that had a fearful underlying motivation)<ref>Dodman, N.H., Reisner, I., Shuster, L., et al. Effect of dietary protein content on behaviour of dogs. J Am Vet Med Assoc 1996; 208:376-9</ref>, although other types of aggression seemed to be uninfluenced. In another, protein content and relative level to l-tryptophan were found to affect different forms of aggression<ref>DeNapoli, J.S., Dodman, N.H., Shuster, L., Rand, W.M., Gross, K.L. (2000) Effect of dietary protein content and tryptophan supplementation on dominance aggression, territorial aggression, and hyperactivity in dogs. J Am Vet Med Assoc. 217(4):504-8.</ref>.
  
 
Increasing carbohydrate level in the diet has also been proposed as a means of altering anxiety in dogs and cats, but such diets also include a reduced protein content.
 
Increasing carbohydrate level in the diet has also been proposed as a means of altering anxiety in dogs and cats, but such diets also include a reduced protein content.

Revision as of 13:57, 15 July 2014

Overview

Several aspects of feeding can have an effect on behaviour:

  • Dietary composition: Nutrient composition, palatability, method of preservation (raw, dried, moist)
  • Timing of access: Meal-feeding, on demand feeding, ad-lib feeding
  • Type of access: Bowl, simulated foraging (activity feeding)

All of these should be taken into account when designing a feeding regime for domestic cats and dogs.

Feeding Pattern

It is particularly important to ensure appropriate timing and type of access that satisfies species-specific time and energy allocation; cats and dogs would normally spent large parts of the day on foraging behaviour. A lack of opportunity to do this can lead to welfare and behaviour problems.

  • Feral and wild cats allocate 6-8 hours every day on foraging (searching for prey and hunting). They eat 10-20 small meals each day, and return to hunting after consuming a meal. Frequency of hunting is not affected by satiation; cats will hunt whether hungry or not, but latency to kill-bite delivery is reduced when cats are hungry.
  • Feral dogs and wolves hunt more sporadically, as opportunities arise, but also spend several hours each day foraging (often searching for carrion and non-meat food).

For cats, the most ethologically appropriate presentation of food is ad-lib using simulated foraging (activity feeders). A cat given 2 meals per day is effectively having its feeding frequency reduced to the equivalent of a person being fed every 2nd or 3rd day.

For dogs, some opportunity for simulated foraging should also be provided, in the form of activity feeders.

Dietary Components Which Affect Behaviour

Certain dietary components have an effect on an animals behaviour, leading to the possibility that behaviour may be manipulated using a modified diet.

Protein, Tryptophan and Carbohydrate

L-Tryptophan is large neutral amino acid (LNAA) which acts as a precursor for serotonin. L-Tryptophan is actively transported across the blood brain barrier by the L1 carrier[1]. It is therefore in competition for this carrier with other LNAAs (such as leucine, valine, methionine, histidine, isoleucine, tyrosine, phenylalanine, and threonine) leading to theories that l-tryptophan supplementation might increase serotonin availability and therefore alter mood and behaviour. However, l-tryptophan is converted to kynurenine by the enzyme indoleamine 2,3,-dioygenase (IDO), which is activated by cortisol or pro-inflammatory cytokines[2]. Activation of IDO leads to depletion of l-tryptophan, and therefore of serotonin, which indicates a significant role in anxiety and depression[3] [4]. Through IDO there is therefore an interaction between stress hormones (e.g. cortisol), inflammation and serotonin production. Supplementation of l-tryptophan in stressed individuals might therefore be expected to have variable effects. Supplementation with 5-hydroxytryptophan, which is converted directly to serotonin and bypasses IDO, might be expected to circumvent this problem. However, despite a large number of trials, evidence of the clinical effect of l-tryptophan supplementation in humans is weak, with a Cochrane Report concluding that evidence for effect above placebo was positive but of insufficient quality to be conclusive both for l-tryptophan and 5-hydroxytryptophan [5].

Dysfunction of the serotonergic neurotransmitter system in dogs has been linked to a number of problems, including aggression[6]. However, evidence for the efficacy of l-tryptophan supplemented diets is as equivocal and unreliable as in humans.

In both dogs and cats fed a l-tryptophan supplement, lower levels of behaviours related to stress and fewer signs of anxiety were seen in one study, but this was not in a peer-reviewed journal[7]. In another study, an axiolytic effect was found, but the diet contained alpha-casozepine as well as l-tryptophan, so any effect cannot be ascribed to amino acid acid supplementation alone[8]. A randomised double-blinded, placebo-controlled study showed no effect of an l-tryptophan enriched diet on behaviour or salivary cortisol in dogs, despite measurable increases in plasma levels of the amino acid[8][9].

The effect of dietary protein content is also uncertain. In one study feeding dogs a diet with a lower protein content decreased territorial aggression (territorial aggression that had a fearful underlying motivation)[10], although other types of aggression seemed to be uninfluenced. In another, protein content and relative level to l-tryptophan were found to affect different forms of aggression[11].

Increasing carbohydrate level in the diet has also been proposed as a means of altering anxiety in dogs and cats, but such diets also include a reduced protein content.

Pyridoxine

Pyridoxine (vitamin B6) is a cofactor in the production of serotonin, and there is evidence that supplementation can alter tryptophan metabolism to produce higher CNS levels of 5-hydroxytryptophan and serotonin in studies involving laboratory animals[12]. However, the specific effects of this vitamin alone on behaviour in cats and dogs has not been established. Caution should be exercises regarding pyridoxine dose, given that is potentially neurotoxic in overdose[13].

Fatty Acids

For cats, cis-linoleic and arachidonic acid are essential fatty acids. However, other fatty acids, specifically long-chain omega-3 fatty acids such as docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) are essential for normal development[14]. DHA and EPA have been shown to have anti-inflammatory effects[15][16][17].

There is evidence that higher levels of DHA in puppy diets produce improved cognitive performance in laboratory tests (reversal task learning, visual contrast discrimination, and early psychomotor performance)[18], and are essential for normal retinal function[19] and neurological development. [20].

Fatty acids such as DHA form part of the modified diets and dietary supplements that are used to treat canine and feline cognitive dysfunction[21].

There is also some evidence that omega-3 PUFAs may have a role in the treatment of psychiatric problems in people[22].

Antioxidant enriched diets

Antioxidant enriched diets have been shown to have short, medium and long term effects on memory and perception in dogs with cognitive dysfunction syndrome[23] [24] [25].

Medium Chain Triglycerides

In human Alzheimer's disease, CNS hypo metabolism may be a target for dietary therapy[26]. Ketone bodies, such as beta-hydroxybutyrate, are a potential supplementary energy source for neurones, and support cells, with impaired oxidative phosphorulation systems. Supplementation with beta-hydroxybutyrate has been shown to improve cognition in human adults with memory impairment[27]. Medium chain triglycerides, which are metabolised to beta-hydroxybutyrate by the liver, have been shown to produce beneficial effects on the cognition of aged dogs[28].

References

  1. ↑ Hawkins, R.A., O’Kane, R.L., Simpson, I.A., Vin ̃az, J.R. (2006) Structure of the Blood–Brain Barrier and Its Role in the Transport of Amino Acids. J. Nutr. 136: 218S–226S.
  2. ↑ Oxenkrug, G.F. (2010) Tryptophan–Kynurenine Metabolism as a Common Mediator of Genetic and Environmental Impacts in Major Depressive Disorder: The Serotonin Hypothesis Revisited 40 Years Later. Isr J Psychiatry Relat Sci. 47(1): 56–63.
  3. ↑ Wichers, M.C., Maes, M. (2004) The role of indoleamine 2,3-dioxygenase (IDO) in the pathophysiology of interferon-α-induced depression. J Psychiatry Neurosci. 29(1):11-7.
  4. ↑ Elovainio, M., Hurme, M., Jokela, M., Pulkki-Råback, L., Kivimäki, M., Hintsanen, M., Hintsa, T., Lehtimäki, T., Viikari, J., Raitakari, O.T., Keltikangas-Järvinen, L. (2012) Indoleamine 2,3-dioxygenase activation and depressive symptoms: results from the Young Finns Study. Psychosom Med. 74(7):675-81.
  5. ↑ Shaw, K.A., Turner, J., Del Mar, C. (2008) Tryptophan and 5-Hydroxytryptophan for depressions.The Cochrane Collaboration. Published by John Wiley & Sons, Ltd.
  6. ↑ Rosado, B., Garcia-Belenguer, S., Leon, M., et al. Blood concentrations of serotonin, cortisol, and dehydroepiandrosterone in aggressive dogs. Appl Anim Behav Sci 2010; 123:124-30
  7. ↑ Da Graca Pereira, G., Fragoso, S., L-tryptophan supplementation and its effect of multi-housed cats and working dogs. Proceedings of the 2010 European Veterinary Behaviour Meeting. Hamburg, 2010, 30-35
  8. ↑ 8.0 8.1 Kato, M., Miyaji, K., Ohtani, N., et al. (2012) Effects of prescription diet on dealing with stressful situations and performance of anxiety-related behaviours in privately owned anxious dogs. Journal of Veterinary Behavior: Clinical Applications and Research. 7(1). 21–26.
  9. ↑ Bosch, G., Beerda, B., Beynen, A.C., van der Borg, J.A.M., b, van der Poel, A.F.B., Hendriks, W.H., (2009) Dietary tryptophan supplementation in privately owned mildly anxious dogs. Applied Animal Behaviour Science. 121. 197–205
  10. ↑ Dodman, N.H., Reisner, I., Shuster, L., et al. Effect of dietary protein content on behaviour of dogs. J Am Vet Med Assoc 1996; 208:376-9
  11. ↑ DeNapoli, J.S., Dodman, N.H., Shuster, L., Rand, W.M., Gross, K.L. (2000) Effect of dietary protein content and tryptophan supplementation on dominance aggression, territorial aggression, and hyperactivity in dogs. J Am Vet Med Assoc. 217(4):504-8.
  12. ↑ Calderón-Guzmána, D., Hernández-Islasa, J.L., Espitia-Vázqueza, I., Barragán-Mejı́aa, G., Hernández-Garcı́aa, E., Santamarı́a-del Ángela, D., Juárez-Olguı́nb, H. (2004) Pyridoxine, regardless of serotonin levels, increases production of 5-hydroxytryptophan in rat brain. Archives of Medical Research. 35(4).271–274.
  13. ↑ Rao, D.B., Jortner, B.S., Sills, R.C. (2014) Animal models of peripheral neuropathy due to environmental toxicants. ILAR J. 54(3):315-23.
  14. ↑ Innis, S.M. Dietary (n-3) fatty acids and brain development. J Nutr 2007:137:855-9
  15. ↑ Serini, S., Bizzarro, A., Piccioni, E., Fasano, E., Rossi, C., Lauria, A., Cittadini, A.R., Masullo, C., Calviello, G. (2012) EPA and DHA differentially affect in vitro inflammatory cytokine release by peripheral blood mononuclear cells from Alzheimer's patients. Curr Alzheimer Res. 9(8):913-23.
  16. ↑ Weldon, S.M., Mullen, A.C., Loscher, C.E., Hurley, L.A., Roche, H.M. (2007) Docosahexaenoic acid induces an anti-inflammatory profile in lipopolysaccharide-stimulated human THP-1 macrophages more effectively than eicosapentaenoic acid. J Nutr Biochem. 18(4):250-8.
  17. ↑ Mullen, A., Loscher, C.E., Roche, H.M. (2010) Anti-inflammatory effects of EPA and DHA are dependent upon time and dose-response elements associated with LPS stimulation in THP-1-derived macrophages.. J Nutr Biochem. 21(5):444-50.
  18. ↑ Zicker, S.C, Jewell, D.E., Yamka, R.M., et al. Evaluation of cognitive learning, memory, psychomotor, immunologic, and retinal functions in healthy puppies fed foods fortified with docosahexanoeic acid-rich fish oil from 8-52 weeks. J Am Vet Med Assoc 2012;241:583-94
  19. ↑ Bauer, J.E., Heinemann, K.M., Lees, G.E., et al. Retinal functions of young dogs are improved and maternal plasma phospholipids are altered with diets containing long-chain n-3 polyunsaturated fatty acids during gestation, lactation, and after weaning. J Nutr 2006;1191S-994S
  20. ↑ Heinemann, K.M., Bauer, J.E., Docosaheaenoic acid and neurologic development in animals. J Am Vet Med Assoc 2006;228:700-6
  21. ↑ Heath, S.E., Barabas, S., Craze, P.G., (2007) Nutritional supplementation in cases of canine cognitive dysfunction—A clinical trial Applied Animal Behaviour Science. 105. 284–296.
  22. ↑ Ross, B.M., Seguin, J., Sieswerda, (2007) L.E. 3 Omega-3 fatty acids as treatments for mental illness: which disorder and which fatty acid? Lipids in Health and Disease. 6:21.
  23. ↑ Milgram, N.W., Head, E., Zicker, S.C., Ikeda-Douglas, C.J., Murphey, H., Muggenburg, B., Siwak, C., Tapp, D., Cotman, C.W. (2005) Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: a two-year longitudinal study. Neurobiology of Aging. 26. 77–90.
  24. ↑ Milgram, N.W., Head, E., Muggenburg, B., Holowachuka, D., Murphey, H., Estradaa, J., Ikeda-Douglas, C.C., Zickerd, S.C., Cotman, C.W. (2002) Landmark discrimination learning in the dog: effects of age, an antioxidant fortified food, and cognitive strategy. Neuroscience and Biobehavioral Reviews. 26. 679–695
  25. ↑ Milgram, N.W., Zicker, S.C., Head, E., Muggenburg, B.A., Murphey, H., Ikeda-Douglas, C.J., Cotman, C.W. ( 2002) Dietary enrichment counteracts age-associated cognitive dysfunction in canines. Neurobiology of Aging. 23. 737–745.
  26. ↑ Costantini, L.C., Barr, L.J., Vogel, J.L., Henderson, S.T. (2008) Hypometabolism as a therapeutic target in Alzheimer's disease. BMC Neuroscience. 9(Suppl 2). S16.
  27. ↑ Reger, M.A., Henderson, S.T., Hale, C., Cholerton, B., Baker, L.D., Watson, G.S., Hyde, K., Chapman, D., Craft, S. (2004) Effects of Beta-hydroxybutyrate on cognition in memory-impaired adults. Neurobiology of Aging. 25. 311–314.
  28. ↑ Pan, Y., Larson, B., Araujo, J.A., Lau, W., de Rivera, C., Santana, R., Gore, A., Milgram, N.W. (2010) Dietary supplementation with medium-chain TAG has long-lasting cognition-enhancing effects in aged dogs. British Journal of Nutrition. 103. 1746–1754.
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