Limbic forebrain structures in emotional memory
Neuromodulatory systems and memory storage: Role of the amygdala

https://doi.org/10.1016/0166-4328(93)90092-5Get rights and content

Abstract

This article reviews findings of research examining the interaction of peripheral adrenergic systems with cholinergic, opioid peptidergic and GABAergic systems in modulating memory storage. It is well established that retention is enhanced by posttraining systemic or intra-amygdala injections of adrenergic agonists, opiate antagonists and GABAergic antagonists. These influences appear to be mediated by activation of NE receptors within the amygdala, as intra-amygdala injections of β-adrenergic antagonists block the memory-modulating effects of hormones and drugs affecting these systems. Furthermore, these influences also appear to involve, at a subsequent step, activation of a cholinergic system: atropine blocks the memory-enhancing effects of adrenergic agonists and opiate and GABAergic antagonists and oxotremorine attenuate the memory-impairing effects of opiate agonists and GABAergic agonists. These findings suggest that the amygdala integrates the memory-modulating effects of neuromodulatory systems activated by learning experiences.

References (92)

  • C. Castellano et al.

    Retention enhancement with posttraining picrotoxin: lack of state dependency

    Behav. Neural Biol.

    (1989)
  • C. Castellano et al.

    Oxotremorine attenuates retrograde amnesia induced by posttraining administration of the GABAergic agonists muscimol and baclofen

    Behav. Neural Biol.

    (1991)
  • R. Dingledine et al.

    Naloxone as a GABA agonist: evidence from iontophoretion receptor binding and convulsant studies

    Eur. J. Pharmacol.

    (1978)
  • M. Gallagher

    Naloxone enhancement of memory processes: effects of other opiate antagonists

    Behav. Neural Biol.

    (1982)
  • M. Gallagher et al.

    Opiate antagonist facilitation of time-dependent memory processes: dependence upon intact norepinephrine function

    Brain Res.

    (1985)
  • P.E. Gold

    Glucose modulation of memory storage processing

    Behav. Neural Biol.

    (1986)
  • P.E. Gold et al.

    Plasma catecholamines: changes after footshock and seizure-producing frontal cortex stimulation

    Behav. Neural Biol.

    (1981)
  • P.E. Gold et al.

    Facilitation of time-dependent memory processes with posttrial epinephrine injections

    Behav. Biol.

    (1975)
  • P.E. Gold et al.

    Posttraining brain norepinephrine concentrations: correlation with retention performance of avoidance training with peripheral epinephrine modulation of memory processing

    Behav. Biol.

    (1978)
  • P.E. Gold et al.

    Effects of alpha and beta adrenergic receptor antagonists on post-trial epinephrine modulation of memory: relationship to posttraining brain norepinephrine concentrations

    Behav. Biol.

    (1978)
  • J.M. Hitchcock et al.

    Fear-potentiated startle using an auditory conditioned stimulus: effect of lesions of the amygdala

    Physiol. Behav.

    (1987)
  • I.B. Introini-Collison et al.

    Opioid peptidergic systems modulate the activity of beta-adrenergic mechanisms during memory consolidation processes

    Behav. Neural Biol.

    (1986)
  • I.B. Introini-Collison et al.

    Epinephrine modulates long-term retention of an aversively motivated discrimination task

    Behav. Neural Biol.

    (1986)
  • I.B. Introini-Collison et al.

    Memory enhancement with intra-amygdala posttraining naloxone is blocked by concurrent administration of propranolol

    Brain Res.

    (1989)
  • I.B. Introini-Collison et al.

    Memory enhancing effects of posttraining dipivefrin and epinephrine: involvement of peripheral and central adrenergic receptors

    Brain Res.

    (1992)
  • I. Izquierdo et al.

    Effect of ACTH, epinephrine, β-endorphin, naloxone and of the combination of naloxone or β-endorphin with ACTH or epinephrine on memory consolidation

    Psychoneuroendocrinology

    (1983)
  • B.L. Jacobs

    Single unit activity of locus coeruleus neurons in behaving animals

    Prog. Neurobiol.

    (1986)
  • B. Jones et al.

    Limbic lesions and the problem of stimulus-reinforcement association

    Exp. Neurol.

    (1972)
  • R.P. Kesner et al.

    Central but not basolateral amygdala mediates memory for positive affective experiences

    Behav. Brain Res.

    (1989)
  • R.P. Kesner et al.

    A review of electrical stimulation of the brain in context of learning and retention

    Behav. Biol.

    (1974)
  • R.A. Leslie et al.

    The central distribution of the cervical vagus nerve and gastric afferents and efferent projections in the rat

    Brain Res. Bull.

    (1982)
  • K.C. Liang et al.

    Peripheral epinephrine modulates the effects of posttraining amygdala stimulation on memory

    Behav. Brain Res.

    (1985)
  • K.C. Liang et al.

    Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system

    Brain Res.

    (1986)
  • K.C. Liang et al.

    Lesions of the stria terminalis attenuate the enhancing effect of posttraining epinephrine on retention of an inhibitory avoidance response

    Behav. Brain Res.

    (1983)
  • K.C. Liang et al.

    Involvement of amygdala pathways in the influence of posttraining amygdala norepinephrine and peripheral epinephrine on memory storage

    Brain Res.

    (1990)
  • K.C. Liang et al.

    Posttraining amygdaloid lesions impair retention of an inhibitory avoidance response

    Behav. Brain Res.

    (1982)
  • J.L. McGaugh

    Dissociating learning and performance: drug and hormone enhancement of memory storage

    Brain Res. Bull.

    (1989)
  • J.L. McGaugh et al.

    Memory enhancing effects of posttraining naloxone: involvement of β-noradrenergic influences in the amygdaloid complex

    Brain Res.

    (1988)
  • R.B. Messing et al.

    Naloxone enhancement of memory

    Behav. Neural Biol.

    (1979)
  • S. Nakamura et al.

    Noradrenergic terminal excitability: effects of opioids

    Neurosci. Letters

    (1982)
  • J.D. Oh et al.

    Cholinergic neurons in the rat central nervous system demonstrated by in situ hybridization of choline acetyltranferase mRNA

    Neurosci.

    (1992)
  • R. Peoples et al.

    γ-Aminobuteric acid enhancement of potassium-stimulated release of [3H]norepinephrine by multiple mechanisms in rat cortical slices

    Biochem. Pharmacol.

    (1991)
  • J.A. Ricardo et al.

    Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures of the rat

    Brain Res.

    (1978)
  • S. Sagratella et al.

    Convulsant and anticonvulsant effects of opioids: relationships to GABA-mediated transmission

    Neuropharmacology

    (1982)
  • B.J. Spiegler et al.

    Evidence for sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations

    Behav. Brain Res.

    (1981)
  • D.B. Sternberg et al.

    Epinephrine facilitation of appetitive learning: attenuation with adrenergic receptor antagonists

    Behav. Neural Biol.

    (1985)
  • Cited by (161)

    View all citing articles on Scopus
    View full text