Neurochemical Research

, Volume 15, Issue 5, pp 551–558 | Cite as

Learning-induced change in neural activity during acquisition and consolidation of a passive avoidance response in the rat

  • Emer Doyle
  • Patrick M. Nolan
  • Ciaran M. Regan
Original Articles


Time-dependent alterations in neural activity have been established during the acquisition and consolidation of a stepdown passive avoidance paradigm. Change in neural activity was established by administering a glucose analogue, [3H]2-deoxyglucose, 50min prior to sacrifice and estimating perchloric acid soluble counts in nine hand dissected brain regions. Change in [3H]2-deoxyglucose uptake was closely paralleled in both trained and yoked animals for up to 40min following task acquisition however the striatum was the only area to exhibit a task-specific increase in [3H]2-deoxyglucose uptake at 20–30min after training. Longterm changes in neural activity were also apparent as the amygdala and brainstem showed increased [3H]2-deoxyglucose uptake at the 24h time point. No further paradigm-specific changes were apparent at 48 h. These findings are concluded to suggest that the striatum is involved in the early events of acquiring a passive avoidance response and the amygdala and brainstem during the later events.

Key Words

memory/learning passive avoidance deoxyglucose striatum amygdala brainstem 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Beatty, R. F., Bierley, R. A., and Rush, J. R. 1985. Spatial memory in rats: electroconvulsive shock selectively disrupts working memory but spares reference memory. Behav Neural Biol 44:403–414.PubMedGoogle Scholar
  2. 2.
    Berman, R. F., Kesner, R. P., Partlow, L. M. 1978. Passive avoidance impairment in rats following cycloheximide injection into the amygdala. Brain Res 158:171–178.Google Scholar
  3. 3.
    Bryan, Jr. R. M., Lehman, R. A. W., 1988. Cerebral glucose utilisation after aversive conditioning and during conditioned fear in the rat. Brain Res 444:17–24.PubMedGoogle Scholar
  4. 4.
    Chrobak, J. J., Hanin, I., Schmechel, D. E., Walsh, T. J. 1988. AF64A-induced working memory impairment: behavioural, neurochemical and histological correlates. Brain Res 463:107–117.PubMedGoogle Scholar
  5. 5.
    Collins, R. C., McCandless, D. W., Wagman, I. L. 1987. Cerebral glucose utilisation: Comparison of carbon-14 deoxyglucose and (6-carbon-14) glucose quantitative autoradiography. J Neurochem 49:1564–1570.PubMedGoogle Scholar
  6. 6.
    Davis, H. P., Squire, L. R. 1984. Protein biosynthesis and memory: a review. Psychol Bull 96:518–559.PubMedGoogle Scholar
  7. 7.
    Delanoy, R. L., Dunn, A. J. 1978. Mouse brain deoxyglucose uptake after footshock, ACTH analogues, α-MSH, corticosterone or lysine vasopressin. Pharmacol Biochem and Behavior 9:21–26.Google Scholar
  8. 8.
    Gjedde, A. 1987. Does deoxyglucose uptake in the brain reflect energy metabolism? Biochem Pharmacol 36:1853–1861.PubMedGoogle Scholar
  9. 9.
    Gold, P. E. 1986. The use of avoidance training in studies of modulation of memory storage. Behav Neural Biol 46:87–98.PubMedGoogle Scholar
  10. 10.
    Gonzalez-Lima, F., Scheich, H. 1986. Classical conditioning of tone signaled bradycardia modifies 2-deoxyglucose uptake patterns in cortex, thalamus, habenula, caudate-putamen and hippocampal formation. Brain Res 363:239–256.PubMedGoogle Scholar
  11. 11.
    Greenough, W. T., Chang, F. L. F. 1985. Synaptic structural correlates of information storage in mammalian nervous systems. In Cotman C. W. (ed) “Synaptic Plasticity”. New York: Guilford Press pp335–372.Google Scholar
  12. 12.
    Hargreaves, R. J., Eley, B. P., Moorhouse, S. R., Pelling, D. 1988. Regional cerebral glucose metabolism and blood flow during the silent phase of methylmercury neurotoxicity in rats. J Neurochem 51:1350–1355.PubMedGoogle Scholar
  13. 13.
    Hirofumi, N., Yamamoto, Y. L., Diksic, M., Matsuda, H., Takara, E., Meyer, E., Redies, C. 1987: Time-dependent changes of lumped and rate constants in the deoxyglucose method in experimental cerebral ischemia. J Cereb Blood Flow Metab 7(5):640–648.PubMedGoogle Scholar
  14. 14.
    Horn, G., McCabe, B. J., and Bateson, P. P. G. 1979. An autoradiographic study of the chick brain after imprinting. Brain Res 168:361–373.PubMedGoogle Scholar
  15. 15.
    Jay, T. M., Jouvet, M., Des Rosier, M. H. 1985. Local cerebral glucose utilisation in the free moving mouse: a comparison during two stages of the activity-rest cycle. Brain Res 342:297–306.PubMedGoogle Scholar
  16. 16.
    Kohsaka, S-I., Takamatsu, K., Aoki, E., Tsukada, Y. 1979. Metabolic mapping of chick brain after imprinting using (14C)2-deoxyglucose technique. Brain Res 172:539–544.PubMedGoogle Scholar
  17. 17.
    Kossut, M., Rose, S. P. R. 1984. Differential 2-deoxyglucose uptake into the chick brain structures during passive avoidance training. Neurosci 12:971–977.Google Scholar
  18. 18.
    Lynch, G., Baudry, M. 1984. The biochemistry of memory: a new and specific hypothesis. Science 224:1057–1063.PubMedGoogle Scholar
  19. 19.
    Maier, V., Scheich, H. 1983. Acoustic imprinting leads to differential 2-deoxy-D-glucose uptake in the chick forebrain. Proc Natl Acad Sci USA 80:3860–3864.PubMedGoogle Scholar
  20. 20.
    Martinez, J. I., Curlee, P., Messing, R. B. 1982. Regional brain uptake of 2-deoxy-D-glucose following training in a discriminated Y-maze avoidance task. J Comp Physiol Psychol 96:721–724.PubMedGoogle Scholar
  21. 21.
    McGaugh, J. L. 1966. Time-dependent processes in memory storage. Science 153:1351–1358.PubMedGoogle Scholar
  22. 22.
    Morris, R. G. M., Hagan, J. J., Nadel, L., Jenson, J., Baudry, M., Lynch, G. S. 1987. Spatial learning in the rat: Impairment induced by the thiol proteinase inhibitor, leupeptin, and an analysis of 3H glutamate receptor binding in relation to learning. Behav Neural Biol 47:333–345.PubMedGoogle Scholar
  23. 23.
    Olton, D. S. 1983. Memory functions and the hippocampus. In W. Seifert (Ed) ‘Neurobiology of the hippocampus’ New York: Academic Press.Google Scholar
  24. 24.
    Plum, F., Gjedde, A., Samson, F. E. 1976. Neuroanatomical functional mapping by the radioactive 2-deoxy-D glucose method. Neurosci Res Prog Bull 14:457–518.Google Scholar
  25. 25.
    Porrino, L. J., Esposito, R. U., Seeger, T. F., Crane, A. M., Pert, A., Sokoloff, L. 1984. Metabolic mapping of the brain during rewarding self stimulation. Science 224:306–309.PubMedGoogle Scholar
  26. 26.
    Ramm, P., Frost, B. J. 1983. Regional metabolic activity in rat brain during sleep-wake activity. Sleep 6:196–216.PubMedGoogle Scholar
  27. 27.
    Reivich, M., Sokoloff, L. 1976. Application of the 2-deoxy-D-glucose method to the coupling of cerebral metabolism and blood flow. Neurosci Res Prog Bull 14:474–475.Google Scholar
  28. 28.
    Sahgal, A. 1984. A critique of the vasopressin memory hypothesis. Psychopharmacology 83:215–228.PubMedGoogle Scholar
  29. 29.
    Saji, M., and Obata, K. 1981. Stimulus-dependent labeling of cultured ganglionic cells with (14C)2-deoxyglucose. Brain Res 212:435–446.PubMedGoogle Scholar
  30. 30.
    Sarter, M., Markowitsch, T. 1985. Involvement of the amygdala in learning and memory: a critical review with emphasis on anatomical relations. Behav Neurosci 99:342–380.PubMedGoogle Scholar
  31. 31.
    Schwartzman, R. J., Greenberg, M. R., Reivich, M., Klose, K. J., Alexander, G. M. 1981. Functional metabolic mapping of a conditioned motor task in primates utilizing 2-(14C)deoxyglucose. Exp Neurol 72:153–163.PubMedGoogle Scholar
  32. 32.
    Shimada, M., Murakami, T. H., Imahayashi, T., Ozaki, H. S. 1983. Local cerebral alterations in (14C)-deoxyglucose uptake following memory formation. J Anat 136:751–759.PubMedGoogle Scholar
  33. 33.
    Sokoloff, L. 1977. Relation between physiological function and energy metabolism in the central nervous system. J Neurochem 29:13–26.PubMedGoogle Scholar
  34. 34.
    Sokoloff, L., Reivich, M., Kennedy, C., Des Rosier, M. H., Palak, C. S., Pettigrew, K. D., Sakurada, O., Shinohara, M. 1977. The 14C-deoxyglucose method of measurement of local cerebral glucose utilisation: theory, procedures and normal values in the conscious and anaesthetised albino rat. J Neurochem 28:897–916.PubMedGoogle Scholar
  35. 35.
    Squire, L. R. 1987. Memory and brain. New York and Oxford: Oxford University Press.Google Scholar

Copyright information

© Plenum Publishing Corporation 1990

Authors and Affiliations

  • Emer Doyle
    • 1
  • Patrick M. Nolan
    • 1
  • Ciaran M. Regan
    • 1
  1. 1.Department of PharmacologyUniversity CollegeDublin 4Ireland

Personalised recommendations