Advertisement

Experimental Brain Research

, Volume 48, Issue 2, pp 199–208 | Cite as

Thiamine deficiency in the cat leads to severe learning deficits and to widespread neuroanatomical damage

  • E. Irle
  • H. J. Markowitsch
Article

Summary

Behavioral and neuroanatomical consequences of a thiamine-deficient diet, combined with the application of a thiamine-antagonist (pyrithiamine) were investigated in the cat. Eight cats (the experimental group) were subjected to a vitamine-B1-poor diet until they developed neurological symptoms (epileptic attacks, ataxia, gait disturbances), while 24 cats were fed normally and served as control group. Immediately following the appearance of neurological signs, a high dose of thiamine was given to the cats of the experimental group; they were then allowed to recover for ten days. Thereafter the performance in learning an alternation task in a T-maze was tested and compared with that of the control group. Behaviorally, the cats of the experimental group manifested drastically retarded acquisition rates in the learning task compared to the cats of the control group. Neuroanatomically, damage was found in the brains of each of the cats in the experimental group; this damage consisted mainly of enlarged ventricles, hemorrhages, neuronal loss and gliosis. Those regions most consistently affected were the periaqueductal gray, the inferior colliculi and the mamillary nuclei. The thalamic mediodorsal nucleus was affected to a minor degree in three cats only. Four cats manifested damage in the hippocampal formation. No damage was found in the cerebellum. Most of the damaged neuroanatomical loci resemble those found in patients with a Wernicke-Korsakoff syndrome.

Key words

Thiamine Vitamin B1 Cat Amnesia Brain lesions 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams RD (1969) The anatomy of memory mechanisms in the human brain. In: Talland GA, Waugh NC (eds) The pathology of memory. Academic Press, New York, pp 91–106Google Scholar
  2. Bai P, Bennion M, Gubler CJ (1971) Biochemical factors involved in the anorexia of thiamine deficiency in rats. J Nutr 101: 731–738Google Scholar
  3. Behse F, Buchthal F (1977) Alcoholic neuropathy: Clinical, electrophysiological, and biopsy findings. Ann Neurol 2: 95–110Google Scholar
  4. Ben-Ari Y, Tremblay E, Riche D, Ghilini G, Naquet R (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: Metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6: 1361–1391CrossRefPubMedGoogle Scholar
  5. Bender L, Schilder P (1933) Encephalopathia alcoholica (Polioencephalitis haemorrhagica superior of Wernicke). Arch Neurol Psychiat 29: 990–1053Google Scholar
  6. Bernhardt KS, Herbert R (1937) A further study of vitamin B deficiency and learning with rats. J Comp Physiol Psychol 24: 263–267Google Scholar
  7. Blank NK, Vick NA, Schulman S (1975) Wernicke's encephalopathy. An experimental study in the rhesus monkey. Acta Neuropathol (Berl) 31: 137–150Google Scholar
  8. Brožek J, Vase G (1961) Experimental investigations on the effects of dietary deficiencies on animal and human behavior. Vitam Horm 19: 43–94Google Scholar
  9. Campbell ACP, Biggart JH (1939) Wernicke's encephalopathy (Polioencephalitis haemorrhagica superior): Its alcoholic and non-alcoholic incidence. J Pathol Bacteriol 48: 245–262Google Scholar
  10. Cerecedo LR (1955) Thiamine antagonists. Am J Clin Nutr 3: 273–281Google Scholar
  11. Collins RC, Kirkpatrick JB, McDougal DB, Jr (1970) Some regional pathologic and metabolic consequences in mouse brain pyrithiamine-induced thiamine deficiency. J Neuropathol Exp Neurol 29: 57–69Google Scholar
  12. Cruickshank EK (1976) Effects of malnutrition on the central nervous system and the nerves. In: Vinken PJ, Bruyn GW (eds) Handbook of clinical neurology, vol 28, part II: Metabolic and deficiency diseases of the nervous system. Elsevier/North-Holland, Amsterdam, pp 1–41Google Scholar
  13. Davison C, Stone L (1937) Lesions of the nervous system of the rat in vitamin B deficiency. Arch Pathol 23: 207–223Google Scholar
  14. DeOlmos JS, Ingram WR (1971) An improved cupric-silver method for impregnation of axonal and terminal degeneration. Brain Res 33: 523–529Google Scholar
  15. Drachman DA, Arbit J (1966) Memory and the hippocampal complex. Arch Neurol 15: 52–61Google Scholar
  16. Dreyfus PM, Victor M (1961) Effects of thiamine deficiency on the central nervous system. Am J Clin Nutr 9: 414–425Google Scholar
  17. Fritz MF (1932) Maze performance of the white rat in relation to unfavorable salt mixture and vitamin B deficiency. J Comp Physiol Psychol 13: 365–389Google Scholar
  18. Grunnet ML (1969) Changing incidence, distribution and histopathology of Wernicke's polioencephalopathy. Neurology 19: 1135–1139Google Scholar
  19. Hakim AM, Pappius HM (1981) The effect of thiamine deficiency on local cerebral glucose utilization. Ann Neurol 9: 334–339Google Scholar
  20. Irle E, Markowitsch HJ (1982) Single and combined lesions of the cat's thalamic mediodorsal nucleus and the mamillary bodies lead to severe deficits in the acquisition of an alternation task. Behav Brain Res (in press)Google Scholar
  21. Joliffe N, Wortis H, Fein HD (1941) The Wernicke syndrome. Arch Neurol Psychiat 46: 569–597Google Scholar
  22. Jubb KV, Saunders LZ, Coates HV (1956) Thiamine deficiency encephalopathy in cats. J Comp Pathol 66: 217–227Google Scholar
  23. Langohr HD, Petruch F, Schroth G (1981) Vitamin B1, B2 and B6 deficiency in neurological disorders. J Neurol 225: 95–108Google Scholar
  24. Lee K, Dunwiddie T, Deitrich R, Lynch G, Hoffer B (1981) Chronic ethanol consumption and hippocampal neuron dendritic spines: A morphometric and physiological analysis. Exp Neurol 71: 541–549Google Scholar
  25. Mair WGP, Warrington EK, Weiskrantz L (1979) Memory disorder in Korsakoff psychosis. A neuropathological and neuropsychological investigation of two cases. Brain 102: 749–783Google Scholar
  26. Mancall EL, McEntee WJ (1965) Alterations of the cerebellar cortex in nutritional encephalopathy. Neurology 15: 303–313Google Scholar
  27. Markowitsch HJ (1982) Retention performance of a learned delayed-alternation task after chemical lesions of the cat's mediodorsal nucleus. Behav Brain Res 4: 263–277Google Scholar
  28. Markowitsch HJ, Pritzel M, Kessler J, Guldin W, Freeman RB, Jr (1980) Delayed-alternation performance after selective lesions within the prefrontal cortex of the cat. Behav Brain Res 1: 67–91Google Scholar
  29. Maurer S (1935) III. The effect of partial depletion of vitamin B (B1) upon performance in rats. J Comp Physiol Psychol 20: 309–317Google Scholar
  30. Maurer S, Tsai LS (1931) The effect of partial depletion of vitamin B complex upon learning ability in rats. J Nutr 4: 507–516Google Scholar
  31. Meyer JG, Neundörfer B, Rethel R, Walker G, Bayerl J (1981) Über die Beziehung zwischen alkoholischer Polyneuropathie und Vitamin b1, B12 und Folsäure. Nervenarzt 52: 329–332Google Scholar
  32. O'Neill PH (1949) The effect on subsequent maze learning ability of graded amounts of vitamin B1 in the diet of very young rats. J Genet Psychol 74: 85–95Google Scholar
  33. Phillips GB, Victor M, Adams RD, Davidson CS (1952) A study of the nutritional defect in Wernicke's syndrome. The effect of purified diet, thiamine, and other vitamins on the clinical manifestations. J Clin Invest 31: 859–871Google Scholar
  34. Poe CF, Poe E, Muenzinger KF (1937) The effect of vitamin deficiency upon the acquisition and retention of the maze habit in the white rat. J Comp Physiol Psychol 23: 67–76Google Scholar
  35. Poe E, Poe CF, Muenzinger KF (1936) The effect of vitamin, deficiency upon the acquisition and retention of the maze habit in the white rat. I. The vitamin B-complex. J Comp Physiol Psychol 22: 69–77Google Scholar
  36. Poe E, Poe CF, Muenzinger KF (1939) The effect of vitamin deficiency upon the acquisition and retention of the maze habit in the white rat. IV. Vitamins B-complex, B1, and B2 (G). J Comp Physiol Psychol 27: 211–214Google Scholar
  37. Ponsford JL, Donnan GA (1980) Transient global amnesia — a hippocampal phenomenon? J Neurol Neurosurg Psychiat 43: 285–287Google Scholar
  38. Riggs HE, Boles RS (1944) Wernicke's disease. A clinical and pathological study of 42 cases. Q J Stud Alcohol 5: 361–370Google Scholar
  39. Riley JN, Walker DW (1978) Morphological alterations in hippocampus after long-term alcohol consumption in mice. Science 201: 646–648Google Scholar
  40. Rindi G, Perri V, DeCaro L (1961) The uptake of pyrithiamine by cerebral tissue. Experientia 17: 546–547Google Scholar
  41. Rinehart JF, Friedman M, Greenberg LD (1949) Effect of experimental thiamine deficiency on the nervous system of the rhesus monkey. Arch Pathol 48: 129–139Google Scholar
  42. Still CN (1976) Nicotinic acid and nicotinamide deficiency: Pellagra and related disorders of the nervous system. In: Vinken PJ, Bruyn GW (eds) Handbook of clinical neurology, vol 28, part II: Metabolic and deficiency diseases of the nervous system. Elsevier/North-Holland, Amsterdam, pp 59–104Google Scholar
  43. Troncosco JC, Johnston MV, Hess KM, Price DL (1981) Model of Wernicke's encephalopathy. Arch Neurol 38: 350–354Google Scholar
  44. Van Buren JM, Borke RC (1972) The mesial temporal substratum of memory. Brain 95: 599–632Google Scholar
  45. Victor M (1976) The Wernicke-Korsakoff syndrome. In: Vinken PJ, Bruyn GW (eds) Handbook of clinical neurology, vol 28, part II: Metabolic and deficiency diseases of the nervous system. Elsevier/North-Holland, Amsterdam, pp 243–270Google Scholar
  46. Victor M, Adams RD (1961) On the etiology of the alcoholic neurological diseases. Am J Clin Nutr 9: 379–397Google Scholar
  47. Victor M, Adams RD, Collins GH (1971) The Wernicke-Korsakoff syndrome. Blackwell, OxfordGoogle Scholar
  48. Victor M, Angevine J, Mancall E, Fisher CM (1961) Memory loss with lesions of hippocampal formation. Arch Neurol 5: 244–263Google Scholar
  49. Victor M, Yakovlev PI (1955) Korsakoff's psychic disorder in conjunction with peripheral neuritis. A translation of Korsakoff's original article with brief comments on the author and his contribution to clinical medicine. Neurology 5: 394–406Google Scholar
  50. Vorhees CV (1979) Avoidance deficits in rats after recovery from mild to moderate thiamin deficiency. Behav Neurol Biol 25: 398–405Google Scholar
  51. Walker DW, Barnes DE, Riley JN, Hunter BE, Zornetzer SF (1980a) Neurotoxicity of chronic alcohol consumption: An animal model. In: Sandler M (ed) Psychopharmacology of alcohol. Raven Press, New York, pp 17–31Google Scholar
  52. Walker DW, Barnes DE, Zornetzer SF, Hunter BE, Kubanis P (1980b) Neuronal loss in hippocampus induced by prolonged ethanol ingestion in rats. Science 209: 711–713Google Scholar
  53. Walker DW, Hunter BE (1978) Short-term memory impairment following chronic alcohol consumption in rats. Neuropsychologia 16: 545–553Google Scholar
  54. Watanabe I, Kanabe S (1978) Early edamatous lesion of pyrithiamine induced acute thiamine deficient encephalopathy in the mouse. J Neuropathol Exp Neurol 37: 401–413Google Scholar
  55. Watanabe I, Tomita T, Hung K-S, Iwasaki Y (1981) Edamatous necrosis in thiamine-deficient encephalopathy of the mouse. J Neuropathol Exp Neurol 40: 454–471Google Scholar
  56. Woolley DW, White AGC (1943) Production of thiamine deficiency disease by the feeding of a pyridine analogue of thiamine. J Biol Chem 149: 285–289Google Scholar
  57. Zimmerman HM, Burack E (1932) Lesions of the nervous system resulting from deficiency of the vitamin B complex. Arch Pathol 13: 207–232Google Scholar

Copyright information

© Springer-Verlag 1982

Authors and Affiliations

  • E. Irle
    • 1
  • H. J. Markowitsch
    • 1
  1. 1.Dept. of PsychologyUniversity of KonstanzKonstanzGermany

Personalised recommendations