Stress During Adolescence Shapes Performance in Adulthood: Context‐Dependent Effects on Foraging and Vigilance

Exposure to chronic stress during adolescence can shape behaviour, cognition and physiology in adulthood, but the consequences of these long‐term changes remain unclear. Prior studies reporting altered performance following exposure to stress in adolescence have generally interpreted lasting changes as impairments. However, we have recently shown that exposure to chronic unpredictable stress during adolescence (from post‐natal days 30–70) can enhance performance in a context‐dependent manner during a foraging task. Increases in foraging performance, (previously measured by the number of rewards obtained), are often associated with trade‐offs in other behaviours, such as vigilance. Here, we examined the effect of stress exposure in adolescence on adult foraging in male Sprague Dawley rats to determine (1) whether the increase in foraging performance exhibited by animals exposed to stress in adolescence is balanced by a decrease in vigilance, and (2) whether stress in adolescence alters time allocation between foraging and vigilance behaviours in low‐ and high‐threat conditions. We found no evidence of a trade‐off between foraging and vigilance; under low‐threat conditions, rats exposed to stress in adolescence spent more time being vigilant compared with unstressed rats, suggesting that exposure to stress in adolescence enhances anticipation of threat in adulthood. Under high‐threat conditions, adolescent‐stressed and unstressed rats did not differ in foraging and vigilance behaviours. Given that we have previously found that rats exposed to stress in adolescence nearly double food intake under high‐threat, and we now show that high‐performing rats do not spend more time foraging, it appears that stress exposure in adolescence may enhance foraging efficiency (food consumed/time) under high‐threat conditions rather than time allocation between foraging and competing behaviours. We also examined the relationship, at the level of the individual, between foraging performance and foraging and vigilance behaviours. We found that changes in individual foraging performance between low‐ and high‐threat conditions were independent of behavioural changes (i.e. both highly and poorly performing rats were equally active and contacted a similar number of patches). This suggests that the ability to obtain many rewards under high‐threat conditions may be related to efficiency, rather than the frequency of foraging and effort‐related behaviours.     

Developmental regulation of fear learning and anxiety behavior by endocannabinoids

The developing brain undergoes substantial maturation into adulthood and the development of specific neural structures occurs on differing timelines. Transient imbalances between developmental trajectories of corticolimbic structures, which are known to contribute to regulation over fear learning and anxiety, can leave an individual susceptible to mental illness, particularly anxiety disorders. There is a substantial body of literature indicating that the endocannabinoid (eCB) system critically regulates stress responsivity and emotional behavior throughout the life span, making this system a novel therapeutic target for stress‐ and anxiety‐related disorders. During early life and adolescence, corticolimbic eCB signaling changes dynamically and coincides with different sensitive periods of fear learning, suggesting that eCB signaling underlies age‐specific fear learning responses. Moreover, perturbations to these normative fluctuations in corticolimbic eCB signaling, such as stress or cannabinoid exposure, could serve as a neural substrate contributing to alterations to the normative developmental trajectory of neural structures governing emotional behavior and fear learning. In this review, we first introduce the components of the eCB system and discuss clinical and rodent models showing eCB regulation of fear learning and anxiety in adulthood. Next, we highlight distinct fear learning and regulation profiles throughout development and discuss the ontogeny of the eCB system in the central nervous system, and models of pharmacological augmentation of eCB signaling during development in the context of fear learning and anxiety.     

Short‐ and long‐chain natural polyamines play specific roles in adult cricket neuroblast proliferation and neuron differentiation in vitro

In the house cricket (Acheta domesticus) mushroom bodies, neurogenesis still occurs during adulthood. Using in vitro approaches, the respective roles of natural polyamines in neurogenesis were examined. Mushroom body neuroblast proliferation was assayed in organotypic culture using 5‐bromo, 2′‐deoxyuridine labeling. The number of labeled cells was significantly increased when putrescine was added to culture medium, whereas spermidine and spermine supplementation did not alter cell proliferation. Conversely, in vitro morphometric studies on mushroom body neurons cultured in a defined medium showed that putrescine addition failed to alter any morphological character of these interneurons, whereas addition of the long‐chain polyamines, spermidine and spermine, stimulated neuron differentiation. These two polyamines significantly increased total neurite length; moreover, spermidine‐treated cells exhibited more branches than the controls. The present data demonstrate that putrescine has a mitogenic effect on mushroom body neuronal precursors, and that spermidine and spermine, which failed to induce neuroblast proliferation, act on neuronal differentiation, inducing neurite outgrowth. Our results indicate that short‐ and long‐chain polyamines play specific roles during neurogenesis, and provide a basis for further studies on neuronal precursor proliferation and differentiation. © 2001 John Wiley & Sons, Inc. J Neurobiol 48: 315–324, 2001     

Behavioural mating displays depend on mitochondrial function: a potential mechanism for linking behaviour to individual condition

Males of many animal species court females using complex behavioural displays that are challenging to produce, and some of these displays have been shown to be associated with aspects of male quality. However, the mechanisms by which behavioural displays are linked to individual condition remain uncertain. Herein, we illustrate fundamental mechanistic connections between mitochondrial function and neurogenesis, energy production, and a variety of pathways that underlie the ability of an individual to perform complex behaviours. We consider the biomedical evidence for how mitochondrial activity shapes neurogenesis during development and neural function in adulthood, and how both genetics and environmental conditions can cause variation in mitochondrial function in wild animals. An individual's mitochondrial phenotype determines not just metabolism and available energy, but also appears to serve as an important driver of capacity to perform cognitively complex and other challenging display behaviours. We apply this concept to the example of birdsong, a well‐studied display behaviour with known links to neural pathways, and we describe how mitochondrial involvement in a variety of important internal processes creates links between display quality and key traits like immunocompetence. By synthesizing the intimate involvement of mitochondria in neural processes with the physiological bases of display behaviour, we aim to provide new mechanistic explanations for information that females may gain by assessing complex male displays.     

Turning Shy on a Winter's Day: Effects of Season on Personality and Stress Response in Microtus arvalis

Animal personalities are by definition stable over time, but to what extent they may change during development and in adulthood to adjust to environmental change is unclear. Animals of temperate environments have evolved physiological and behavioural adaptations to cope with the cyclic seasonal changes. This may also result in changes in personality: suites of behavioural and physiological traits that vary consistently among individuals. Winter, typically the adverse season challenging survival, may require individuals to have shy/cautious personality, whereas during summer, energetically favourable to reproduction, individuals may benefit from a bold/risk‐taking personality. To test the effects of seasonal changes in early life and in adulthood on behaviours (activity, exploration and anxiety), body mass and stress response, we manipulated the photoperiod and quality of food in two experiments to simulate the conditions of winter and summer. We used the common voles (Microtus arvalis) as they have been shown to display personality based on behavioural consistency over time and contexts. Summer‐born voles allocated to winter conditions at weaning had lower body mass, a higher corticosterone increase after stress and a less active, more cautious behavioural phenotype in adulthood compared to voles born in and allocated to summer conditions. In contrast, adult females only showed plasticity in stress‐induced corticosterone levels, which were higher in the animals that were transferred to the winter conditions than to those staying in summer conditions. These results suggest a sensitive period for season‐related behavioural plasticity in which juveniles shift over the bold–shy axis.     

The Role of Adolescent Behaviors in the Female–Male Disparity in Obesity Incidence in US Black and White Young Adults

In the United States, black women are at much greater risk for obesity than black men. We explored whether adolescent behaviors (family dinners, hours of television, playing sports with mother, playing sports with father, bouts of physical activity) were associated with gender disparity in 6‐year obesity incidence in young adulthood. We used data from the nationally representative National Longitudinal Study of Adolescent Health to examine adolescent behaviors in nonimmigrant black (n = 1,503) and white (n = 4,452) youths in 1994–95 (aged 11–19 years) and 1995–96 (aged 12–20). We assessed gender disparity in obesity incidence (female incidence minus male incidence) during young adulthood (2001–02; aged 18–26). Standardized gender disparities were calculated using race‐ and gender‐stratified, covariate‐adjusted logistic regression models in which males and females were set to the same distributions of adolescent behaviors. In adolescence, black females reported less leisure‐time physical activity and lower likelihood of playing sports with either parent compared with black males. Setting adolescent behaviors equal for black males and females did not reduce the estimated gender disparity in obesity incidence (nonstandardized: 9.8 percentage points (95% confidence interval (CI): 4.5, 15.1); fully standardized: 10.2 percentage points (5.2, 15.2)). There was little gender disparity in whites before or after adjustments. To our knowledge, this is the first study to examine to what extent behavioral differences during adolescence might account for gender disparity in obesity incidence in black young adults. Male‐female differences in these adolescent behaviors did not appear to underlie the gender gap in young adult obesity.     

Repeatability of dispersal behaviour in a common dwarf spider: evidence for different mechanisms behind short‐ and long‐distance dispersal

Abstract 1. The response of dispersal towards evolution largely depends on its heritability for which upper limits are determined by the trait’s repeatability. 2. In the Linyphiid spider E. atra, we were able to separate long‐ and short‐distance dispersal behaviours (respectively ballooning and rappelling) under laboratory conditions. By performing repeated behavioural trials for females, we show that average dispersal trait values decrease with increasing testing days. By comparing mated and unmated individuals during two periods (before and after mating for the mated group, and the same two periods for the unmated group), we show that mating has no effect on the mean displayed dispersal behaviour or its within‐individual variation. Repeatabilities were high and consistent for ballooning motivation, but not for rappelling. 3. Ballooning motivation can be regarded as highly individual‐specific behaviour, while general pre‐dispersal and rappelling behaviours showed more individual variation. Such difference in repeatability between long‐ and short‐distance dispersal suggests that short‐ and long‐distance dispersal events are triggered by different ecological and evolutionary mechanisms.     

Cytometry in the brain: studying differentiation to diagnostic applications in brain disease and regeneration therapy

During brain development, a population of uniform embryonic cells migrates and differentiates into a large number of neural phenotypes – origin of the enormous complexity of the adult nervous system. Processes of cell proliferation, differentiation and programmed death of no longer required cells, do not occur only during embryogenesis, but are also maintained during adulthood and are affected in neurodegenerative and neuropsychiatric disease states. As neurogenesis is an endogenous response to brain injury, visible as proliferation (of to this moment silent stem or progenitor cells), its further stimulation can present a treatment strategy in addition to stem cell transfer for cell regeneration therapy. Concise techniques for studying such events in vitro and in vivo permit understanding of underlying mechanisms. Detection of subtle physiological alterations in brain cell proliferation and neurogenesis can be explored, that occur during environmental stimulation, exercise and ageing. Here, we have collected achievements in the field of basic research on applications of cytometry, including automated imaging for quantification of morphological or fluorescence‐based parameters in cell cultures, towards imaging of three‐dimensional brain architecture together with DNA content and proliferation data. Multi‐parameter and more recently in vivo flow cytometry procedures, have been developed for quantification of phenotypic diversity and cell processes that occur during brain development as well as in adulthood, with importance for therapeutic approaches.     

NCAM deficiency in the mouse forebrain impairs innate and learned avoidance behaviours

The neural cell adhesion molecule (NCAM) has been implicated in the development and plasticity of neural circuits and the control of hippocampus‐ and amygdala‐dependent learning and behaviour. Previous studies in constitutive NCAM null mutants identified emotional behaviour deficits related to disturbances of hippocampal and amygdala functions. Here, we studied these behaviours in mice conditionally deficient in NCAM in the postmigratory forebrain neurons. We report deficits in both innate and learned avoidance behaviours, as observed in elevated plus maze and passive avoidance tasks. In contrast, general locomotor activity, trait anxiety or neophobia were unaffected by the mutation. Altered avoidance behaviour of the conditional NCAM mutants was associated with a deficit in serotonergic signalling, as indicated by their reduced responsiveness to (±)‐8‐hydroxy‐2‐(dipropylamino)‐tetralin‐induced hypo-thermia. Another serotonin‐dependent behaviour, namely intermale aggression that is massively increased in constitutively NCAM‐deficient mice, was not affected in the forebrain‐specific mutants. Our data suggest that genetically or environmentally induced changes of NCAM expression in the late postnatal and mature forebrain determine avoidance behaviour and serotonin (5‐HT)_1A receptor signalling.     

Adolescents' perceived weight associated with depression in young adulthood: a longitudinal study

Objective: The objective of this study is to examine whether adolescents’ measured BMI and self‐ or mother's perception of weight status at age 14 are associated with depression at age 21. Research Methods and Procedures: The study participants were a subsample of 2017 participants of the Mater–University of Queensland Study of Pregnancy and Its Outcomes, a population‐based birth cohort study, which commenced in 1981 in Brisbane, Australia, for whom measured BMI at ages 14 and 21 and information on self‐reported mental health problems were available at the age 21 follow‐up. A total of 1802 individuals had measured BMI and reported weight perception in a supplementary questionnaire at 14 years, and their self‐reported mental health problems were reported at 21 years. Mental health was measured using Center for Epidemiology Studies Depression Scale and Young Adults Self‐Reported depression/anxiety at 21 years of age. Results: We found that both young adult males and females who perceived themselves as overweight at age 14 had more mental health problems compared with those who perceived themselves as the right weight. When we combined adolescents’ weight perception with their measured BMI categories, weight perception but not measured overweight was associated with mental health problems for males and females at age 21. This association remained after adjusting for potential confounders, including adolescents’ behavioral problems, family meals, diet, physical activity, and television watching. Conclusions: This study suggests that the perception of being overweight during adolescence is a significant risk factor for depression in young adult men and women. The perception of being overweight during adolescence should be considered a possible target for a prevention intervention.     

Male aggression,limited female choice and the ontogeny of mating behaviour in the flesh fly Sarcophaga crassipalpis

Previous work has shown that male flesh flies (Sarcophaga crassipalpis Macquart) exhibit an ontogeny of behaviour from eclosion through sexual maturity that includes extensive changes in the expression of aggressive, non‐aggressive interactive and non‐interactive behaviours. To determine how the presence of a female flesh fly influences the manifestation of these behaviours, male flesh flies of different ages post‐eclosion are paired with same‐age females and their behaviours are monitored in a simple arena during a 50‐min observation period. All flies are socially isolated until pairing. Although the levels of expression of aggressive and non‐aggressive interactive behaviours are depressed relative to previous findings in male‐opponent pairs, the ontogeny of aggression still occurs as indicated by a significant increase, with age, in the agonistic behaviour ‘hold’. Similar to male‐opponent pairs and individual males, the performance by males of the non‐interactive behaviours ‘walking’ and ‘standing’ diminishes, whereas ‘upside‐down’ increases with age. By contrast, ‘grooming’ shows a significant age‐related decline. No courtship behaviours are observed in the males, although the aggressive behaviour ‘hold’ is a significant transition to mating. Females show no obvious courtship or rejection behaviours, although the significant increase in ‘upside‐down’ with age could possibly be a behavioural gateway to mating. The results of this study indicate that extensive age‐related changes encompassing the entire behavioural repertoire are intrinsic to male flesh flies and persist under a variety of different social contexts.     

Sensorimotor gating and spatial learning in α7‐nicotinic receptor knockout mice

The role of acetylcholine and specific nicotinic receptors in sensorimotor gating and higher cognitive function has been controversial. Here, we used a commercially available mouse with a null mutation in the Chrna7^tm1Bay gene [α7‐nicotinic acetylcholine receptor (nAChR) knockout (KO) mouse] in order to assess the role of the α7‐nAChR in sensorimotor gating and spatial learning. We examined prepulse inhibition (PPI) of startle and nicotine‐induced enhancement of PPI. We also tested short‐ and long‐term habituation of the startle response as well as of locomotor behaviour in order to differentiate the role of this receptor in the habituation of evoked behaviour (startle) vs. motivated behaviour (locomotion). To address higher cognition, mice were also tested in a spatial learning task. Our results showed a mild but consistent PPI deficit in α7‐nAChR KO mice. Furthermore, they did not show nicotine‐induced enhancement of startle or PPI. Short‐ and long‐term habituation was normal in KO mice for both types of behaviours, evoked or motivated, and they also showed normal learning and memory in the Barnes maze. Thorough analysis of the behavioural data indicated a slightly higher degree of anxiety in α7‐nAChR KO mice; however, this could only be partially confirmed in an elevated plus maze test. In summary, our data suggest that α7‐nAChRs play a minor role in PPI, but seem to mediate nicotine‐induced PPI enhancement. We found no evidence to suggest that they are important for habituation or spatial learning .     

Anxiety‐related behavioral inhibition in rats: a model to examine mechanisms underlying the risk to develop stress‐related psychopathology

Behavioral inhibition (BI) is an adaptive defensive response to threat; however, children who display extreme BI as a stable trait are at risk for development of anxiety disorders and depression. The present study validates a rodent model of BI based on an ethologically relevant predator exposure paradigm. We show that individual differences in rat BI are stable and trait‐like from adolescence into adulthood. Using in situ hybridization to quantify expression of the immediate early genes homer1a and fos as measures of neuronal activation, we show that individual differences in BI are correlated with the activation of various stress‐responsive brain regions that include the paraventricular nucleus of the hypothalamus and CA3 region of the hippocampus. Further supporting the concept that threat‐induced BI in rodents reflects levels of anxiety, we also show that BI is decreased by administration of the anxiolytic, diazepam. Finally, we developed criteria for identifying extreme BI animals that are stable in their expression of high levels of BI and also show that high BI (HBI) individuals exhibit maladaptive appetitive responses following stress exposure. These findings support the use of predator threat as a stimulus and HBI rats as a model to study mechanisms underlying extreme and stable BI in humans.     

Water loss and temperature interact to compound amphibian vulnerability to climate change

Ectotherm thermal physiology is frequently used to predict species responses to changing climates, but for amphibians, water loss may be of equal or greater importance. Using physical models, we estimated the frequency of exceeding the thermal optimum (T_opt) or critical evaporative water loss (EWL_crit) limits, with and without shade‐ or water‐seeking behaviours. Under current climatic conditions (2002–2012), we predict that harmful thermal (>T_opt) and hydric (>EWL_crit) conditions limit the activity of amphibians during ~70% of snow‐free days in sunny habitats. By the 2080s, we estimate that sunny and dry habitats will exceed one or both of these physiological limits during 95% of snow‐free days. Counterintuitively, we find that while wet environments eliminate the risk of critical EWL, they do not reduce the risk of exceeding T_opt (+2% higher). Similarly, while shaded dry environments lower the risk of exceeding T_opt, critical EWL limits are still exceeded during 63% of snow‐free days. Thus, no single environment that we evaluated can simultaneously reduce both physiological risks. When we forecast both temperature and EWL into the 2080s, both physiological thresholds are exceeded in all habitats during 48% of snow‐free days, suggesting that there may be limited opportunity for behaviour to ameliorate climate change. We conclude that temperature and water loss act synergistically, compounding the ecophysiological risk posed by climate change, as the combined effects are more severe than those predicted individually. Our results suggest that predictions of physiological risk posed by climate change that do not account for water loss in amphibians may be severely underestimated and that there may be limited scope for facultative behaviours to mediate rapidly changing environments.     

Ecological genetics of sediment browsing behaviour in a planktonic crustacean

Zooplankton can display complex habitat selection behaviours that influence the way they interact with their environments. Some species, although primarily pelagic, can exploit sediment‐borne particles as a food source or use sediments as a refuge from pelagic predation. However, this strategy may increase the exposure to other risks such as benthic predation and infection from sediment‐borne parasite transmission stages. The evolution of habitat selection behaviour in these species is thus expected to be influenced by multiple and possibly contrasting selective forces. Here, we study the browsing behaviour of the water flea Daphnia magna on bottom sediments. First, we demonstrated genetic variation for sediment browsing among D. magna genotypes from natural populations sampled across a broad geographic range. Next, we used an F2 recombinant panel to perform a QTL analysis and identified three regions in the D. magna genome contributing to variation in browsing behaviour. We also analysed the correlation between our data and previously published data on the phototactic behaviour of genotypes from the same F2 panel. Clonal means of the two behavioral traits were not correlated, suggesting that they may evolve independently. Browsing behaviour is likely to be a relevant component of habitat selection in D. magna, and its study may help to incorporate the interactions with the sediment into eco‐evolutionary models of this key freshwater species.     

Parental death in childhood and pathways to increased mortality across the life course in Stockholm,Sweden: A cohort study

BackgroundPrevious studies have shown that the experience of parental death during childhood is associated with increased mortality risk. However, few studies have examined potential pathways that may explain these findings. The aim of this study is to examine whether familial and behavioural factors during adolescence and socioeconomic disadvantages in early adulthood mediate the association between loss of a parent at age 0 to 12 and all-cause mortality by the age of 63.Methods and findingsA cohort study was conducted using data from the Stockholm Birth Cohort Multigenerational Study for 12,615 children born in 1953, with information covering 1953 to 2016. Familial and behavioural factors at age 13 to 19 included psychiatric and alcohol problems in the surviving parent, receipt of social assistance, and delinquent behaviour in the offspring. Socioeconomic disadvantage in early adulthood included educational attainment, occupational social class, and income at age 27 to 37. We used Cox proportional hazard regression models, combined with a multimediator analysis, to separate direct and indirect effects of parental death on all-cause mortality.Among the 12,582 offspring in the study (men 51%; women 49%), about 3% experienced the death of a parent in childhood. During follow-up from the age of 38 to 63, there were 935 deaths among offspring. Parental death was associated with an elevated risk of mortality after adjusting for demographic and household socioeconomic characteristics at birth (hazard ratio [HR]: 1.52 [95% confidence interval: 1.10 to 2.08, p-value = 0.010]). Delinquent behaviour in adolescence and income during early adulthood were the most influential mediators, and the indirect associations through these variables were HR 1.03 (1.00 to 1.06, 0.029) and HR 1.04 (1.01 to 1.07, 0.029), respectively. After accounting for these indirect paths, the direct path was attenuated to HR 1.35 (0.98 to 1.85, 0.066). The limitations of the study include that the associations may be partly due to genetic, social, and behavioural residual confounding, that statistical power was low in some of the subgroup analyses, and that there might be other relevant paths that were not investigated in the present study.ConclusionsOur findings from this cohort study suggest that childhood parental death is associated with increased mortality and that the association was mediated through a chain of disadvantages over the life course including delinquency in adolescence and lower income during early adulthood. Professionals working with bereaved children should take the higher mortality risk in bereaved offspring into account and consider its lifelong consequences. When planning and providing support to bereaved children, it may be particularly important to be aware of their increased susceptibility to delinquency and socioeconomic vulnerability that eventually lead to higher mortality.

In this cohort study, Ayako Hiyoshi and colleagues show associations between parental death in a child’s life and mortality risk later in that child’s life.     

A lack of functional NK1 receptors explains most,but not all,abnormal behaviours of NK1R‐/‐ mice1

Mice lacking functional neurokinin‐1 receptors (NK1R‐/‐) display abnormal behaviours seen in Attention Deficit Hyperactivity Disorder (hyperactivity, impulsivity and inattentiveness). These abnormalities were evident when comparing the behaviour of separate (inbred: ‘Hom’) wildtype and NK1R‐/‐ mouse strains. Here, we investigated whether the inbreeding protocol could influence their phenotype by comparing the behaviour of these mice with that of wildtype (NK1R+/+) and NK1R‐/‐ progeny of heterozygous parents (‘Het’, derived from the same inbred strains). First, we recorded the spontaneous motor activity of the two colonies/genotypes, over 7 days. This continuous monitoring also enabled us to investigate whether the diurnal rhythm in motor activity differs in the two colonies/genotypes. NK1R‐/‐ mice from both colonies were hyperactive compared with their wildtypes and their diurnal rhythm was also disrupted. Next, we evaluated the performance of the four groups of mice in the 5‐Choice Serial Reaction‐Time Task (5‐CSRTT). During training, NK1R‐/‐ mice from both colonies expressed more impulsive and perseverative behaviour than their wildtypes. During testing, only NK1R‐/‐ mice from the Hom colony were more impulsive than their wildtypes, but NK1R‐/‐ mice from both colonies were more perseverative. There were no colony differences in inattentiveness. Moreover, a genotype difference in this measure depended on time of day. We conclude that the hyperactivity, perseveration and, possibly, inattentiveness of NK1R‐/‐ mice is a direct consequence of a lack of functional NK1R. However, the greater impulsivity of NK1R‐/‐ mice depended on an interaction between a functional deficit of NK1R and other (possibly environmental and/or epigenetic) factors.