Trends in Neurosciences
Volume 21, Issue 7, 1 July 1998, Pages 294-299
Journal home page for Trends in Neurosciences

Mechanisms of emotional arousal and lasting declarative memory

https://doi.org/10.1016/S0166-2236(97)01214-9Get rights and content

Abstract

Neuroscience is witnessing growing interest in understanding brain mechanisms of memory formation for emotionally arousing events, a development closely related to renewed interest in the concept of memory consolidation. Extensive research in animals implicates stress hormones and the amygdaloid complex as key, interacting modulators of memory consolidation for emotional events. Considerable evidence suggests that the amygdala is not a site of long-term explicit or declarative memory storage, but serves to influence memory-storage processes in other brain regions, such as the hippocampus, striatum and neocortex. Human-subject studies confirm the prediction of animal work that the amygdala is involved with the formation of enhanced declarative memory for emotionally arousing events.

Section snippets

Modulation of memory storage

Most studies of brain mechanisms of memory focus on the neural events mediating memory and the anatomical locus of the `memory trace'. Equally important, however, are neurobiological systems that regulate, or modulate, long-term memory storage. Long-term memories are not made instantaneously: they consolidate over time after learning10, 11, 12. Recent evidence concerning memory consolidation comes from many domains of investigation, including studies of synaptic plasticity13, 14, 15 and behavior

Role of stress-released hormones in memory consolidation

The fact that recently formed memories are susceptible to exogenous modulatory treatments provides the opportunity for endogenous modulation of memory storage for emotional events. Stress hormones are a priori candidate endogenous modulators (Fig. 1). Stress-hormone systems activated by emotional situations serve the immediate adaptive needs of an organism[22]. Additionally, extensive evidence suggests they influence memory storage8, 9, 23, 24. Initial studies examined the effects of

Role of the amygdaloid complex in memory modulatory mechanisms

The hypothesis that the amygdala modulates declarative-memory storage is rooted in several lines of research. Early studies demonstrated that electrical stimulation of the amygdaloid complex (AC) elicits behavioral arousal (the `orienting reflex') and activates cortical EEG ([38]). It is of interest for reasons discussed below that the cortical arousal response elicited by AC stimulation is mediated by the stria terminalis (ST), a major AC pathway[38]. Goddard's research[39] was the first to

Fractionation of amygdala nuclei function in memory

The `amygdala' is a heterogeneous collection of distinct nuclei. As long ago as 1915, Johnston noted that the AC `is a complex of many diverse elements which have been brought together by mechanical forces and have no primary functional unity' (quoted by Goddard[51]). Although Johnston might have overstated the case, the evidence indicates that nuclei of the AC have different functions in learning33, 35, 52.

The basolateral AC (BL) appears to be the nucleus most crucially involved in the

AC modulation of memory storage in other brain regions

The evidence briefly summarized above strongly suggests that the amygdala is not the neural site of long-term memory for declarative information. It is equally evident that the amygdala, particularly the BL nucleus, is involved in modulating memory storage processes in other brain regions. Other recent findings strongly support these implications. Packard et al.[60] reasoned that if the AC modulates memory in a particular brain structure, stimulation of the AC should influence formation of the

The AC and emotionally influenced, long-term declarative memory in humans

There has been controversy concerning the role of the AC in declarative memory73, 74. Scoville and Milner[73] examined memory in ten patients (including H.M.) who had received medial temporal-lobe surgery, often including removal of the AC, and concluded that `Removal of the amygdala bilaterally does not appear to cause memory impairment'. A recent study investigating a rare patient with AC damage concluded that, although the AC is important for classical conditioning of autonomic responses, it

Concluding remarks

An impressively broad array of experimental evidence either directly supports, or is consistent with the hypothesis that stress-hormone systems and the AC are key components of an endogenous memory modulating system. Generally inactive in unemotional learning situations, this system is activated during and after an emotionally arousing event and appears to regulate declarative-memory storage processes in other brain regions (Fig. 5). This mechanism aids in the selection of long-term memories on

References (83)

  • L. Weiskrantz et al.

    Neuropsychologia

    (1979)
  • A. Arai et al.

    Brain Res.

    (1990)
  • S. Lupien et al.

    Brain Res. Rev.

    (1997)
  • P. Gold et al.

    Behav. Biol.

    (1975)
  • I. Introini-Collison

    Brain Res.

    (1992)
  • K.A. Nielson et al.

    Behav. Neural. Biol.

    (1994)
  • B. Roozendaal et al.

    Neurobiol. Learn. Mem.

    (1996)
  • B. Roozendaal et al.

    Brain Res.

    (1996)
  • B. Roozendaal et al.

    Neurobiol. Learn. Mem.

    (1997)
  • P.E. Gold

    Brain Res.

    (1975)
  • C. Bennett et al.

    Behav. Brain Res.

    (1985)
  • K.C. Liang et al.

    Behav. Brain Res.

    (1985)
  • K.C. Liang et al.

    Brain Res.

    (1990)
  • K.C. Liang

    Brain Res.

    (1986)
  • J.L. McGaugh

    Brain Res.

    (1988)
  • R. Galvez et al.

    Neurobiol. Learn. Mem.

    (1996)
  • M. Parent et al.

    Brain Res.

    (1994)
  • P. Gold

    Behav. Biol.

    (1975)
  • H.C. Breiter

    Neuron

    (1996)
  • W. James

    Principles of Psychology,

    (1890)
  • Christianson, S. (ed.) (1992) The Handbook of Emotion and Memory: Research and Theory...
  • M. Davis

    Annu. Rev. Neurosci.

    (1992)
  • J.E. LeDoux

    Annu. Rev. Psychol.

    (1995)
  • L.R. Squire et al.

    Annu. Rev. Psychol.

    (1993)
  • P.E. Gold et al.
  • J.L. McGaugh
  • J.L. McGaugh et al.

    Proc. Natl. Acad. Sci. U. S. A.

    (1996)
  • D.O. Hebb

    The Organization of Behavior

    (1949)
  • J.L. McGaugh

    Science

    (1966)
  • J.I. McGaugh et al.

    Memory Consolidation

    (1972)
  • U. Frey et al.

    Nature

    (1997)
  • T. Seidenbecher et al.

    Proc. Natl. Acad. Sci. U. S. A.

    (1997)
  • J. Guzowski et al.

    Proc. Natl. Acad. Sci. U. S. A.

    (1997)
  • I. Izquierdo

    Eur. J. Neurosci.

    (1997)
  • E. Doyle et al.

    Neurochem. Res.

    (1990)
  • T. Brashers-Krug et al.

    Nature

    (1996)
  • F.B. Krasne

    Brain Res.

    (1978)
  • C. Pelz et al.

    J. Exp. Biol.

    (1997)
  • Frankenheuser, M. (1975) Emotions – Their Parameters and Measurement (Levi, L., ed.), pp. 209–234, Raven...
  • B. Bohus
  • C.L. Williams et al.
  • Cited by (0)

    View full text