Skip to main content
SpringerLink
Log in

Differential modulation of dopaminergic systems in the rat brain by dietary protein

  • Original Articles
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Rats that consume a diet 50% rich in protein exhibit hyperactivity and hyperresponsiveness to nociceptive stimuli, in which facilitation of dopaminergic activity has been implicated. We studied the regional changes in the concentrations of dopamine (DA) and its metabolites, dihydroxyphenylacetic acid (DOPAC) and homovanillic acid (HVA) in the brains of rats that were maintained on high-protein (HP, 50% casein), normal-protein (NP, 20% casein), and low-protein (LP, 8% casein) diets for 36 weeks. Brain nuclei that represented different DAergic systems were punchdissected and analyzed using HPLC. In the substantia nigra, the striatum, and the dentate gyrus, DA concentrations decreased and increased, respectively, with a decrease and increase in dietary protein (p<0.05 compared to the NP diet). Similar trends in the effect of the HP diet were observed in the ventral tegmental area, amygdala, frontal cortex, subiculum, centromedial nucleus (CM) of the thalamus, and inferior colliculi (IC), although the differences in DA concentrations were not statistically significant. These brain areas also showed a pattern of decreased DA concentration in association with the LP diet, and the differences were statistically significant (p<0.05) in the CM and IC. DA concentrations in most regions of the midbrain and brainstem were not different between the diet groups, nor were consistent trends observed in those regions. Also, there were no consistent relationships between DOPAC/DA and HVA/DA ratios and dietary protein level. These data suggest that only discrete dopaminergic neuronal circuits in the rat forebrain were sensitive to changes in dietary protein level.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bannon, M.J., and Roth, R.H. 1983. Pharmacology of mesocortical dopamine neurons. Pharmacol. Rev. 35(1):53–68.

    Google Scholar 

  2. Bartholini, G., Stadler, H., Gadea-Ciria, M., and Lloyd, K.G. 1977. Interaction of dopaminergic and cholinergic neurons in the extrapyramidal and limbic systems.in, Costa, E., and Gessa, G.L. (eds.), Advances in Biochemical Psychopharmacology, vol. 16, Raven Press, New York, pp. 391–395.

    Google Scholar 

  3. Bischoff, S. 1986. Mesohippocampal dopamine system: characterization, function, and clinical implications. Pages 1–32,in Isaacson, R.L., and Pribram, K.H. (eds.), The Hippocampus, vol. 3, Plenum Publishing Corp. New York.

    Google Scholar 

  4. Brock, J.W., and Prasad, C. 1991. Motor, but not sensory, cortical potentials are amplified by high-protein diet. Physiol. Behav. 50:887–893.

    Google Scholar 

  5. Brownstein, M., Saavedra, J.M., and Palkovits, M. 1974. Norepinephrine and dopamine in the limbic system of the rat. Brain Res. 79:431–436.

    Google Scholar 

  6. Carboni, E., Imperato, A., Perezzani, L., and Di Chiara, G. 1989. Amphetamine, cocaine, phencyclidine, and nomifensine increase extracellular dopamine concentrations preferentially in the nucleus accumbens of freely moving rats. Neuroscience 28:653–661.

    Google Scholar 

  7. Costa, E., Panula, P., Thompson, H.K., and Cheny, D.L. 1983. The trans-synaptic regulation of the septo-hippocampal cholinergic neurons. Life Sci. 32:165–179.

    Google Scholar 

  8. Damsma, G., Wenkstern, D., Pfaus, J.G., Phillips, A.G., and Fibiger, H.C. 1992. Sexual behavior increases dopamine transmission in the nucleus accumbens and striatum of male rats: comparison with novelty and locomotion. Behav. Neurosci. 106(1):181–191.

    Google Scholar 

  9. During, M.J., Acworth, I.N., and Wurtman, R.J. 1989. Dopamine release in the striatum: physiological coupling to tyrosine supply. J. Neurochem. 52:1449–1454.

    Google Scholar 

  10. Fallon, J.H., and Loughlin, S.E. 1985. Substantia nigra. Pages 353–374,in Paxinos, G. (ed.), The Rat Nervous System, Academic Press, Australia.

    Google Scholar 

  11. Fanelli, M., Nahmod, V.E., Torres, N., Santajuliana, D., Garcia, S.I., Finkielman, S., and Pirola, C.J. 1992. Brain amines in glucocorticoid-induced hypertension in the rat. Neurosci. Lett 135:189–192.

    Google Scholar 

  12. Galey, D., Durkin, T., Sifakis, G., Kempf, E., and Jaffard, R. 1985. Facilitation of spontaneous and learned spatial behaviors following 6-hydroxydopamine lesions of the lateral septum: a cholinergic hypothesis. Brain Res. 340:171–174.

    Google Scholar 

  13. Gardier, A.M., Trouvin, J.H., Orosco, M., Nicolaidis, S., and Jacquot, C. 1988. Biogenic amines and turnover in discrete rat hypothalamic and amygdalar feeding related structures by an improved LC-ECD assay. Biogenic Amines 5(2):177–189.

    Google Scholar 

  14. German, D.C., Manaye, K., Smith, W.K., Woodward, D.J., and Saper, C.B. 1989. Midbrain dopaminergic cell loss in Parkinson's disease: computer visualization. Ann. Neurol. 26:507–514.

    Google Scholar 

  15. Glaeser, B.S., Maher, T.J., and Wurtman, R.J. 1983. Changes in brain levels of acidic, basic, and neutral amino acids after consumption of single meals containing various proportions of protein. J. Neurochem. 41(4):1016–1021.

    Google Scholar 

  16. Growden, J.H., Melamed, E., Logue, M., Hefti, F., and Wurtman, R.J. 16. 1982. Effects of orall-tyrosine administration on CSF tyrosine and homovanillic acid levels in patients with Parkinson's Disease. Life Sci. 30:827–832.

    Google Scholar 

  17. Hamdi, A., Onaivi, E.S., and Prasad, C. 1992. A low protein-high carbohydrate diet decreases D2 dopamine receptor density in rat brain. Life Sci. 50:1529–1534.

    Google Scholar 

  18. Heffner, T.G., Hartman, J.A., and Seiden, L.S. 1980. Feeding increases dopamine metabolism in the rat brain. Science 208:1168–1170.

    Google Scholar 

  19. Hjemdahl, P. 1984. Catecholamine measurements by high-performance liquid chromatography. Am. J. Physiol. 247 (Endrocrinol. Metab. 10):E13-E20.

    Google Scholar 

  20. Kabani, N.J., Reader, T.A., and Dykes, R.W. 1990. Monoamines and their metabolites in somatosensory, visual, and cingulate cortices of adult rat: differences in content and lack of sidedness. Neurochem. Res. 15(10):1031–1036.

    Google Scholar 

  21. Kaneyuki, T., Morimasa, T., and Shohmori, T. 1984. Relationship of tyrosine concentration to catecholamine levels in rat brain. Acta Med. Okayama 38(4):403–407.

    Google Scholar 

  22. Langlais, P.J., Walsh, F.X., Stevens, T.J., and Bird, E.D. Estimation of dopamine turnover in striatal, limbic and frontal cortical areas of human brain. Soc. Neurosci. Abstr. 8:114, 1982.

    Google Scholar 

  23. Lavielle, S., Tassin, J.P., Thierry, A.M., Blanc, G., Herve, D., Barthelemy, C., and Glowinski, J. 1978. Blockade by benzodiazepines of the selective high increase in dopamine turnover induced by stress in mesocortical dopaminergic neurons of the rat. Brain Res. 168:585–594.

    Google Scholar 

  24. LeDoux, J.E., Ruggiero, D.A., Forest, R., Stornetta, R. and Reis, D.J. 1987. Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J. Comp. Neurol. 264:123–146.

    Google Scholar 

  25. Le Moal, M., and Simon, H. 1991. Mesocorticolimbic dopaminergic network: functional and regulatory roles. Physiol. Rev. 71(1):155–234.

    Google Scholar 

  26. Louilot, A., Taghzouti, K., Simon, H., and Le Moal, M. 1989. Limbic system, basal ganglia, and dopaminergic neurons. Brain Behav. Evol. 33:157–161.

    Google Scholar 

  27. Lindvall, O., Bjorklund, A., and Divac, I. 1977. Organization of mesencephalic dopamine neurons projecting to neocortex and septum. Pages 39–46,in Costa, E., and Gessa, G.L. (eds.), Advances in Biochemical Psychopharmacology, vol. 16, Raven Press, New York.

    Google Scholar 

  28. Moore, R.Y., and Bloom, F.E. 1978. Central catecholamine neuron systems: anatomy and physiology of the dopamine systems. Ann. Rev. Neurosci. 1:129–169.

    Google Scholar 

  29. Munkvad, I., Pakkenberg, H., and Randrup, A. 1968. Aminergic systems in basal ganglia associated with stereotyped hyperactive behavior and catalepsy. Brain Behav. Evol. 1:89–100.

    Google Scholar 

  30. Niemegeers, C.J.E., McGuire, J.L., and Janssen, P.A.J. 1978. Domperidone, a novel gastrokinetic drug. Pharmacologist 20:209.

    Google Scholar 

  31. Oades, R.D., Taghzouti, K., Rivet, J.M., Simon, H. and Le Moal, M. 1986. Locomotor activity in relation to dopamine and noradrenaline in t he nucleus accumbens, septal and frontal areas: a 6-hydroxydopamine study. Neuropsychobiology 16:37–42.

    Google Scholar 

  32. Onaivi, E.S., Payne, S., Brock, J.W., Hamdi, A., Farooqui, S., and Prasad, C. 1991. The performance of Sprague-Dawley and Hooded rats in the shuttle-box avoidance paradigm is dependent on the level of protein in the diet. IBRO World Congr. Neurosci. Abstr. 1:424.

    Google Scholar 

  33. Onaivi, E.S., Brock, J.W., and Prasad, C. 1992. Dietary protein levels alter rat behavior. Nutr. Res. 12:1025–1039.

    Google Scholar 

  34. Palkovits, M. 1973. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res. 59:449–450.

    Google Scholar 

  35. Palkovits, M., Brownstein, M., Saavedra, J.M., and Axelrod, J. 1974. Norepinephrine and dopamine content of hypothalamic nuclei of the rat. Brain Res. 77:137–149.

    Google Scholar 

  36. Paxinos, G., and Watson, C. 1986. The Rat Brain in Stereotaxic Coordinates, 2nd Ed., Academic Press, Inc. San Diego, CA.

    Google Scholar 

  37. Peters, J.C., and Harper, A.E. 1985. Adaptation of rats to diets containing different levels of protein: effects on food intake, plasma and brain amino acid concentrations and brain neurotransmitter metabolism. J. Nutr. 115:382–398.

    Google Scholar 

  38. Peters, J.C., and Harper, A.E. 1987. Acute effects of dietary protein on food intake, tissue amino acids, and brain serotonin. Am. J. Physiol. 252:R902-R914.

    Google Scholar 

  39. Plantz, R.G., Williston, J.S., and Jewett, D.L. 1981. Effects of undernutrition on development of far-field auditory brain stem responses in rat pups. Brain Res. 68:319–326.

    Google Scholar 

  40. Prasad, C., Hamdi, A., Brock, J.W., and Hilton, C.W. 1992. Cyclo(His-Pro) and Food Intake. Pages 277–289,in Bray, G., and Ryan, D.H. (eds.), The science of food regulation. Pennington Center Nutrition Series, vol 2, Louisiana State University Press, Baton Rouge, LA.

    Google Scholar 

  41. Raab, A., and Oswald, R. 1980. Coping with social conflict: impact on the activity of tyrosine hydroxylase in the limbic system and in the adrenals. Physiol. Behav. 24:387–394.

    Google Scholar 

  42. Ranje, C., and Ungerstedt, U. 1977. High correlations between number of dopamine cells, dopamine levels and motor performance. Brain Res. 134:83–93.

    Google Scholar 

  43. Spring, B. 1986. Effects of foods and nutrients on the behavior of normal individuals. Pages 1–47,in Wurtman, R.J., and Wurtman, J.J. (eds.), Nutrition and the Brain, vol 7, Raven Press, New York.

    Google Scholar 

  44. Suave, Y., and Reader, T.A. 1988. Effects of alpha-methyl-ptyrosine on monoamines and catecholamine receptors in rat cerebral cortex and neostriatum. Neurochem. Res. 13:807–815.

    Google Scholar 

  45. Weiss, J.M., Goodman, P.A., Losito, B.G., Corrigan, S., Charry, J.M., and Bailey, W.H. 1981. Behavioral depression produced by an uncontrollable stressor: relationship to norepinephrine, dopamine, and serotonin levels in various regions of rat brain. Brain Res. Rev. 3:167–205.

    Google Scholar 

  46. Westerink, B.H.C., and De Vries, J.B. 1991. Effect of precursor loading on the synthesis rate and release of dopamine and serotonin in the striatum: a microdialysis study in conscious rats. J. Neurochem. 56:228–233.

    Google Scholar 

  47. Winick, M. 1970. Nutrition and mental development. Med. Clin. N. Am. 54:1413–1429.

    Google Scholar 

  48. Woods, S.K., and Meyer, J.S. 1991. Exogenous tyrosine potentiates the methylphenidate-induced increase in extracellular dopamine in the nucleus accumbens: a microdialysis study. Brain Res. 560:97–105.

    Google Scholar 

  49. Wurtman, R.J., Hefty, F., and Melamed, E. 1981. Precursor control of neurotransmitter synthesis. Pharmacol. Rev. 32:315–335.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Neurosciences, Pennington Biomedical Research Center, 6400 Perkins Road, 70808, Baton Rouge, Louisiana

    Shakeel M. Farooqui, Jeffery W. Brock, Emmanuel S. Onaivi, Anwar Hamdi & Chandan Prasad

  2. Section of Endocrinology, Department of Medicine, Louisiana State University Medical Center, 70112, New Orleans, Louisiana

    Chandan Prasad

Authors
  1. Shakeel M. Farooqui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeffery W. Brock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emmanuel S. Onaivi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anwar Hamdi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chandan Prasad
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Farooqui, S.M., Brock, J.W., Onaivi, E.S. et al. Differential modulation of dopaminergic systems in the rat brain by dietary protein. Neurochem Res 19, 167–176 (1994). https://doi.org/10.1007/BF00966812

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00966812

Key Words

Search

Navigation