Fear of novelty in infant rats predicts adult corticosterone dynamics and an early death

Abstract

Individuals who are fearful of novelty have a larger hypothalamicpituitary-adrenal axis response than do nonfearful individuals. We hypothesized that a fearful behavioral style emerging early in life would be associated with life-long altered adrenal activity. Because there is ample physiological evidence both costs and benefits of adrenal activation, we determined whether such a stable emotional-neuroendocrine trait was associated with differential morbidity and mortality. To conduct such lifespan work, we studied a relatively short-lived mammal: the Norway rat. We first established that an animal's hesitation or willingness to explore a novel environment (''neophobia'' and ''neophilia,'' respectively) is an identifiable and stable behavioral trait in young-adult males and that neophobia, compared with neophilia, was associated with a greater glucocorticoid response to novelty. Second, we were able to detect behavioral differences among infant rats within a family, and this behavioral disposition at infancy predicted the magnitude of the glucocorticoid response in late middle age. Males identified as neophobic during infancy died sooner than their less fearful brothers. Although both types of males died with similar pathologies (tumors), neophobic males were 60% more likely to die at any point in time. This lifespan study identifies an emotional trait in infancy that predicts an early death and an associated neuroendocrine trait in adulthood that is a potential mechanism underlying the relationship between behavioral style and longevity.S ome individuals respond to novelty with fear (i.e., ''neophobia''), whereas others do not. Individuals that show behavioral signs of fear also experience increased activation of certain physiological systems, such as amygdala activation, sympathetic activation of the autonomic nervous system, and activation of the hypothalamic-pituitary-adrenal axis (1-4). In humans, the neophobic behavioral͞neuroendocrine response pattern (i) emerges as early as 14 mo of age (5), (ii) is stable during childhood (6, 7), and (iii) is associated with childhood adrenal activation (8-10), which can be both beneficial to and costly for health (11). We have tested the hypothesis that an individual's early propensity to respond fearfully to novelty can have cumulative effects on health and physiology over the lifespan, thereby affecting rate of aging and longevity.In a variety of mammalian species, minimal exploration in the face of novelty is typically interpreted to indicate fear (12, 13). In humans, traits similar to neophobia include behavioral inhibition, shyness, negative affect, extraversion͞surgency, and fearfulness (14-16). Because both fearful animals and fearful children show greater activation of brain areas and physiological systems associated with the classic fight͞flight response (1-4), we refer to a hesitant or stilted behavioral response to novelty as neophobia across species and use ''neophilia'' to refer to an interactive behavioral response to the same stimulus.Previous research o...

Stress response during development predicts fitness in a wild, long lived vertebrate

“…The positive effect of mass residuals on survival is consistent with an intuitive notion that the physical condition of nestlings is also a major determinant on individual fitness, possibly linked to parental quality and/or timing of breeding (20). With regard to the negative association between adrenocortical function and both survival and recruitment, there is evidence that the behavioral and physiological response to stress is consistent over time (8,10,12). High GC responders may trigger more often, or more robust, emergency responses to other sorts of perturbations, not only during development but also later in life.…”

“…However, even within animal populations exposed to constant environments there is a strong interindividual variability in the adrenocortical response to standardized stressors (8)(9)(10), and it remains unknown whether such natural variability exerts an impact on fitness. Only recently, studies in fish, birds, and mammals, including humans, suggest that interindividual differences in stress-coping responses are key attributes defining personality types (10)(11)(12)(13)(14), and variability in natural populations is maintained through different payoffs on adaptive capacity and vulnerability to disease. We tested whether individual variation in the GC response to stress early in life has long-term consequences to unequivocal components of fitness: survival and reproduction.…”

Female temperament, tumor development and life span: Relation to glucocorticoid and tumor necrosis factor α levels in rats

“…females from high-locomotion, high-glucocorticoid families succumbed much earlier than females from low-locomotion, low-glucocorticoid families (Cavigelli, unpublished data). These latter results, in conjunction with prior findings with male mice and rats (Cavigelli and McClintock, 2003;Péréz-Álvarez et al, 2005), suggest that there are important individual differences in the relationship between glucocorticoid overproduction and lifespan. In the present experiment, we hypothesized that female temperaments associated with natural variance in glucocorticoid production would be associated with natural variance in immune function, thereby providing an additional mechanism underlying differential life span among individuals with different behavioral tendencies.…”

“…Novel Non-Social Arena-The arena, previously described in (Cavigelli and McClintock, 2003), was designed to be minimally anxiety-provoking. The square test arena (120cm × 120cm × 46cm) contained a novel rat-sized object in three corners (a plastic tube, an inverted bowl, or a wire tunnel).…”

Patterns of predator neophobia: a meta-analytic review

“…M.C.O. In a study on neophobic rats, Rattus norvegicus, a 20% increase in stress-related mortality occurred [43]. In addition to the energetic cost of a highly vigilant state, it also reduces time allocated to other fitness-related activities.…”