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Modulation of memory by post-training epinephrine: involvement of cholinergic mechanisms

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Abstract

Extensive evidence indicates that memory storage can be modulated by peripheral epinephrine as well as by drugs affecting the muscarinic cholinergic system. Low doses of epinephrine (Epi) facilitate memory while high doses induce amnesia. Retention is enhanced by post-training administration of cholinergic muscarinic agonists and impaired by antagonists. The present experiments examined the interaction of peripheral Epi and cholinergic drugs in memory modulation. Male CFW mice (60 days old) were trained on an inhibitory avoidance response (IA) or a Y-maze discrimination response (YMD), injected (IP) immediately post-training and tested 24 h later. In the Y-maze task, retention was assessed by discrimination reversal training. Findings obtained in the two tasks were comparable. Epi (IA: 3.0 μg/kg; YMD: 30.0 μg/kg) potentiated the memory-enhancing effect of low doses of oxotremorine (Otm) (IA: 16; YMD: 5.0 μg/kg) and physostigmine (Phy) (6.8 and 22.0 μg/kg for both IA and YMD). The memory-facilitating effect of Otm (50.0 μg/kg) was not blocked by an amnestic dose of Epi (IAT: 0.3 mg/kg; YMD: 1.0 mg/kg). Retention was not affected when these amnestic doses of Epi were administered together with a memory-facilitating dose of Phy (68.0 μg/kg). In contrast, atropine (IA: 10.0 mg/kg; YMD: 3.0 mg/kg) completely blocked the facilitatory effect of Epi (IA: 10.0 μg/kg; YMD: 300 μg/kg). These findings indicate that, when administered in low doses, Epi interacts with Otm and Phy. However, cholinergic drugs can block both the memory-enhancing and the memory-impairing effects of Epi. The findings suggest that Epi may modulate memory through cholinergic systems.

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References

  • Axelrod J, Weil-Malherbe H, Tomchick R (1959) The physiological disposition of 3H-epinephrine and its metabolite metanephrine. J Pharmacol Exp Ther 127:251–256

    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 

  • Bartus RT, Dean RL, Goss JA, Lippa AS (1980) Age-related changes in passive avoidance retention: Modulation with dietary choline. Science 209:301–313

    Google Scholar 

  • Bennett C, Liang KC, McGaugh JL (1985) Depletion of adrenal catecholamines alters the amnestic effect of amygdala stimulation. Behav Brain Res 15:83–91

    Google Scholar 

  • Blackwood DH, Christie JE (1986) The effects of physostigmine on memory and auditory P300 in Alzheimer-type dementia. Biol Psychiatry 21:557–560

    Google Scholar 

  • Bowman WC, Bowman A, Bowman A (1986) Dictionary of pharmacology. Blackwell, Oxford

    Google Scholar 

  • Carrasco MA, Dias RD, Perry MLS, Wofchuk ST, Souza DO, Izquierdo I (1982) Effect of morphine, ACTH, epinephrine, Met-, Leu- and des-Tyr-Met- enkephalin on β-endorphin-like immunoreactivity of rat brain. Psychoneuroendocrinology 7:229–234

    Google Scholar 

  • Castellano C (1981) Strain-dependent effects of naloxone on discrimination learning in mice. Psychopharmacology 73:152–156

    Google Scholar 

  • Croul C, Stone WS, Gold PE (1986) Epinephrine and glucose attenuation of scopolamine-induced amnesia in mice. Soc Neurosci Abstr 12:709

    Google Scholar 

  • Drachman DA (1977) Memory and cognitive function in man: Does the cholinergic system have a specific role? Neurology 27:783–790

    CAS  PubMed  Google Scholar 

  • Drachman DA, Leavitt J (1974) Human memory and the cholinergic system. Arch Neurol 30:113–121

    Google Scholar 

  • Dunnett SB (1985) Comparative effects of cholinergic drugs and lesions of nucleus basalis or fimbria-fornix on delayed matching in rats. Psychopharmacology 87:357–363

    Google Scholar 

  • Flood JF, Landry DW, Jarvik ME (1981) Cholinergic receptor interactions and their effects on long-term memory processing. Brain Res 215:177–185

    Google Scholar 

  • Flood JF, Smith GE, Cherkin A (1983) Memory retention: Potentiation of cholinergic drug combinations in mice. Neurobiol Aging 4:37–43

    Google Scholar 

  • Flood JF, Smith GE, Cherkin A (1984a) Memory retention: Effect of prolonged cholinergic stimulation in mice. Pharmacol Biochem Behav 20:161–163

    Google Scholar 

  • Flood JF, Smith GE, Cherkin A (1984b) Memory retention test performance in mice: Improvement by chronic oral cholinergic drug treatment. Pharmacol Biochem Behav 21:169–173

    Google Scholar 

  • Flood JF, Smith GE, Cherkin A (1985) Memory enhancement: supra-additive effect of subcutaneous cholinergic drug combinations in mice. Psychopharmacology 86:61–67

    Google Scholar 

  • Gallagher M (1982) Naloxone enhancement of memory processes: Effects of other opiate antagonists. Behav Neural Biol 35:375–382

    Google Scholar 

  • Gallagher M (1985) Re-viewing modulation of learning and memory. In: Weinberger NM, McGaugh JL, Lynch G (eds) Memory systems of the brain: animal and human cognitive processes. Guilford Press, New York, pp 311–334

    Google Scholar 

  • Gallagher M, Kapp BS (1978) Manipulation of opiate activity in the amygdala alters memory processes. Life Sci 23:1973–1978

    Google Scholar 

  • Gallagher M, Kapp BS (1981) Effect of phentolamine administration into the amygdala complex of rats on time-dependent memory processes. Behav Neurol Biol 31:90–95

    Google Scholar 

  • Gold PE, McGaugh JL (1977) Hormones and memory. In: Miller LH, Sandman CA, Kastin AJ (eds) Neuropeptide influences on the brain and behavior. Raven Press, New York, pp 127–143

    Google Scholar 

  • Gold PE, van Buskirk R (1975) Facilitation of time-dependent memory processes with posttrial epinephrine injections. Behav Biol 13:145–153

    Google Scholar 

  • Gold PE, van Buskirk R (1978a) Posttraining brain norepinephrine concentrations: Correlation with retention performance of avoidance training with peripheral epinephrine modulation of memory processing. Behav Biol 23:509–520

    Google Scholar 

  • Gold PE, van Buskirk R (1978b) Effects of α- and β-adrenergic receptor antagonists on post-trial epinephrine modulation of memory: Relationship to posttraining brain norepinephrine concentrations. Behav Biol 24:168–184

    Google Scholar 

  • Gold PE, McCarty R, Sternberg DB (1982) Peripheral catecholamines and memory modulation. In: Marsan CA, Matthies H (eds) Neuronal plasticity and memory formation. Raven Press, New York, pp 327–338

    Google Scholar 

  • Gower AJ (1986) Lesioning of the nucleus basalis in the rat as a model of Alzheimer disease. TIPS 7:432–434

    Google Scholar 

  • Haroutanian V, Barnes E, Davis KL (1985) Cholinergic modulation of memory in rats. Psychopharmacology 87:266–271

    Google Scholar 

  • Introini I, Baratti CM (1984) The impairment of retention induced by β-endorphin in mice may be mediated by reduction of central cholinergic activity. Behav Neural Biol 41:152–163

    Google Scholar 

  • Introini-Collison IB, Baratti CM (1986) Opioid peptidergic systems may modulate the activity of β-adrenergic mechanism during memory consolidation processes. Behav Neural Biol 46:227–241

    Google Scholar 

  • Introini-Collison I, McGaugh JL (1986a) Epinephrine modulates long-term retention of an aversively-motivated discrimination task. Behav Neural Biol 45:358–365

    Google Scholar 

  • Introini-Collison I, McGaugh JL (1986b) Interaction of adrenergic, cholinergic and opioid systems in modulation of memory storage. Soc Neurosci Abstr 12:710

    Google Scholar 

  • Introini-Collison I, McGaugh JL (1987) Naloxone and β-endorphin alter the effects of post-training epinephrine on retention of an inhibitory avoidance response. Psychopharmacology 92:229–235

    Google Scholar 

  • Introini IB, McGaugh JL, Baratti CM (1985) Pharmacological evidence of a central effect of naltrexone, morphine and β-endorphin and a peripheral effect of Met- and Leu-enkephalin on retention of an inhibitory response in mice. Behav Neural Biol 44:434–446

    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, Dias RD (1983a) Memory as a state dependent phenomenon: Role of ACTH and epinephrine. Behav Neural Biol 38:144–149

    Google Scholar 

  • Izquierdo I, Dias RD (1983b) The influence of adrenergic receptor antagonists on the amnestic and antiamnestic actions of adrenaline and tyramine. Psychopharmacology 80:181–183

    Google Scholar 

  • Izquierdo I, Dias RD (1985) Influence on memory of posttraining and pre-test injections of ACTH, vasopressin, epinephrine, or β-endorphin, and their interaction with naloxone. Psychoneuroendocrinology 10:165–172

    Google Scholar 

  • Izquierdo I, Graudenz M (1980) Memory facilitation by naloxone is due to release of dopaminergic and β-adrenergic systems from tonic inhibition. Psychopharmacology 67:165–222

    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 acetylcholinesterase in the dorsal hippocampus and frontal cortex of rats. Psychopharmacologia 33:103–110

    Google Scholar 

  • Jhamandas K, Sutak M (1974) Modifications of brain acetylcholine release by morphine and its antagonists in normal and morphine-dependent rats. Br J Pharmacol 50:57–62

    Google Scholar 

  • Jhamandas K, Sutak M (1983) Stereospecific enhancement of evoked release of brain acetylcholine by narcotic antagonists. Br J Pharmacol 78:433–440

    Google Scholar 

  • Karczmar AG, Dun NJ (1978) Cholinergic synapses: physiological, pharmacological and behavior considerations. In: Lipton MA, DiMascio A, Killam KF (eds) Psychopharmacology: a generation of progress. Raven Press, New York, pp 293–305

    Google Scholar 

  • Liang KC, Chang L (1986) Intra-amygdala injections of DSP-4 attenuate the memory enhancing effect of peripheral epinephrine. Soc Neurosci Abstr 12:702

    Google Scholar 

  • Liang KC, McGaugh JL (1983) Lesions of the stria terminalis attenuate the enhancing effect of posttraining epinephrine on retention of an inhibitory avoidance response. Behav Brain Res 9:49–58

    Google Scholar 

  • Liang KC, Bennett C, McGaugh JL (1985) Peripheral epinephrine modulates the effects of posttraining amygdala stimulation on memory. Behav Brain Res 15:93–100

    Google Scholar 

  • Mantione CR, Fisher A, Hanin I (1981) The AF64A-treated mouse: Possible model for central cholinergic hypofunction. Science 213:579–580

    Google Scholar 

  • McCarty R, Gold PE (1981) Plasma catecholamines: Effects of footshock level and hormonal modulators of memory storage. Horm Behav 15:168–182

    Google Scholar 

  • McGaugh JL (1983) Hormonal influences on memory. Annu Rev Psychol 34:297–323

    Google Scholar 

  • McGaugh JL (1985) Peripheral and central adrenergic influences on brain systems involved in the modulation of memory storage. In: Olton DS, Gamzu E, Corkin S (eds) Memory dysfunctions: an integration of animal and human research from preclinical and clinical perspectives. New York Academy of Sciences, New York, pp 150–162

    Google Scholar 

  • McGaugh J, Introini-Collison I (1986) Memory: peptide neurotransmitters and drug influences. Clin Neuropharmacol 9:289–291

    Google Scholar 

  • McGaugh JL, Introini-Collison IB, Nagahara A (1988) Memory-enhancing effects of posttraining naloxone: Involvement of B-noradrenergic influences in the amygdaloid complex. Brain Research (in press)

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

    Google Scholar 

  • Murray CL, Fibiger HC (1985) Learning and memory deficits after lesions of the nucleus basalis magnocellularis: Reversal by physostigmine. Neuroscience 14:1025–1032

    Google Scholar 

  • Powell DA, Buchanan S, Hernandez L (1985) Intracerebral scopolamine administration attenuates Pavlovian heart rate conditioning in the rabbit. Pavlov J Biol Sci 20:116–123

    Google Scholar 

  • Russell RW (1982) Cholinergic systems in behavior: The search for the mechanisms of action. Annu Rev Pharmacol Toxicol 22:435–463

    Google Scholar 

  • Sternberg DB, Korol D, Novack G, McGaugh JL (1986) Epinephrine-induced memory facilitation: Attenuation by adrenergic receptor antagonists. Eur J Pharmacol 129:189–193

    Google Scholar 

  • Stratton LO, Petrinovich LF (1963) Post-trial injections of an anticholinesterase drug and maze learning in two strains of rats. Psychopharmacologia 5:47–54

    Google Scholar 

  • Taylor P (1985a) Cholinergic agonists. In: Goodman AG, Goodman LS, Rall TW, Murad F (eds) The pharmacological basis of therapeutics. MacMillan New York, pp 100–109

    Google Scholar 

  • Taylor P (1985b) Anticholinesterase agents. In: Goodman AG, Goodman LS, Rall TW, Murad F (eds) The pharmacological basis of therapeutics. MacMillan, New York, pp 110–129

    Google Scholar 

  • Weinberger NM, Gold PE, Sternberg DB (1984) Epinephrine enables Pavlovian fear conditioning under anesthesia. Science 223:605–607

    Google Scholar 

  • Weiner N (1985) Atropine, scopolamine and related antimuscarinic drugs. In: Goodman AG, Goodman LS, Rall TW, Murad F (eds) The pharmacological basis of therapeutics. MacMillan, New York, pp 120–144

    Google Scholar 

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  1. Center for the Neurobiology of Learning and Memory, University of California, 92717, Irvine, CA, USA

    Ines B. Introini-Collison & James L. McGaugh

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  1. Ines B. Introini-Collison
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  2. James L. McGaugh
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Introini-Collison, I.B., McGaugh, J.L. Modulation of memory by post-training epinephrine: involvement of cholinergic mechanisms. Psychopharmacology 94, 379–385 (1988). https://doi.org/10.1007/BF00174693

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