Skip to main content
Log in

Investigation on Acetylcholine, Aspartate, Glutamate and GABA Extracellular Levels from Ventral Hippocampus During Repeated Exploratory Activity in the Rat

Neurochemical Research Aims and scope Submit manuscript

Abstract

The extracellular levels of aspartate, glutamate, γ-aminobutyric acid (GABA), and acetylcholine (ACh) were investigated by microdialysis, coupled with HPLC, in the ventral hippocampus of rats during two 30-min exploration periods. Motor activity was monitored. During exploration I, an increase in motor activity associated with a 315% increase in aspartate, 181% in glutamate, and 264% in ACh levels, occurred during the first 10 min. The increase in GABA level reached a maximum of 257% during the second 10 min. The neurotransmitter levels returned to basal values within 40 min. During exploration II, 1 h later, a smaller increase in neurotransmitter levels and motor activity was observed. In both explorations, the increase in neurotransmitter levels was completely abolished by 1 and 3 μM TTX. A statistically significant relationship was found between neurotransmitter extracellular levels and motor activity, for aspartate and glutamate in exploration I, and for ACh in exploration I and II. In conclusion, exploratory activity is associated with or depends on the activation of neuronal systems in the ventral hippocampus releasing aspartate, glutamate, GABA, and ACh. The activation is dampened by habituation.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

REFERENCES

  1. Green, E. J., McNaughton, B. L., and Barnes, C. A. 1990. Exploration-dependent modulation of evoked responses in fascia dentata: Dissociation of motor, EEG, and sensory factors and evidence for a synaptic efficacy change. J. Neurosci. 10: 1455–1471.

    PubMed  Google Scholar 

  2. Steriade, M. and Buszaki, G. 1990. Parallel activation of thalamic and cortical neurons by brainstem and basal forebrain cholinergic systems. Pages 3–62, in Steriade, M. and Biesold, D. (eds.), Brain Cholinergic Systems, Oxford Science Publications, Oxford.

    Google Scholar 

  3. Aloisi, A. M., Casamenti, F., Scali, C., Pepeu, G., and Carli, G. 1997. Effects of novelty, pain and stress on hippocampal extracellular acetylcholine levels in male rats. Brain Res. 748:219–226.

    PubMed  Google Scholar 

  4. Ceccarelli, I., Casamenti, F., Massafra, C., Pepeu, G., Scali, C., and Aloisi, A. M. 1999. Effects of novelty and pain on behavior and hippocampal extracellular ACh levels in male and female rats. Brain Res. 815:169–176.

    PubMed  Google Scholar 

  5. Giovannini, M. G., Bartolini, L., Kopf, S. R., and Pepeu, G. 1998. Acetylcholine extracellular levels from the frontal cortex during exploratory activity. Brain Res. 784:218–227.

    PubMed  Google Scholar 

  6. Giovannini, M. G., Rakovska, A., Benton, R. S., Pazzagli, M., Bianchi, L., and Pepeu, G. 2001. Effects of novelty and habituation on acetylcholine GABA, and glutamate extracellular levels from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106:43–53.

    PubMed  Google Scholar 

  7. Saigusa, T., Tuinstra, T., Koshikawa, N., and Cools, A. R. 1999. High and low responders to novelty: Effects of a catecholamine synthesis inhibitor on novelty-induced changes in behaviour and extracellular levels of accumbal dopamine. Neuroscience 88:1153–1163.

    PubMed  Google Scholar 

  8. Day, J., Damsma, G. M., and Fibiger, H. C. 1991. Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: An in vivo microdialysis study. Pharmacol. Biochem. Behav. 38:723–729.

    PubMed  Google Scholar 

  9. Moore, H., Sarter, M., and Bruno, J. P. 1992. Age-dependent modulation of in vivo cortical acetylcholine release by benzodiazepine receptor ligands. Brain Res. 596:17–29.

    PubMed  Google Scholar 

  10. Thiel, C. M., Huston, J. P., and Schwarting, R. K. 1998. Hippocampal acetylcholine and habituation learning. Neuroscience 85:1253–1262.

    PubMed  Google Scholar 

  11. Cerbone, A. and Sadile, A. G. 1994. Behavioral habituation to spatial novelty: Interference and noninterference studies. Neurosci. Biobehav. Res. 18:497–518.

    Google Scholar 

  12. Dudai, Y. 1989. The Neurobiology of Memory. Pages 20–22. Oxford University Press, Oxford.

    Google Scholar 

  13. Dai, H., Krost, M., and Carey, R. J. 1995. A new methodological approach to the study of habituation: The use of positive and negative behavioural indices of habituation. J. Neurosci. Methods 62:169–176.

    PubMed  Google Scholar 

  14. Platel, A. and Porsolt, R. D. 1982. Habituation and exploratory activity in mice: A screening test for memory enhancing drugs. Psychopharmacol. (Berl.) 78:346–352.

    Google Scholar 

  15. Acquas, A., Wilson, H. C., and Fibiger, H. C. 1996. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine extracellular levels: Effects of novelty, habituation and fear. J. Neurosci. 16:3088–3096.

    Google Scholar 

  16. Narahashi, T. 1974. Chemicals as tools in the study of excitable membranes. Physiol. Rev. 54:813–888.

    PubMed  Google Scholar 

  17. Paxinos, G. and Watson, G. 1982. The Rat Brain in Stereotaxic Coordinates, Academic Press, New York.

    Google Scholar 

  18. Giovannini, M. G., Mutolo, D., Bianchi, L., Michelassi, A., and Pepeu, G. 1994. NMDA receptor antagonists decrease GABA outflow from the septum and increase acetylcholine outflow from the hippocampus: A microdialysis study. J. Neurosci. 14:1358–1365.

    PubMed  Google Scholar 

  19. Bianchi, L., Della Corte, L., and Tipton, K. F. 1999. Simultaneous determination of basal and evoked output levels of aspartate, glutamate, taurine, and 3-aminobutyric acid during microdialysis and from superfused brain slice. J. Chromatogr. B. Biomed. Sci. Appl. 723:47–59.

    PubMed  Google Scholar 

  20. Bland, S. T., Gonzales, R. A., and Schallert, T. 1999. Movement-related glutamate levels in rat hippocampus, striatum and sensorimotor cortex. Neurosci. Lett. 277:19–122.

    Google Scholar 

  21. Mizuno, T., Endo, Y., Arita, J., and Kimura, F. 1991. Acetylcholine release in the rat hippocampus as measured by the microdialysis method correlates with motor activity and exhibits a diurnal variation. Neuroscience 44:607–612.

    PubMed  Google Scholar 

  22. Hock, B. J. and Bunsey, M. D. 1998. Differential effects of dorsal and ventral hippocampal lesions. J. Neurosci. 18:7027–7032.

    PubMed  Google Scholar 

  23. Jung, M. W., Wiener, S. I., and McNaughton, B. 1994. Comparison of spatial firing characteristics of unit in dorsal and ventral hippocampus of the rat. J. Neurosci. 14:7347–7356.

    PubMed  Google Scholar 

  24. Krettek, J. E. and Price, J. L. 1977. Projection from the amygdala complex and adjacent olfactory structure to the entorhinal cortex and to the subiculum in the rat and cat. J. Comp. Neurol. 172:723–752.

    PubMed  Google Scholar 

  25. Van Groen, T. and Wyss, J. M. 1990. Extrinsic projection from area CA1 of the rat hippocampus: Olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J. Comp. Neurol. 302:515–528.

    PubMed  Google Scholar 

  26. Milner, T. A., Loy, R., and Amaral, D. G. 1983. An anatomical study of the development of the septo-hippocampal projection in the rat. Dev. Brain Res. 8:343–371.

    Google Scholar 

  27. Amaral, D. G. and Kurz, J. 1985. An analysis of the origins of the cholinergic and non cholinergic septal projections to the hippocampal formation of the rat. J. Comp. Neurol. 240: 37–59.

    PubMed  Google Scholar 

  28. Garcia Ruiz, A. J., Zimbelli, M., LA Porta, C., Ladinski, H., and Consolo, S. 1993. Differences between the rat dorsal and ventral hippocampus in muscarinic receptors agonist binding and interaction with phospholipase C. Eur. J. Pharmacol. 244:125–131.

    PubMed  Google Scholar 

  29. Paylor, R., Zhao, Y., Libbey, M., Westphal, H., and Crawley, J. N. 2001. Learning impairment and motor dysfunctions in adult Lhx5-deficient mice displaying hippocampal disorganization. Physiol. Behav. 73:781–792.

    PubMed  Google Scholar 

  30. Shin, J. and Talnov, A. 2001. A single trial analysis of hippocampal theta frequency during nonsteady wheel running in rats. Brain Res. 908:104–105.

    Google Scholar 

  31. Carlsson, M. and Swensson, A. 1990. Interfering with gluta-matergic neurotransmission by means of NMDA antagonist administration discloses the locomotor stimulatory potential of other transmitter systems. Pharmacol. Biochem. Behav. 36:45–50.

    PubMed  Google Scholar 

  32. Bartolini, L., Casamenti, F., and Pepeu, G. 1996. Aniracetam restores object recognition impaired by age, scopolamine, and nucleus basalis lesions. Pharmacol. Biochem. Behav. 53:277–283.

    PubMed  Google Scholar 

  33. Timmerman, W. and Westerink, B. H. C. 1997. Brain microdialysis of GABA and glutamate: What does it signify? Synapse 27:42–261.

    Google Scholar 

  34. Corradetti, R., Moneti, G., Moroni, F., Pepeu, G., and Wieraszko, A. 1983. Electrical stimulation of the stratum radiatum increases the extracellular levels and neosynthesis of aspartate, glutamate, and gamma-aminobutyric acid in rat hippocampal slices. J. Neurochem. 41:1518–1525.

    PubMed  Google Scholar 

  35. Silva, E., Quinones, B., Freund, N., Gonzales, L. E., and Hernandez, L. 2001. Extracellular glutamate, aspartate and arginine increase in the ventral posterolateral thalamic nucleus during nociceptive stimulation. Brain Res. 923:45–49.

    PubMed  Google Scholar 

  36. Morris, R. G. M., Anderson, E., Lynch, G. S., and Baudry, M. 1986. Selective impairment of learning and blockade of long term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774–776.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bianchi, L., Ballini, C., Colivicchi, M.A. et al. Investigation on Acetylcholine, Aspartate, Glutamate and GABA Extracellular Levels from Ventral Hippocampus During Repeated Exploratory Activity in the Rat. Neurochem Res 28, 565–573 (2003). https://doi.org/10.1023/A:1022881625378

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022881625378

Navigation