Skip to main content
SpringerLink
Log in

Similar ameliorating effects of benzomorphans and 5-HT2 antagonists on drug-induced impairment of passive avoidance response in mice: comparison with acetylcholinesterase inhibitors

  • Original Investigations
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Mice were trained to avoid electric shocks by means of step-down type passive avoidance learning tasks, and memory retention was measured 24 h after the training session. Memory impairment (amnesia) was produced by administering eitherp-chloroamphetamine (PCA), a serotonin (5-HT) releaser or scopolamine (SCOP), a muscarinic cholinoceptor antagonist, 30 min prior to the training session. Benzomorphans, 5-HT2 antagonists and acetylcholinesterase (AChE) inhibitors were administered immediately after the training session. PCA- but not SCOP-induced amnesia was attenuated by the post-training administration of two benzomorphans, (+)N-allylnormetazocine ((+)SKF-10,047) and (±)pentazocine ((±)PTZ). Similarly, PCA-induced amnesia was reversed by the post-training administration of 5-HT2 antagonists, ritanserin (RIT) and mianserin (MIA), but SCOP-induced amnesia was not. However, the AChE inhibitors, tetrahydroaminoacridine (THA) and physostigmine (PHY) attenuated both PCA- and SCOP-induced amnesia when administered immediately after the training session. These results indicated that benzomorphans and 5-HT2 antagonists have antiamnestic effects in mice, as do AChE inhibitors. In addition, it is interesting that the patterns of ameliorating effect of benzomorphans were similar to those of 5-HT2 antagonists, which differ from those of AChE inhibitors.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ajima A, Kato T (1988) Brain dialysis: detection of acetylcholine release in the striatum, hippocampus and frontal cortex of freely moving rats. Biogenic Amines 5:461–464

    Google Scholar 

  • Altman HJ, Normile HJ (1986) Enhancement of the memory of a previously learned aversive habit following pre-test administration of a variety of serotonergic antagonists in mice. Psychopharmacology 90:24–27

    Google Scholar 

  • Altman HJ, Normile HJ (1987) Different temporal effects of serotonergic antagonists on passive avoidance retention. Pharmacol Biochem Behav 28:353–359

    Google Scholar 

  • Archer T, Ögren SO, Johansson C (1981) The acute effect ofp-chloroamphetamine on the retention of fear conditioning in the rat: evidence for a role of serotonin in memory consolidation. Neurosci Lett 25:75–81

    Google Scholar 

  • Baratti CM, Huygens P, Mino J, Merlo A, Gardella J (1979) Memory facilitation with posttrial injection of oxotremorine and physostigmine in mice. Psychopharmacology 64:85–88

    Google Scholar 

  • Baratti CM, Introini IB, Huygens P (1984) Possible interaction between central cholinergic muscarinic and opioid peptidergic systems during memory consolidation in mice. Behav Neural Biol 40:155–169

    Google Scholar 

  • Brog JS, Beinfeld MC (1990) Inhibition of carbachol-induced inositol phosphate accumulation by phencyclidine, phencyclidine-like ligands andsigma agonists involves blockade of the muscarinic cholinergic receptor: a novel dioxadrol-preferring interaction. J Pharmacol Exp Ther 254:952–956

    Google Scholar 

  • Butcher SH, Butcher LL, Cho AK (1976) Modulation of neostriatal acetylcholine in the rat by dopamine and 5-hydroxytryptamine afferents. Life Sci 18:733–744

    Google Scholar 

  • Candura SM, Coccini T, Manzo L, Costa LG (1990) Interaction of σ-compounds with receptor-stimulated phosphoinositide metabolism in the rat brain. J Neurochem 55:1741–1748

    Google Scholar 

  • Ceci A, Smith M, French ED (1988) Activation of the A10 mesolimbic system by the σ-receptor agonist (+)SKF 10,047 can be blocked by rimcazole, a novel putative antipsychotic. Eur J Pharmacol 154:53–57

    Google Scholar 

  • Damsma G, Westerink BHC, De Vries JB, Van den Berg CJ, Horn AS (1987) Measurement of acetylcholine release in freely moving rats by means of automated intracerebral dialysis. J Neurochem 48:1523–1528

    Google Scholar 

  • Essman WB (1973) Age dependent effects of 5-hydroxytryptamine upon memory consolidation and cerebral protein synthesis. Pharmacol Biochem Behav 1:7–14

    Google Scholar 

  • Flood JF, Cherkin A (1986) Scopolamine effects on memory retention in mice: a model of dementia? Behav Neural Biol 45:169–184

    Google Scholar 

  • Freeman AS, Bunney BS (1984) The effects of phencyclidine and N-allylnormetazocine on midbrain dopamine neuronal activity. Eur J Pharmacol 104:287–293

    Google Scholar 

  • French ED, Ceci A (1990) Non-competitiveN-methyl-d-aspartate antagonists are potent activators of ventral tegmental A10 dopamine neurons. Neurosci Lett 119:159–162

    Google Scholar 

  • Garzón J, Rubio J, Del Río J (1981) Naloxone blocks the effect of 5-hydroxy-tryptophan on passive avoidance learning in rats: implication of endogenous opioid peptides. Life Sci 29:17–25

    Google Scholar 

  • Gillet G, Ammor S, Fillion G (1985) Serotonin inhibits acetylcholine release from rat striatum slices: evidence for a presynaptic receptor-mediated effect. J Neurochem 45:1687–1691

    Google Scholar 

  • Glick SD, Zimmerberg B (1972) Amnesic effects of scopolamine. Behav Biol 7:245–254

    Google Scholar 

  • Iyengar S, Dilworth VM, Mick SJ, Contreras PC, Monahan JB, Rao TS, Wood PL (1990) Sigma receptors modulate both A9 and A10 dopaminergic neurons in the rat brain: functional interaction with NMDA receptors. Brain Res 524:322–326

    Google Scholar 

  • Izquierdo I (1979) Effect of naloxone and morphine on various forms of memory in the rat: possible role of endogenous opiate mechanisms in memory consolidation. Psychopharmacology 66:199–203

    Google Scholar 

  • Izquierdo I (1989) Mechanism of action of scopolamine as an amnestic. TIPS 10:175–177

    Google Scholar 

  • Izquierdo JA, Baratti CM, Torrelio M, Arevalo L, McGaugh JL (1973) Effects of food deprivation, discrimination experience and physostigmine on choline acetylase and acetylcholine esterase in dorsal hippocampus and frontal cortex of rats. Psychopharmacologia 33:103–110

    Google Scholar 

  • Jackson D, Stachowiak MK, Bruno JP, Zigmond MJ (1988) Inhibition of striatal acetylcholine release by endogenous serotonin. Brain Res 457:259–266

    Google Scholar 

  • Johnson KM, Hillman GR (1982) Comparisons between phencyclidine, its monohydroxylated metabolites, and the stereoisomers ofN-allyl-N-normetazocine (SKF 10047) as inhibitors of the muscarinic receptor and acetylcholinesterase. J Pharm Pharmacol 34:462–464

    Google Scholar 

  • Jones KW, Bauerle LM, DeNoble VJ (1990) Differential effects of σ and phencyclidine receptor ligands on learning. Eur J Pharmacol 179:97–102

    Google Scholar 

  • Joyce D, Hurwitz HMB (1964) Avoidance behaviour in the rat after 5-hydroxytryptophan (5-HTP) administration. Psychopharmacologia 5:424–430

    Google Scholar 

  • Kameyama T, Nabeshima T, Kozawa T (1986) The antagonistic effects of naloxone on cycloheximide and anisomicin-induced amnesia. Pharmacol Biochem Behav 25:567–572

    Google Scholar 

  • Lalonde R, Vikis-Freibergs V (1985) Manipulations of 5-HT activity and memory in the rat. Pharmacol Biochem Behav 22:377–382

    Google Scholar 

  • Largent BL, Gundlach AL, Snyder SH (1984) Psychotomimetic opiate receptors labeled and visualized with (+)-[3H]3-(3-hydroxyphenyl)-N-(1-propyl)piperidine. Proc Natl Acad Sci USA 81:4983–4987

    Google Scholar 

  • Largent BL, Gundlach AL, Snyder SH (1986) Pharmacological and autoradiographic discrimination ofsigma and phencyclidine receptor binding sites in brain with (+)-[3H]SKF 10,047, (+)-[3H]-3-[3-hydroxyphenyl]-N-(1-propyl)piperidine and [3H]-1-[1-(2-thienyl)cyclohexyl]piperidine. J Pharmacol Exp Ther 238:739–748

    Google Scholar 

  • Matsuno K, Matsunaga K, Mita S (1992) Increase of extracellular acetylcholine level in rat frontal cortex induced by (+)N-allylnormetazocine as measured by brain microdialysis. Brain Res 575:315–319

    Google Scholar 

  • Maura G, Raiteri M (1986) Cholinergic terminals in rat hippocampus possess 5-HT1B receptors mediating inhibition of acetylcholine release. Eur J Pharmacol 129:333–337

    Google Scholar 

  • Maura G, Fedele E, Raiteri M (1989) Acetylcholine release from rat hippocampal slices is modulated by 5-hydroxytryptamine. Eur J Pharmacol 165:173–179

    Google Scholar 

  • McGaugh JL (1973) Drug facilitation of learning and memory. Annu Rev Pharmacol 13:229–241

    Google Scholar 

  • Messing RB, Jensen RA, Martinez JL Jr, Spiehler VR, Vasquiz BJ, Soumireu-Mourat B, Liang KC, McGaugh JL (1979) Naloxone enhancement of memory. Behav Neural Biol 27:266–275

    Google Scholar 

  • Muramatsu M, Tamaki-Ohashi J, Usuki C, Araki H, Aihara H (1988) Serotonin-2 receptor-mediated regulation of release of acetylcholine by minaprine in cholinergic nerve terminal of hippocampus of rat. Neuropharmacology 27:603–609

    Google Scholar 

  • Nabeshima T, Kamei H, Matsuno K, Kameyama T (1986) Conditioned suppression and opioid kappa receptor in mice. J Pharmacobiodyn 9:74–80

    Google Scholar 

  • Nabeshima T, Itoh K, Kawashima K, Kameyama T (1989) Effects of 5-HT2 receptor antagonist on cycloheximide-induced amnesia in mice. Pharmacol Biochem Behav 32:787–790

    Google Scholar 

  • Nabeshima T, Ichihara K, Tohyama K, Murase K, Suzuki T, Kameyama T (1991) Involvement of serotonergic neuronal systems in the anti-amnesic action of naftidrofuryl oxalate. Eur J Pharmacol 205:55–61

    Google Scholar 

  • Nishimura M, Shiigi Y, Kaneto H (1990) State dependent and/or direct memory retrieval by morphine in mice. Psychopharmacology 100:27–30

    Google Scholar 

  • Normile HJ, Altman HJ (1987) Evidence for a possible interaction between noradrenergic and serotonergic neurotransmission in the retrieval of a previously learned aversive habit in mice. Psychopharmacology 92:388–392

    Google Scholar 

  • Normile HJ, Altman HJ (1988) Enhanced passive avoidance retention following posttrain serotonergic receptor antagonist administration in middle-aged and aged rats. Neurobiol Aging 9:377–382

    Google Scholar 

  • Ögren SO (1982) Forebrain serotonin and avoidance learning: behavioral and biochemical studies on the acute effect of p-chloroamphetamine on one-way active avoidance learning in the male rat. Pharmacol Biochem Behav 16:881–895

    Google Scholar 

  • Ögren SO, Johansson C (1985) Separation of the associative and non-associative effects of brain serotonin released byp-chloroamphetamine: dissociable serotoninergic involvement in avoidance learning, pain and motor function. Psychopharmacology 86:12–26

    Google Scholar 

  • Parada-Turska J, Turski WA (1990) Excitatory amino acid antagonists and memory: effect of drugs acting atN-methyl-d-aspartate receptors in learning and memory tasks. Neuropharmacology 29:1111–1116

    Google Scholar 

  • Quirion R, Richard J, Dam TV (1985) Evidence for the existence of serotonin type-2 receptors on cholinergic terminals in rat cortex. Brain Res 333:345–349

    Google Scholar 

  • Quirion R, Chicheportiche R, Contreras PC, Johnson KM, Lodge D, Tam SW, Woods JH, Zukin SR (1987) Classification and nomenclature of phencyclidine and sigma receptor sites. TINS 10:444–446

    Google Scholar 

  • Robinson SE (1983) Effect of specific serotonergic lesions on cholinergic neurons in the hippocampus, cortex and striatum. Life Sci 32:345–353

    Google Scholar 

  • Rush DK (1986) Reversal of scopolamine-induced amnesia of passive avoidance by pre- and post-training naloxone. Psychopharmacology 89:296–300

    Google Scholar 

  • Samanin R, Quattrone A, Peri G, Ladinsky H, Consolo S (1978) Evidence of an interaction between serotoninergic and cholinergic neurons in the corpus striatum and hippocampus of the rat brain. Brain Res 151:73–82

    Google Scholar 

  • Siniscalchi A, Cristofori P, Veratti E (1987) Influence of N-allylnormetazocine on acetylcholine release from brain slices: involvement of muscarinic receptors. Naunyn-Schmiedeberg's Arch Pharmacol 336:425–429

    Google Scholar 

  • Sircar R, Nichtenhauser R, Ieni JR, Zukin SR (1986) Characterization and autoradiographic visualization of (+)-[3H]SKF10,047 binding in rat and mouse brain: further evidence for phencyclidine/“sigma opiate” receptor commonality. J Pharmacol Exp Ther 237:681–688

    Google Scholar 

  • Smith G (1988) Animal models of Alzheimer's disease: experimental cholinergic denervation. Brain Res Rev 13:103–118

    Google Scholar 

  • Su TP (1982) Evidence forsigma opioid receptor: binding of [3H]SKF-10047 to etorphine-inaccessible sites in guinea-pig brain. J Pharmacol Exp Ther 223:284–290

    Google Scholar 

  • Tam SW (1983) Naloxone-inaccessible σ receptor in rat central nervous system. Proc Natl Acad Sci USA 80:6703–6707

    Google Scholar 

  • Venable N, Kelly PH (1990) Effects of NMDA receptor antagonists on passive avoidance learning and retrieval in rats and mice. Psychopharmacology 100:215–221

    Google Scholar 

  • Vizi ES, Hársing LG, Zsilla G (1981) Evidence of the modulatory role of serotonin in acetylcholine release from striatal interneurons. Brain Res 212:89–99

    Google Scholar 

  • Warburton DM, Brown K (1972) The facilitation of discrimination performance by physostigmine sulphate. Psychopharmacologia 27:275–284

    Google Scholar 

  • Wenk GL, Engisch KL (1986) [3H] Ketanserin (serotonin type-2) binding increases in rat cortex following basal forebrain lesions with ibotenic acid. J Neurochem 47:845–850

    Google Scholar 

  • Wetzel W, Getsova VM, Jork R, Matthies H (1980) Effect of serotonin on Y-maze retention and hippocampal protein synthesis in rats. Pharmacol Biochem Behav 12:319–322

    Google Scholar 

  • Whitehouse L (1965) The effects of physostigmine on discrimination learning. Psychopharmacologia 9:183–188

    Google Scholar 

  • Wood PL, Sanschagrin D, Richard JW, Thakur M (1983) Multiple opiate receptor affinities of kappa and agonist/antagonist analgesics: in vivo assessment. J Pharmacol Exp Ther 226:545–550

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. New Drug Research, Central Research Laboratories, Santen Pharmaceutical Co., Higashiyodogawa, 533, Osaka, Japan

    Kiyoshi Matsuno, Toshihiko Senda, Keiko Matsunaga & Shiro Mita

  2. Department of Pharmacology, Faculty of Pharmaceutical Sciences, Nagasaki University, 852, Nagasaki, Japan

    Hiroshi Kaneto

Authors
  1. Kiyoshi Matsuno
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Toshihiko Senda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Keiko Matsunaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shiro Mita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hiroshi Kaneto
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matsuno, K., Senda, T., Matsunaga, K. et al. Similar ameliorating effects of benzomorphans and 5-HT2 antagonists on drug-induced impairment of passive avoidance response in mice: comparison with acetylcholinesterase inhibitors. Psychopharmacology 112, 134–141 (1993). https://doi.org/10.1007/BF02247374

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02247374

Key words

Search

Navigation