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Allostasis, Allostatic Load, and the Aging Nervous System: Role of Excitatory Amino Acids and Excitotoxicity*

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Allostasis, Allostatic Load, and the Aging Nervous System: Role of Excitatory Amino Acids and Excitotoxicity* Neurochemical Research, Vol. 25, Nos. 9/10, 2000, pp. 1219–1231 Allostasis, Allostatic Load, and the Aging Nervous System: Role of Excitatory Amino Acids and Excitotoxicity* Bruce S. McEwen1 (Accepted March 15, 2000) The adaptive responses of the body to challenges, often known as “stressors”, consists of active re- sponses that maintain homeostasis. This process of adaptation is known as “allostasis”, meaning “achieving stability through change”. Many systems of the body show allostasis, including the au- tonomic nervous system and hypothalamo-pituitary-adrenal (HPA) axis and they help to re-estab- lish or maintain homeostasis through adaptation. The brain also shows allostasis, involving the ac- tivation of nerve cell activity and the release of neurotransmitters. When the individual is challenged repeatedly or when the allostatic systems remain turned on when no longer needed, the mediators of allostasis can produce a wear and tear on the body that has been termed “allostatic load”. Ex- amples of allostatic load include the accumulation of abdominal fat, the loss of bone minerals and the atrophy of nerve cells in the hippocampus. Circulating stress hormones play a key role, and, in the hippocampus, excitatory amino acids and NMDA receptors are important mediators of neuronal atrophy. The aging brain seems to be more vulnerable to such effects, although there are consider- able individual differences in vulnerability that can be developmentally determined. Yet, at the same time, excitatory amino acids and NMDA receptors mediate important types of plasticity in the hip- pocampus. Moreover, the brain retains considerable resilience in the face of stress, and estrogens appear to play a role in this resilience. This review discusses the current status of work on under- lying mechanisms for these effects. KEY WORDS: Allostasis; allostatic load; aging brain; excitatory amino acid; excitotoxicity. INTRODUCTION hormones. In the nervous system, for example, neuro- transmitters are released by neuronal activity, and they When the body is challenged by unexpected or threat- produce effects locally to either propagate or inhibit fur- ening events, it reacts physiologically in an adaptive ther neural activity. Neurotransmitters and hormones are manner in order to maintain homeostasis. This process is usually released during a discrete period of activation called “allostasis”, literally “maintaining stability through and then are shut off, and the mediators themselves are change” (1) and it involves the production and/or release removed from the intracellular space by reuptake or me- of physiological mediators such as adrenalin from the ad- tabolism in order not to prolong their effects. When the renal medulla and glucocorticoids from the adrenal cor- shut off or removal of the mediator does not occur, ef- tex. However, allostasis also applies to organs and tis- fects of the mediators on target cells are prolonged, lead- sues of the body, as well as the production of systemic ing to other consequences that may include receptor de- sensitization and tissue damage. This process has been 1 Harold and Margaret Milliken Hatch Laboratory of Neuroendocrinol- named “allostatic load” (2,3), and it refers to the price the ogy, Rockefeller University, 1230 York Avenue, New York, N.Y. 10021. Fax: 212 327 8634; E-mail: [email protected] tissue or organ pays for an overactive or inefficiently * Special issue dedicated to the 25th anniversary of Neurochemical Re- managed allostatic response. Therefore, allostatic load search. refers to the “cost” of adaptation. 1219 0364-3190/00/09/1000–1219$18.00/0 © 2000 Plenum Publishing Corporation 1220 McEwen The processes of allostasis and allostatic load have cium channels increases in hippocampal CA1 pyramidal been described and measured for metabolic and cardio- neurons of aging rats and results in an increased after- vascular changes that are associated with obesity, Type 2 hyperpolarization (18). Some of this can be mimicked in diabetes and cardiovascular disease (4). However, ele- a cell culture system. In embryonic hippocampal neurons vated and prolonged secretion of glucocorticoids during that are maintained for 28d in cell culture, there is en- aging has also been associated with impairment of cog- hanced calcium channel activity and increased after- nitive function in rodents (5–7) and in humans (8–10). hyperpolarization that are accompanied by decreased Moreover, the endogenous excitatory amino acid neuro- neuronal survival; blocking L-type calcium channels in- transmitters appear to play a major role in these changes creased neuronal survival (19). It is interesting to note (7) even though they are also an essential part of normal that the increased after-hyperpolarization is associated synaptic neurotransmission and plasticity. Their actions with alterations of two important neurophysiologic re- lead to the formation of free radicals that can damage sponses in CA1 pyramidal neurons of the hippocampus, nerve cells, leading to the search for agents that can in- namely, enhanced induction of long-term depression terfere with free radical production or enhance free rad- (LTD) and an impaired induction of long-term potentia- ical quenching. tion (LTP)(20). Thus, insofar as LTP and LTD may be In spite of its vulnerability, the brain retains consid- related to synaptic plasticity during learning (21), these erable resilience in the face of challenges to adapt through age-related changes suggest a possible basis for cogni- allostasis. Studies on the hippocampus reveal a number of tive impairment in aging rats (20). types of structural plasticity, ranging from neurogenesis Glucocorticoids enhance calcium channel activity in the dentate gyrus to remodelling of dendrites to the for- and after-hyperpolarization (18;22), and hippocampal mation and replacment of synapses. These changes, along glucocorticoid receptor expression shows a progressive with compensatory neurochemical and neuroendocrine failure of negative feedback regulation in old versus responses, provide the brain with a considerable amount young rats. In young rats, repeated stress causes a down- of resilience. This has led to a search for agents that help regulation of glucocorticoid receptor levels, thus de- the brain maintain its resilience as it ages. This article dis- creasing glucocorticoid efficacy on various target genes, cusses allostasis and allostatic load in the brain in relation whereas this down-regulation is lost with increasing age, to the aging process and a number of brain disorders in thus potentiating glucocorticoid actions, some of which which there is overactivity of stress mediators that causes may be destructive to brain cells (23). Therefore, there is brain dysfunction. It also discusses the topic of neuropro- a natural mechanism in the young hippocampus for re- tection and the potential value of estrogens and flavonoids silience in the face of repeated stress that acts to reduce as anti-oxidants in promoting allostasis and enhancing re- the magnitude of the glucocorticoid feedback signal and silience and countering the allostatic load promoted by thus reduce the impact of glucocorticoids on calcium excitatory amino acids and other free radical generators channel activity, among other effects. This may be pro- such as the beta amyloid protein. tective, insofar as increased calcium channel activity Age-Related Shifts of Calcium Homeostasis and Its contributes to free radical generation and other processes Consequences. The hippocampus is a brain region that is that may damage neurons (24,25). With the loss of very important for declarative and spatial learning and stress-induced down-regulation of glucocorticoid recep- memory, and yet is a particularly vulnerable and sensitive tors, older rats appear to lose this protective device and region of the brain that expresses high levels of receptors may be more vulnerable to increased levels of glucocor- for adrenal steroid “stress” hormones (11,12). Hippocam- ticoids, particularly in cognitively-impaired rats (23). pal neurons are vulnerable to seizures, strokes and head It is still unclear whether outright neuronal loss is a trauma, as well as responding to stressful experiences major event in the aging hippocampus of cognitively- (12–14). At the same time these neurons show remarkable impaired rats ((26,27); see (28) for review). Neverthe- and paradoxical plasticity, involving long-term synaptic less, there are indications that gene products associated potentiation and depression, dendritic remodeling, synap- with neurodegeneration and damage are differentially tic turnover and neurogenesis in the case of the dentate regulated in the aging-impaired brain compared to un- gyrus (15–17). This will be discussed further below. impaired aging rats and young rats, although the inter- Studies in animal models have shown that the hip- pretation of the results is very complex (29). In aging, pocampus undergoes progressive changes with age in cognitively-impaired rats, the levels of mRNA for the calcium homeostasis, in the plasticity of response to glu- 695 amino acid form of the beta amyloid precursor pro- cocorticoids, and in the expression of markers related to tein (betaAPP) and for the magnesium-dependent super- neuroprotection and damage. The activity of L-type cal- oxide dismutase (Mg-SOD) were both elevated through- Allostasis, Allostatic Load, and the Aging Nervous System 1221 out the hippocampus compared with young rats; at the production and/or removal of a mediator
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