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The Effects of Stress and Trauma on Brain and Memory: a View from Developmental Cognitive Neuroscience

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The Effects of Stress and Trauma on Brain and Memory: a View from Developmental Cognitive Neuroscience The Effects of Stress and Trauma on Brain and Memory: A View from Developmental Cognitive Neuroscience The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Nelson, Charles A., and Leslie J. Carver. 1998. The Effects of Stress and Trauma on Brain and Memory: A View from Developmental Cognitive Neuroscience. Development and Psychopathology 10, no. 4: 793–809. Published Version doi:10.1017/S0954579498001874 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:12997517 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Development and Psychopathology, 10 (1998), 793±809 Copyright 1998 Cambridge University Press Printed in the United States of America The effects of stress and trauma on brain and memory: A view from developmental cognitive neuroscience CHARLES A. NELSON AND LESLIE J. CARVER University of Minnesota Abstract Many aspects of brain development depend on experience. Because the major macro-morphological events of brain development occur over the first 2±3 years of postnatal life, this time period can be considered both a period of opportunity as well as a period of vulnerability. In this paper we describe how experience with stress early in life can have a negative impact on certain aspects of brain development, and specifically, those neural circuits that underlie memory. We also describe the effects of traumatic events on the development of the neural basis of memory. In support of our argument, we review the literature on brain, stress, and memory in the context of development. Based on this review, we suggest that the developing brain is particularly vulnerable to the harmful physiological effects of stress, which in turn has the potential to lead to impairments in memory. Unfortunately, there are few empirical data that directly address this hypothesis. In this context we offer a number of suggestions for future research. In this paper we examine the possible delete- Here we intend to demonstrate that the neural rious effects of stress on the developing brain, mechanisms at the cellular level that underlie and at the behavioral level, on the develop- functional plasticity, including long-term po- ment and formation of memory. The thesis tentiation (LTP) and axonal regeneration, and that we will put forward is that stress acts on that are adaptive in the normally developing known neural circuits, a subset of which over- child, will prove maladaptive to the child ex- lap with those that subserve memory. As a posed to early, repetitive, and/or chronic result, we will establish a potential neurologi- stress. In other words, although plasticity in cal basis for stress-induced alterations in the developing brain represents a window of memory. In addition, because our research opportunity in normal circumstances, it also agenda is with the study of development we represents a period of vulnerability in adverse will cast this thesis in a developmental light. ones. To provide a compelling argument in sup- port of our thesis, we begin with a brief over- The writing of this paper was made possible by grants view of memory and the neural bases of mem- from the National Institutes of Health (NS23389) and the ory, and then proceed to discuss these topics John D. and Catherine T. MacArthur Foundation, to the first author, and from the National Institutes of Child in a developmental context. Here we conclude Health and Human Development Training Grant that the neural substrate required of explicit 5T32HD07151 Center for Research In Learning, Percep- or declarative memory emerges during the tion, and Cognition, and a University of Minnesota dis- first year of life, although much development sertation fellowship to the second author. awaits further elaboration of both limbic and Address correspondence and reprint requests to: Charles A. Nelson, Institute of Child Development, Uni- cortical structures. versity of Minnesota, 51 East River Road, Minneapolis, The next topic to which we turn is con- MN 55105; E-mail address: [email protected]. cerned with the effects of stress on the brain. 793 794 C. A. Nelson and L. J. Carver Here we focus on both moderate levels of cally include the ability to recall events, stress and acute and/or chronic levels, includ- objects, or places, or to recognize things asso- ing trauma. Again, we begin with a review of ciated with such events. Explicit memory can the adult findings, and then turn to the child occur on a rapid time frame, in as little as one literature. Here we will make clear several trial and under certain circumstances, may in- known effects of stress on the brain. For ex- volve some aspect of ªself.º For example, the ample, stress can alter glucocorticoid recep- subject may see him/herself in some scene, tors in regions of the hippocampus. In addi- such as what he/she was doing when John F. tion, some stressors can exert long-lasting, Kennedy was assassinated or when the space seemingly permanent effects on the brain. The shuttle Challenger exploded. dentate region of the hippocampal formation Implicit memory, on the other hand, is typ- can experience permanent cell loss as a result ically thought to reflect a cluster of different of prolonged stress. Finally, the developing subtypes of memory, although collectively, all brain may be particularly vulnerable to stress. are distinct from explicit memory. Indeed, Exposing fetal monkeys to unpredictable loud perhaps a better way to frame this is that im- sounds, for example, seemingly has perma- plicit memory as a whole represents a type nent effects on postnatal neurobehavioral de- of nondeclarative memory. Thus, all forms of velopment. implicit memory are assumed to be uncon- Having established the link between brain scious, to require multiple trials to acquire, and memory and between brain and stress, in and may not involve the self at all. One exam- the next section of our paper we attempt to ple of implicit memory is priming, which integrate across these domains. Here we ex- might involve presenting subjects with stimuli amine the neural bases of changes in memory in a study phase that reappear briefly or in that are stress-induced or perhaps more parsi- degraded form during a test phase. A subject's moniously, stress-related. Because this is not faster or more accurate identification of the the main area of activity of our laboratory, we test items relative to similar but unstudied will depend heavily on the work of other in- items is taken as evidence of priming. A sec- vestigators. The developmental literature on ond form of implicit memory might be proce- this topic is not extensive, and a portion of dural learning. An example of a procedural our time will be spent on describing fruitful learning task is the Serial Reaction Time areas of future research. It will be these rec- (SRT) task, in which subjects are required to ommendations that will conclude our paper. respond to a pattern of lights flashing across a screen. In such a case, the subject may show no overt, conscious awareness of learning the What Is Memory? pattern; for example, when asked, ªdid you Although the jury is still deliberating, most see a pattern,º the subject might respond cognitive psychologists agree that there are ªwhat pattern?º Yet, despite the lack of likely two major types of memory: explicit (or awareness, the subject will nonetheless re- declarative) memory and implicit (or nonde- spond faster and faster, indicating that the pat- clarative) memory. The former typically re- tern has been detected, albeit unconsciously. fers to memory that can be stated declara- A partial list of other examples of implicit tively, that can be brought to mind as an memory includes conditioning, skilled motor image or proposition, that exists in some tem- learning, and artificial grammar learning. poral time frame, and that, at least in the human adult, is memory of which we are con- What is the Neurobiological Bases of sciously aware. In discussions of develop- Memory? ment, however, it may not be reasonable to impose the requirement of conscious aware- Although cognitive psychologists have con- ness on the nonverbal organism, particularly ducted hundreds of clever and ingenious stud- the human infant (see Nelson, 1997, for dis- ies designed to distinguish these types of cussion). Examples of explicit memory typi- memory at the behavioral level (e.g., see Tul- Effects of stress 795 ving, 1985 for discussion), much of the evi- the effect of leaving him with severe antero- dence in support of this distinction has come grade amnesia. R.B. was of normal intelli- from cognitive neuroscience. Here the ques- gence and performed normally in cognitive tion has been whether there are different neu- tasks except those involving explicit memory, ral systems that subserve these different types on which he was severely impaired. After 5 of memory. Based on several decades of re- years of study, R.B. died, leaving his brain to search, it now appears that explicit memory be examined by the investigators (see depends disproportionately on structures that Schacter, 1996 for a summary of this case). lie in the medial temporal lobe (e.g., hippo- Based on previous work by this group (for campus, rhinal cortex, parahippocampal gy- contemporaneous and subsequent reviews, see rus), whereas the structures that subserve im- Squire, 1986, 1987, 1992, 1994), as well as plicit memory vary depending on the subtype work with monkeys in which selective lesions of memory being discussed. For example, vi- were performed (e.g., Bachevalier & Mishkin, sual perceptual priming likely depends on ar- 1984; Malamut, Saunders, & Mishkin, 1984; eas of the visual cortex, whereas auditory Mishkin, 1982; Zola±Morgan, Squire, Rem- word priming might depend on the auditory pel, Clower, & Amaral, 1992), the authors cortex.
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