Summary
The influence of cholinergic and dopaminergic agents on the acquisition of a passive avoidance response in the rat is demonstrated. Trifluoperazine (0.12 mg/kg), a dopamine antagonist, inhibited task acquisition when present during training or later, during consolidation, at the 10–12 h posttraining period and at no other intervening time point. Induction of amnesia was dose-dependent and was not apparent when the dose exceeded 0.12 mg/ kg. This effect appears to be due to an increase in dopamine release through presynaptic receptor antagonism as similar results could be obtained by the administration of apomorphine (0.5 mg/kg), a dopamine agonist, and this effect could be antagonized by the D 1 receptor selective antagonist SCH-23390. Scopolamine (0.15 mg/kg), a muscarinic antagonist, impaired acquisition of the passive avoidance response when administered during training and, separately, at the 6 h post-training period. This could not be attributed to presynaptic antagonism as oxotremorine (0.2 mg/kg), a muscarinic agonist, had no amnesic action. Administration of apomorphine or scopolamine during training and at the appropriate post-training period prevented subsequent paradigm-specific increases of neural cell adhesion molecule sialylation state in hippocampal immunoprecipitates obtained at 24 h after task acquisition and 4 h following intraventricular infusion of the labelled sialic acid precursor — N-acetyl-D-mannosamine. Oxotremorine alone did not influence neural cell adhesion molecule sialylation state. These observations provide further evidence of a regulatory role for neural cell adhesion molecule sialylation state in information storage processes.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- NCAM :
-
neural cell adhesion molecule
- RSA :
-
relative specific activity
- SDS-PAGE :
-
sodium dodecyl sulphate polyacrylamide gel electrophoresis
- TCA :
-
trichloroacetic acid
- TFP :
-
trifluoperazine
References
Bailey CH, Chen M, Keller F, Kandel ER (1992) Serotonin-mediated endocytosis of apCAM: an early step of learning-related synaptic growth inAplysia. Science 256: 645–649
Barratti CM, Introini IB, Huygens P (1984) Possible interaction between central cholinergic muscarinic and opioid peptidergic systems during memory consolidation. Behav Neural Biol 40: 155–169
Beninger RJ (1983) The role of dopamine in locomotor activity and learning. Brain Res Rev 6: 173–196
Bracs PU, Gregory P, Jackson DM (1984) Passive avoidance in rats: disruption by dopamine applied to the nucleus accumbens. Psychopharmacology 83: 70–75
Breen KB, Regan CM (1988) Differentiation-dependent sialylation of individual neural cell adhesion molecule polypeptides during postnatal development. J Neurochem 50: 712–716
Brown TH, Chapman PF, Kariss EW, Keenan CL (1988) Long-term potentiation. Science 242: 724–728
Castellano C, Cestari V, Cabib S, Puglisi-Allegra S (1991) Post-training dopamine receptor agonists and antagonists affect memory storage in mice irrespective of their selectivity for D 1 or D2 receptors. Behav Neural Biol 56: 283–291
Caulfield MP, Higgins GA, Straughan DW (1983) Central administration of the muscarinic receptor subtype-selective antagonist pirenzepine selectively impairs passive avoidance learning in the mouse. J Pharm Pharmacol 35: 131–132
Chang F-LF, Greenough WT (1984) Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res 309: 35–46
Changeux J-P, Danchin A (1976) Selective stabilisation of synapses as a mechanism for the specification of neuronal networks. Nature 264: 705–712
Cheal ML (1984) Differential effect of haloperidol and clozapine on attention. Psychopharmacology 84: 268–271
Doyle E, Bruce MT, Breen KC, Smith DC, Anderton B, Regan CM (1990 a) Intraventricular infusion of antibodies to amyloid-β-protein precursor impairs the acquisition of a passive avoidance response in the rat. Neurosci Lett 115: 97–102
Doyle E, Nolan P, Regan CM (1990 b) Learning-induced change in neural activity during acquisition and consolidation of a passive avoidance in the rat. Neurochem Res 15: 551–558
Doyle E, Nolan P, Bell R, Regan CM (1992 a) Neurodevelopmental events underlying information acquisition and storage. Network 3: 89–94
Doyle E, Nolan P, Bell R, Regan CM (1992 b) Hippocampal NCAM 180 transiently increases sialylation state during the acquisition and consolidation of a passive avoidance response in the adult rat. J Neurosci Res 31: 513–523
Doyle E, Nolan PM, Bell R, Regan CM (1992 c) Intraventricular infusions of anti-neural cell adhesion molecules in a discrete posttraining period impair consolidation of a passive avoidance response in the rat. J Neurochem 59: 1570–1573
Fernandez-Tome MP, Sanchez-Blazquez P, del Rio J (1979) Impairment by apomorphine of one trial passive avoidance learning in mice: the apposing roles of the dopamine and noradrenaline systems. Psychopharmacology 61: 43–47
Fibiger HC, Fibiger AP, Phillips AG (1975) Haloperidol-induced disruption of conditioned avoidance responding: alteration by prior training or by anticholinergic drugs. Eur J Pharmacol 30: 309–314
Flood JF, Cherkin A (1986) Scopolamine effects on memory retention in mice: a model of dementia? Behav Neural Biol 45: 169–184
Gower AJ (1987) Enhancement by secoverine and physostigmine on retention of passive avoidance response in mice. Psychopharmacology 91: 326–329
Gray EG, Whittaker VP (1962) The isolation of nerve endings from brain — an electron-microscope study of cell fragments derived by homogenisation and centrifugation. J Anat 96: 76–87
Greenough WT, Bailey CH (1988) The anatomy of memory: convergence of results across a diversity of tests. Trends Neurosci 11: 142–147
Hagan JJ, Tweedie F, Morris RGM (1986) Lack of task specificity and absence of post-training effects of atropine on learning. Behav Neurosci 100: 483–493
Ichihara K, Nabeshima T, Kameyama T (1988 a) Effects of haloperidol, sulpiride and SCH 23390 on passive avoidance learning in mice. Eur J Pharmacol 151: 435–442
Ichihara K, Nabeshima T, Kameyama T (1988 b) Opposite effects induced by low and high doses of apomorphine on single-trial passive avoidance learning in mice. Pharmacol Biochem Behav 30: 107–113
Ichihara K, Nabeshima T, Kameyama T (1989) Differential effects of pimozide and SCH 23390 on acquisition of learning in mice. Eur J Pharmacol 164: 189–195
Introini-Collison IB, McGaugh JL (1988) Modulation of memory by post-training epinephrine: involvement of cholinergic mechanism. Psychopharmacology 94: 379–385
Jork K, Lossner B, Matthies H (1979) The influence of cholinergic transmitter substances on the incorporation of (14C)-leucine and (3H)-fucose into the total proteins of hippocampus in vivo and in vitro. Pharmacol Biochem Behav 11: 243–245
Jork R, Grecksch G, Jirka M, Lossner B, Matthies H (1980 a) Apomorphine and glycoprotein synthesis in rat hippocampus. Pharmacol Biochem Behav 12: 317–318
Jork R, Lossner B, Matthies H (1980 b) The influence of dopamine on the incorporation of different sugars into total proteins of hippocampal slices. Pharmacol Biochem Behav 13: 303–304
Jork R, Smalla K-H, Karsten U, Grecksch G, Ruthrich H-L, Matthies H (1991) Monoclonal antibody specific for histo-blood group antigens H (types 2 and 4) interferes with long-term memory formation in rats. Neurosci Res Commun 8: 21–27
Lee KS, Schottler F, Oliver M, Lynch G (1980) Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus. J Neurophysiol 44: 247–258
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin reagent. J Biol Chem193: 265–275
Mayford M, Barzilai A, Keller F, Schacher S, Kandel ER (1992) Modulation of an NCAM- related adhesion molecule with long-term synaptic plasticity inAplysia. Science 256: 638–644
Meyers B (1965) Some effects of scopolamine on a passive avoidance response in rats. Psychopharmacologia 8: 111–119
Niemegeers CJE, Verbruggen FJ, Janssen PAJ (1969) The influence of various neuroleptic drugs on shock avoidance responding in rats. Psychopharmacologia 16: 161–174
Nolan PM, Bell R, Regan CM (1987 a) Acquisition of a brief behavioural experience in the rat is inhibited by the brain-specific monoclonal antibody, F 3-87-8. Neurosci Lett 79: 346–350
Nolan PM, Bell R, Regan CM (1987 c) Acquisition of a brief behavioural experience in the presence of neuron-specific and D 2-CAM/N-CAM-specific antisera. Neurochem Res 12: 619–624
Oscos A, Martimez Jr JL, McGaugh JL (1988) Effects of post-trainingd-amphetamine on acquisition of an appetitive autoshaped lever press response in rats. Psychopharmacology 95: 132–134
Persohn E, Pollerberg GE, Schachner M (1989) Immunoelectronmicroscopic localization of the 180 kDa component of the neural cell adhesion molecule NCAM in postsynaptic membranes. J Comp Neurol 288: 92–100
Plioplys AV, Hemmens SE, Regan CM (1990) Expression of a NCAM serum fragment is depressed in autism. J Neuropsychiat Clin Neurosci 2: 413–417
Prado-Alcala RA, Fernandez-Samblancat M, Solodkin M (1985) Injections of atropine into caudate nucleus impair the acquisition of and maintenance of passive avoidance. Pharmacol Biochem Behav 22: 243–247
Quatermain D, Judge ME, Leo P (1988) Attenuation of forgetting by pharmacological stimulation of aminergic neurotransmitter systems. Pharmacol Biochem Behav 30: 77–81
Regan CM (1991) Regulation of neural cell adhesion molecule (NCAM) sialylation state. Int J Biochem 23: 513–523
Rose SPR, Jork R (1987) Long-term memory formation in chicks is blocked by 2-deoxygalactose, a fucose analog. Behav Neural Biol 48: 246–258
Rush DK (1988) Scopolamine amnesia of passive avoidance: a deficit of information acquisition. Behav Neural Biol 50: 255–274
Sarter M (1991) Taking stock of cognition enhancers. Trends Pharmacol Sci 12: 456–461
Squire LR, Davis HP (1981) The pharmacology of memory: a neurobiological perspective. Annu Rev Pharmacol Toxicol 21: 323–356
Stanton PK, Sarvey JM, Moskal JR (1987) Inhibition of the production and maintenance of long-term potentiation in rat hippocampal slices by a monoclonal antibody. Proc Natl Acad Sci USA 84: 1684–1688
Staubli U, Vanderklish P, Lynch G (1990) An inhibitor of integrin receptors blocks long-term potentiation. Behav Neural Biol 53: 1–5
Stewart MG, Rose SPR, King TS, Gabbott PLA, Bourne R (1984) Hemispheric asymmetry of synapses in chick medial hyperstriatum ventrale following passive avoidance training: a sterological investigation. Dev Brain Res 12: 261–269
Stewart MG, Csillag A, Rose SPR (1987) Alterations in synaptic structure in the paleostriatal complex of the domestic chick,Gallus domesticus, following passive avoidance training. Brain Res 426: 69–81
Wenzel J, Kammerer E, Kirsche W, Matthies H, Wenzel M (1980) Electron microscopic and morphometric studies on synaptic plasticity in the hippocampus of the rat following conditioning. J Hirnforsch 21: 647–654
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Doyle, E., Regan, C.M. Cholinergic and dopaminergic agents which inhibit a passive avoidance response attenuate the paradigm-specific increases in NCAM sialylation state. J. Neural Transmission 92, 33–49 (1993). https://doi.org/10.1007/BF01245160
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01245160