Abstract
Behavioral manipulations that alleviate forgetting in a complex maze task are paralleled by pharmacological manipulations which modulate noradrenergic activity. Increased noradrenergic activity is observed following prior exposure to contextual reminder cues. It is proposed that the facilitated retrieval reflects a conditioned arousal and an enhanced attention to discriminative stimuli mediated by the noradrenergic response. Failure to find learning and memory retrieval deficits in rats that are depleted of noradrenaline is discussed in terms of functional recovery after lesions.
Article PDF
Similar content being viewed by others
References
Adrien, J., Buisseret, P., Frégnac, Y., Gary-Bobo, D., Imbert, M., Tassin, J. P., & Trotter, Y. (1982). Noradrénaline et plasticité du cortex visuel du chaton: Un réexamen. Comptes-Rendus de I’Academie des Sciences (Paris), 295, 745–750.
Amaral, P. G., & Sinnamon, H. M. (1977). The locus coeruleus: Neurobiology of a central noradrenergic nucleus. Progress in Neurobiology, 1, 147–196.
Archer, T., Cotic, T., & Jarbe, T. U. (1982). Attenuation of the context effect and lack of unconditioned stimulus-preexposure effect in taste-aversion learning following treatment with DSP4, the selective noradrenaline neurotoxin. Behavioral & Neural Biology, 35, 159–173.
Archer, T., Mohammed, A. K., & Järbe, T. U. (1983). Latent inhibition following systemic DSP4: Effects due to presence and absence of contextual cues in taste aversion learning. Behavioral & Neural Biology, 38, 287–306.
Aston-Jones, G. (1985). Behavioral functions of locus coeruleus derived from cellular attributes. Physiological Psychology, 13, 118–126.
Aston-Jones, G., & Bloom, F. (1981). Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non noxious environmental stimuli. Journal of Neuroscience, 1, 887–900.
Chiodo, A., Acheson, A., Zigmond, J., & Stricker, M. (1983). Subtotal destruction of central noradrenergic projections increases the firing rate of locus coeruleus cells. Brain Research, 264, 123–126.
Crow, T. J., Deakin, J., File, S. E., Longden, A., & Wendlandt, S. (1978). The locus coeruleus noradrenergic system: Evidence against a role in attention, habituation, anxiety, and motor activity. Brain Research, 155, 249–261.
Daw, N. W., Rader, R., Robertson, T., & Videen, T. (1983). Do short term and long term depletion of noradrenaline have different effects on visual deprivation in the latter visual cortex. Journal of Neuroscience, 4, 1354–1360.
Descarries, L., Watkins, K., & Lapierre, Y. (1977). Noradrenergic axon terminals in the cerebral cortex of rat. III. Topometric ultrastructural analysis. Brain Research, 133, 197–222.
Deweer, B., & Sara, S. J. (1984). Background stimuli as a reminder after spontaneous forgetting: Role of duration of cuing and cuing-test interval. Animal Learning & Behavior, 12, 238–247.
Deweer, B., Sara, S. J., & Hars, B. (1980). Contextual cues and memory retrieval in rats: Alleviation of forgetting by a pretest exposure to background stimuli. Animal Learning & Behavior, 8, 265–272.
Dismukes, E. (1977). New look at the aminergic nervous system. Nature, 269, 557–558.
Gervais, R., & Pager, J. (1983). Olfactory bulb excitability selectively modified in behaving rats after local 6-hydroxydopamine treatment. Behavioural Brain Research, 9, 165–179.
Gisquet-Verrier, P., Dekeyne, A., & Alexinsky, T. (1985). Memory reorganization over time as revealed by interaction between type of pre-test cueing and length of retention interval. In B. Will, P. Schmitt, & R. Dalrymple-Alford (Eds.), Brain plasticity, learning and memory. New York: Plenum Press.
Goldberg, M., & Robertson, D. (1983). Yohimbine: A pharmacological probe for study of the alpha2-adrenoreceptor. Pharmacological Reviews, 35, 143–180.
Guibert, A., Sara, S. J., & Leviel, V. (1983). [Correlation between cortical and hippocampal levels of noradrenaline and latency and duration of post decapitation clonus after treatment with DSP4.] Unpublished manuscript, CNRS, Gif-sur-Yvette, France.
Hallman, H., Sundstrom, D., & Jonsson, G. (1984). Effects of the noradrenaline neurotoxin DSP4 on monoamine neurons and their transmitter turnover in rat CNS. Journal of Neural Transmission, 60, 89–102.
Harik, S. (1984). Locus coeruleus lesion by local 6-hydroxydopamine infusion causes marked and specific destruction of noradrenergic neurons, long-term depletion of neuropinephrine and the enzymes that synthetize it, and enhanced dopaminergic mechanisms in the ipsilateral cortex. Journal of Neuroscience, 4, 699–707.
Harik, I., Duckrow, R., La Manna, C., Rosenthal, M., Sharma, K., & Banerjee, P. (1981). Cerebral compensation for chronic noradrenergic denervation induced by locus coeruleus lesion: Recovery of receptor binding, isoproterenol-induced adenylate cyclase activity and oxidative metabolism. Journal of Neuroscience, 6, 641–649.
Harrell, L., Barlow, T., Miller, M., Haring, J., & Davis, J. (1984). Facilitated reversal learning of a spatial memory task by medial septal injection of 6-hydroxydopamine. Experimental Neurology, 85, 69–77.
Hobson, J. (1980). Toward a cellular neurophysiology of the reticular formation: Conceptual and methodological milestones. In J. Hobson & M. Brazier (Eds.), The reticular formation revisited. New York: Raven Press.
Kasamatsu, T., & Pettigrew, J. (1976). Depletion of brain catecholamines: Failure of ocular dominance shift after monocular occlusion in kittens. Science, 194, 206–209.
Kasamatsu, T., Pettigrew, J., & Ary, M. (1979). Restoration of visual cortical plasticity by local microperfusion of norepinephrine. Journal of Comparative Neurology, 185, 163–182.
Kasamatsu, T., & Shirokawa, T. (1985). Are beta adrenoreceptors involved in visuocortical plasticity? In B. Will, P. Schmitt, & R. Dalrymple-Alford (Eds.), Brain plasticity, learning and memory. New York: Plenum Press.
Kety, S. (1970). The biogenic amines in the central nervous system: Their possible roles in arousal emotion and learning. In F. O. Schmitt (Ed.), The neurosciences (pp. 324–336). New York: Rockefeller University Press.
Konorski, J. (1967). Integrative activity of the brain. Chicago: Chicago University Press.
Kupalov, P. (1961). Some normal and pathological processes in the brain. In N. Kline (Ed.), Pavlovian Conference on Higher Nervous Activity. Annals of the New York Academy of Sciences, 92, 1046–1053.
La Manna, J., Harik, S., Light, A., & Rosenthal, M. (1981). Norepinephrine depletion alters cerebral oxidative metabolism in the “active” state. Brain Research, 204, 87–101.
Lorden, J. F., Rickert, E., Dawson, R., & Pellymounter, M. (1980). Forebrain norepinephrine and the selective processing of information. Brain Research, 190, 569–573.
Madar, Y., & Segal, M. (1980). The functional role of the noradrenergic system in the visual cortex: Activation of the noradrenergic pathway. Experimental Brain Research, 41, 814.
Mason, S., & Iversen, S. (1978). Reward, attention and the dorsal noradrenergic bundle. Brain Research, 150, 135–148.
Moore, R. Y. (1980). The reticular formation: Monoamine neuron system. In J. A. Hobson & M. A. Brazier (Eds.), The reticular formation revisited (pp. 67–81). New York: Raven Press.
Olpe, H. R., Jones, R., & Steinmann, M. (1983). The locus coeruleus: Actions of psychoactive drugs. Experientia, 39, 242–249.
Olschowka, J., Molliver, M., Grzanna, R., Rice, F., & Coyle, J. (1981). Ultrastructural demonstration of noradrenergic synapses in the rat central nervous system by dopamine-B-hydroxylase immunocytochemistry. Journal of Histochemistry & Cytochemistry, 29, 271–280.
Pickles, J. O. (1976). The noradrenaline-containing innervation of the cochlear nucleus and the detection of signals in noise. Brain Research, 105, 591–596.
Pisa, M., & Fibiger, H. C. (1983). Evidence against a role of the rat’s dorsal noradrenergic bundle in selective attention and place memory. Brain Research, 272, 319–329.
Quartermain, D. (1983). The role of catecholamines in memory processing. In J. A. Deutsch (Ed.), The physiological basis of memory (2nd ed). New York: Wiley.
Reader, T. (1983). The role of catecholamines in neuronal excitability. In A. R. Liss (Ed.), Basic mechanisms of neuronal hyperexcitability (pp. 281–321). New York: Liss.
Robbins, T. W. (1984). Cortical noradrenaline, attention and arousal. Psychological Medicine, 14, 13–21.
Robbins, T. W., & Everitt, H. B. (1985). Noradrenaline and selective attention. In B. Will, P. Schmitt & R. Dalrymple-Alford (Eds.), Brain plasticity, learning and memory, New York: Plenum Press.
Ross, S. (1976). Long-term effects of N-2-chloroethyl-N-ethyl-2-bromobenzylamine hydrochloride on noradrenergic neurons in the rat brain and heart. British Journal of Pharmacology, 58, 521–527.
Sara, S. J. (1985). Noradrenergic modulation of selective attention: Its role in memory retrieval. In D. Olton, E. Gamzu, & S. Corkin (Eds.), Memory dysfunctions: An integration of animal and human research from clinical and preclinical perspectives. Annals of the New York Academy of Sciences, 444, 178–193.
Sara, S. J., & Dekeyne, A. (1985). [Role of intramaze visual cues in performance of a “spatial” discrimination multi unit maze task.] Unpublished manuscript, CNRS, Gif-sur-Yvette, France.
Sara, S. J., & Deweer, B. (1982). Memory retrieval enhanced by amphetamine after a long retention interval. Behavioral & Neural Biology, 26, 146–160.
Sara, S. J., Deweer, B., & Hars, B. (1976). Forgetting as a lapse not a loss: Facilitation of retrieval by a reminder. Bulletin d’Information de la Societe Beige de Psychologie, 1, 22–25.
Sara, S. J., Deweer, B., & Hars, B. (1980). Reticular stimulation facilitates retrieval of a “forgotten” maze habit. Neurosciences Letters, 18, 211–217.
Sara. S. J., Guibert, B., & Leviel, V. (1985). Conditioned increase in hippocampal MHPG in response to contextual stimuli associated with a brief, mild, footshock. In Fifth European Winter Conference on Brain Research. (Abstract)
Sara, S. J., & LeRoch, K. (1985) [Yohimbine effects on spontaneous locomotor activity, exploration and neophobia as measured in the role-board: A dose-response study.] Unpublished manuscript, CNRS, Gif-sur-Yvette, France.
Segal, M. (1981). The action of norepinephrine in the rat hippocampus: Intracellular studies in the slice preparation. Brain Research, 206, 107–128.
Segal, M. (1982). The action of serotonin in the rat hippocampus. In B. Haber (Ed.), Serotonin-current aspects of neurochemistry and function. New York: Plenum Press.
Segal, M. (1985). Mechanisms of action of noradrenaline in the brain. In B. Will, P. Schmitt, & R. Dalrymple-Alford (Eds.), Brain plasticity, learning and memory. New York: Plenum.
Segal, M., & Bloom, F. (1976). Norepinephrine in the rat hippocampus. III. Stimulation of nucleus locus coeruleus in the awake rat. Brain Research, 107, 499–511.
Segal, M., & Edelson, A. (1978). Effects of priming stimulation of catecholamine containing nuclei in rat brain on runway performance. Brain Research Bulletin, 3, 203–206.
Segal, M., Sagie, B., & Mayevsky, A. (1980). Metabolic changes induced in rat hippocampal slices by norepinephrine. Brain Research, 202, 387–399.
Swann, C. (1984). Brain (Na+, K+)-ATPase and noradrenergic function: Recovery of enzyme activity after norepinephrine depletion. Brain Research, 321, 323–326.
Waterhouse, B. D., Moises, H., & Woodward, D. (1980). Locus coeruleus stimulation potentiates somatosensory cortical neuronal responses to different synaptic inputs. Society of Neuroscience Abstracts, 6, 448.
Woodward, D. J., Moises, H. C., Waterhouse, B., Hoffer, B., & Freedman, R. (1979). Modulatory actions of norepinephrine in the central nervous system. Federation Proceedings, 38, 2109–2116.
West, M. O., & Woodward, D. J. (1984). A technique for microion-tophoretic study of single neurons in the freely moving rat. Journal of Neuroscience Methods, 11, 179–186.
Author information
Authors and Affiliations
Additional information
This article is based on a roundtable discussion held at the European Brain and Behavior Society Workshop on Brain Plasticity, Learning and Memory held August 30–September 1, 1984, in Strasbourg, France.
The experiments reported here were carried out with the technical assistance of Michele Dumas. Neurochemical analysis was performed by Bernard Guibert and Vincent Leviel. The research was funded by a grant from the Ministry of Industry and Research of France, ATP 82 F 0689. The author thanks Serge Laroche, William McEntee, and Menahem Segal for helpful comments on an earlier version of this manuscript.
Rights and permissions
About this article
Cite this article
Sara, S.J. The locus coeruleus and cognitive function: Attempts to relate noradrenergic enhancement of signal/noise in the brain to behavior. Psychobiology 13, 151–162 (1985). https://doi.org/10.3758/BF03326515
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.3758/BF03326515