Developmental Lead Exposure in Rats Causes Sex-Dependent Changes in Neurobiological and Anxiety-Like Behaviors that Are Improved by Taurine Co-treatment.

Lead (Pb2+) is a developmental neurotoxicant that causes alterations in the brain's excitation-to-inhibition (E/I) balance by disrupting the development of the GABAergic systems. These GABAergic disruptions have persistent neurobiological and neurobehavioral structure-function relationships that can be examined using animal models of Pb2+ exposure. Further, taurine, a GABA-AR agonist, has been shown to offer neuroprotection against neurodevelopmental Pb2+ exposure and senescence. The present study evaluated the effects of Pb2+ exposure (i.e., at 150 ppm and 1,000 ppm doses) on Long Evans hooded rats during the perinatal period of development on locomotor activity in the open field (OF) and anxiety-like behaviors in the elevated plus maze (EPM). This was followed by an examination of brain mass using an encephalization quotient (EQ) and isotropic fractionation (ITF) of total cells and the number of neurons and non-neuronal cells in the prefrontal cortex, hippocampus, and diencephalon. The results suggest that neurodevelopmental Pb2+ exposure caused persistent anxiety-like behaviors in both the OF and EPM with associated changes in EQ, but not ITF-determined cell density. Further, taurine treatment was observed to compensate for Pb2+ exposure in the behavioral assessments although precise neurobiological mechanisms remain unknown. Thus, more work is required to evaluate the role of taurine and other anxiolytic compounds in the alleviation of neurotoxicant-induced neurobehavioral syndromes and their associated neurobiological correlates.

Challenges to the parental brain: Neuroethological and translational considerations.

Extending from research documenting adaptive parental responses in nonthreatening contexts, the influences of various neuroethological and physiological challenges on effective parenting responses are considered in the current review. In natural habitats, rodent family units are exposed to predators, compromised resources, and other environmental stressors that disrupt HPA axis functions. With the additional physiological demands associated with caring for offspring, alterations in stress-related neuroendocrine responsiveness contribute to adaptive responses in many challenging contexts. Some environmental contexts, however, such as restricted nesting resources, result in disrupted maternal responses that have a negative impact on offspring wellbeing. Additionally, parental dysregulation associated with exposure to environmental chemicals or pharmacological substances, also compromise maternal responses with effects that often extend to future generations. Continued preclinical and clinical research elucidating parental responses to various stressors and physiological disruptors is necessary to provide valuable translational information identifying threats to effective parenting outcomes.

Neuroplasticity in the maternal hippocampus: Relation to cognition and effects of repeated stress.

This article is part of a Special Issue "Parental Care". It is becoming clear that the female brain has an inherent plasticity that is expressed during reproduction. The changes that occur benefit the offspring, which in turn secures the survival of the mother's genetic legacy. Thus, the onset of maternal motivation involves basic mechanisms from genetic expression profiles, to hormone release, to hormone-neuron interactions, all of which fundamentally change the neural architecture - and for a period of time that extends, interestingly, beyond the reproductive life of the female. Although multiple brain areas involved in maternal responses are discussed, this review focuses primarily on plasticity in the maternal hippocampus during pregnancy, the postpartum period and well into aging as it pertains to changes in cognition. In addition, the effects of prolonged and repeated stress on these dynamic responses are considered. The maternal brain is a marvel of directed change, extending into behaviors both obvious (infant-directed) and less obvious (predation, cognition). In sum, the far-reaching effects of reproduction on the female nervous system provide an opportunity to investigate neuroplasticity and behavioral flexibility in a natural mammalian model.

The mother as hunter: significant reduction in foraging costs through enhancements of predation in maternal rats.

In previous laboratory investigations, we have identified enhanced cognition and reduced stress in parous rats, which are likely adaptations in mothers needing to efficiently exploit resources to maintain, protect and provision their immature offspring. Here, in a series of seven behavioral tests on rats, we examined a natural interface between cognition and resource gathering: predation. Experiment 1 compared predatory behavior (toward crickets) in age-matched nulliparous mothers (NULLs) and postpartum lactating mothers (LACTs), revealing a highly significant enhancement of predation in LACT females (mean = -65s in LACTs, vs. -270s in NULLs). Experiment 2 examined the possibility that LACTs, given their increased metabolic rate, were hungrier, and thus more motivated to hunt; doubling the length of time of food deprivation in NULLs did not decrease their predatory latencies. Experiments 3-5, which examined sensory regulation of the effect, indicated that olfaction (anosmia), audition (blockade with white noise), and somatosensation (trimming the vibrissae) appear to play little role in the behavioral enhancement observed in the LACTs; Experiment 6 examined the possibility that visual augmentations may facilitate the improvements in predation; testing LACTs in a 0-lux environment eliminated the behavioral advantage (increasing their latencies from -65s to -212s), which suggests that temporary augmentation to the visual system may be important, and with hormone-neural alterations therein a likely candidate for further study. In contrast, testing NULLS in the 0-lux environment had the opposite effect, reducing their latency to catch the cricket (from -270s to -200s). Finally, Experiment 7 examined the development of predatory behavior in Early-pregnant (PREG), Mid-PREG, and Late-PREG females. Here, we observed a significant enhancement of predation in Mid-PREG and Late-PREG females--at a time when maternity-associated bodily changes would be expected to diminish predation ability--relative to NULLs. Therefore, as with the increasing reports of enhancements to the maternal brain, it is apparent that meaningful behavioral adaptations occur that likewise promote the survival of the mother and her infants at a crucial stage of their lives.

Behavioral training and predisposed coping strategies interact to influence resilience in male Long-Evans rats: implications for depression.

Effective coping strategies and adaptive behavioral training build resilience against stress-induced pathology. Both predisposed and acquired coping strategies were investigated in rats to determine their impact on stress responsiveness and emotional resilience. Male Long-Evans rats were assigned to one of the three coping groups: passive, active, or variable copers. Rats were then randomly assigned to either an effort-based reward (EBR) contingent training group or a non-contingent training group. Following EBR training, rats were tested in appetitive and stressful challenge tasks. Physiological responses included changes in fecal corticosterone and dehydroepiandrosterone (DHEA) metabolites as well as neuropeptide Y (NPY)-immunoreactivity in the hippocampus and amygdala. Regardless of a rat's predisposed coping strategy, EBR rats persisted longer than non-contingent rats in the appetitive problem-solving task. Furthermore, training and coping styles interacted to yield the seemingly most adaptive DHEA/corticosterone ratios in the EBR-trained variable copers. Regardless of training group, variable copers exhibited increased NPY-immunoreactivity in the CA1 region.

Alterations of sex-typical microanatomy: prenatal stress modifies the structure of medial preoptic area neurons in rats.

Prenatal stress disrupts normal sexual differentiation and behavior with concomitant alterations in brain development; however, its effects on the cytoarchitecture of neurons in the sexually dimorphic medial preoptic area (mPOA) of the hypothalamus is not known. Morphometric analysis of the mPOA of adult rats showed sex differences as neurons from control females had significantly greater numbers of basal dendritic branches and cumulative basal dendritic length as compared to control male neurons. Prenatal stress significantly altered these sexual dimorphisms, as prenatally stressed (P-S) males had increased measures of cell body area, perimeter, cumulative basal dendritic length, and branch point numbers as compared to control males. Prenatal stress also altered the cytoarchitecture in the female mPOA neurons as P-S female neurons had significantly greater measures for primary dendritic branch number and a trend towards significance for several additional measures as compared to control females. Therefore, there are significant effects of both sex and prenatal stress on neuronal architecture in the mPOA that may help to explain the well-documented alterations in reproductive behaviors observed in P-S animals.

Characteristic neurobiological patterns differentiate paternal responsiveness in two Peromyscus species.

Rodent paternal models provide unique opportunities to investigate the emergence of affiliative social behavior in mammals. Using biparental and uniparental Peromyscus species (californicus and maniculatus, respectively) we assessed paternal responsiveness by exposing males to biological offspring, unrelated conspecific pups, or familiar brothers following a 24-hour separation. The putative paternal circuit we investigated included brain areas involved in fear/anxiety [cingulate cortex (Cg), medial amygdala (MeA), paraventricular nucleus of the hypothalamus (PVN), and lateral septum (LS)], parental motivation [medial preoptic area (MPOA)], learning/behavioral plasticity (hippocampus), olfaction [pyriform cortex (PC)], and social rewards (nucleus accumbens). Paternal experience in californicus males reduced fos immunoreactivity (ir) in several fear/anxiety areas; additionally, all californicus groups exhibited decreased fos-ir in the PC. Enhanced arginine vasopressin (AVP) and oxytocin (OT)-ir cell bodies and fibers, as well as increased neuronal restructuring in the hippocampus, were also observed in californicus mice. Multidimensional scaling analyses revealed distinct brain activation profiles differentiating californicus biological fathers, pup-exposed virgins, and pup-naïve virgins. Specifically, associations among MPOA fos, CA1 fos, dentate gyrus GFAP, CA2 nestin-, and PVN OT-ir characterized biological fathers; LS fos-, Cg fos-, and AVP-ir characterized pup-exposed virgins, and PC-, PVN-, and MeA fos-ir characterized pup-naïve virgins. Thus, whereas fear/anxiety areas characterized pup-naïve males, neurobiological factors involved in more diverse functions such as learning, motivation, and nurturing responses characterized fatherhood in biparental californicus mice. Less distinct paternal-dependent activation patterns were observed in uniparental maniculatus mice. These data suggest that dual neurobiological circuits, leading to the inhibition of social-dependent anxiety as well as the activation of affiliative responses, characterize the transition from nonpaternal to paternal status in californicus mice.

Neurobiological constituents of active, passive, and variable coping strategies in rats: integration of regional brain neuropeptide Y levels and cardiovascular responses.

Effective coping strategies build resilience against stress-induced pathology. In the current study, young male rats were categorized as active, passive, or variable copers by observing their responses to being gently restrained on their backs (i.e., the back-test). The rats were subsequently exposed to chronic unpredictable stress, which included several ethologically relevant stressors such as predator odors and calls, for approximately three weeks. During this time, the variable copers, defined as rats that demonstrated a variable as opposed to a rigid response to stress, exhibited more seemingly adaptive responsiveness in three successive forced swim tests than the more consistently responding passive and active copers. This behavioral flexibility was accompanied by increased neuropeptide Y-immunoreactivity in the bed nucleus of the stria terminalis (BNST) and the amygdala and increased fos-immunoreactivity in the BNST. Additionally, the alterations in fecal corticosteroid levels and cardiovascular measures (systolic blood pressure and tail blood volume) between baseline and stress conditions differed according to coping strategy. Factor analysis indicates that variable copers were characterized by a distinct cardiovascular and neural response to the stress exposure. These results suggest that this animal coping model may be useful in discerning the adaptive nature of particular response strategies in the face of environmental exigencies.

Enriched Environment Exposure Enhances Social Interactions and Oxytocin Responsiveness in Male Long-Evans Rats.

Both social and physical stimuli contribute to the complexity of an animal's environment, influencing biobehavioral responses to subsequent challenges. In the current study, male Long-Evans rats were randomly assigned to an isolate (ISO), social control (SC) or social enriched (SE) group (n = 8 per group). The SC and SE conditions were group housed with the SE group exposed to physical enrichment stimuli that were natural as opposed to manufactured (e.g., hollowed out log instead of plastic hiding place). On three occasions during their 40-day enriched environment exposure, night/dark phase videos were obtained for 1 h during the early part of the dark phase. During this time, the SE animals exhibited significantly more social grooming with no differences between the SE and SC in the frequency of play or self-grooming bouts. Subsequently, all animals were assessed in social interaction and problem-solving escape tasks during the last week of the enriched environment exposure. SE rats exhibited increased digging bouts toward the restrained conspecific in the social interaction task whereas the other groups exhibited more escape responses. In the problem-solving task, SE animals exhibited a decreased latency to cross the barrier to escape from the predator odor (i.e., cat urine and fur). Neural analyses indicated increased oxytocin-immunoreactive (OT-ir) tissue in the SE supraoptic and paraventricular nuclei of the hypothalamus compared to the other groups. Interestingly, blood samples indicated lower peripheral corticosterone (CORT) and higher OT levels in the ISO animals when compared to the SC and SE animals, an effect retrospectively attributed to separation anxiety in the SE and SC animals in preparation for histology procedures. When the behavioral, neural and endocrine data were visualized as a multifaceted dataset via a multidimensional scaling analysis, however, an association between social enrichment and higher OT involvement was observed in the SE animals, as well as heightened stress responsivity in the ISO and SC groups. In sum, the SE animals exhibited a facilitation of social responses, problem-solving ability and OT immunoreactive responsiveness. These findings provide new information about the influences of both physical and social stimuli in dynamic and enriched environments.

Physiologic Correlates of Interactions between Adult Male and Immature Long-tailed Macaques (Macaca fascicularis).

Interactions between adult males and immature members of the same species are rare in most mammals; in contrast, an estimated 40% of primate species are characterized by an involvement of males in the social life of infants and juveniles. The proximate mechanisms of male-infant interactions are largely unstudied, and very few direct benefits for males have been proposed, especially in uniparental species in which the identity of the male parent is uncertain. In this study, we aimed to assess the relationship among behavioral and physiologic stress, health, and various affiliative behaviors initiated by adult males toward infants and juveniles in long-tailed macaques. We hypothesized that males that spent more time with infants and juveniles would have lower physiologic and social stress and better health than males with less interaction. We observed 2 troops of macaques with established social hierarchies (n = 18 in troop 1 and n = 8 in troop 2), each occupying a stable area within the enclosure, for more than 200 h. Fecal samples were used to assess cortisol levels as a measure of physiologic stress, and blood samples were collected to measure oxytocin levels as an index of social responsiveness. Our results indicated that male affiliative behavior directed toward immature animals was significantly higher in the troop characterized by more social conflicts; midranking males interacted more with infants than high- and low-ranking males in both troops. Furthermore, the DHEA:cortisol ratio, a physiologic index of resilience and coping, was positively correlated with males' affiliative responses, suggesting a neuroprotective role of male-infant interactions. In summary, our data support a proximate mechanism of alloparenting or paternal behavior in uniparental species. Interacting with infants and juveniles could provide an immediate neurobiologic benefit to adult males by facilitating adaptive coping responses to social tensions.

Rising rates of depression in today's society: consideration of the roles of effort-based rewards and enhanced resilience in day-to-day functioning.

Despite the existence of a vastly improved health care system and a multi-billion dollar antidepressant industry, the rates of depression in the US remain alarmingly high. An exploration of lifestyle changes over the past century suggests that the level of physical activity necessary to provide life's basic resources, referred to as effort-based rewards, has diminished in our industrialized, technologically advanced, service-oriented society. The evolution of the accumbens-striatal-cortical circuitry and its modulating neurochemicals in our ancestors played a significant role in sustaining the continued effort critical for the acquisition of resources such as food, water and shelter; consequently, vast reductions in the degree of physical activity required to obtain necessary resources in today's society likely lead to reduced activation of brain areas essential for reward/pleasure, motivation, problem-solving, and effective coping strategies (i.e. depressive symptomology). Comparative cultural and gender analyses reinforce the significant role of effort-based rewards in mood regulation, suggesting that minimal engagement in such endeavors leads to compromised resilience upon exposure to life's stressful challenges. If physical activity is indeed important in the maintenance of mental health, increased emphasis on behavioral and behavioral/cognitive preventative life strategies, as opposed to an emphasis on psychopharmacological strategies directed at very specific neurochemicals after the onset of depression, should be adopted as protective measures against the onset of depressive symptomology. Thus, strategies that include more global neurobiological activation in the relevant context of directed efforts provide a fresh perspective for depression research.

Explorations of coping strategies, learned persistence, and resilience in Long-Evans rats: innate versus acquired characteristics.

In the current investigation, predispositions for coping styles (i.e., passive, flexible, and active) were determined in juvenile male rats. In subsequent behavioral tests, flexible copers exhibited more active responses. In another study, animals were exposed to chronic stress and flexible coping rats had lower levels of corticosteroids. Focusing on the acquired nature of coping strategies, rats receiving extensive training in a task requiring them to dig for food rewards (i.e., effort-based rewards) persisted longer in a challenging task than control animals. Thus, the results suggest that both predisposed coping strategies and acquired behavioral experience contribute to resilience in challenging situations.

Maternal experience produces long-lasting behavioral modifications in the rat.

From 5 to 22 months of age, cognitive and emotional responses of nulliparous, primiparous, and multiparous rats were assessed using a dry land maze (DLM) and an elevated plus-maze (EPM) at 4-month intervals. Parous rats exhibited improved spatial memory in the probe and competitive versions of the DLM, and more exploration in the EPM and a novel stimulus test relative to nulliparous females. The nulliparous females, however, outperformed parous rats during the DLM visual cue test at 17 months of age. At 23 months, no differences in stressed corticosterone levels or Golgi-stained hippocampal neurons were observed. Thus, cognitive and emotional modifications were observed in parous rats; the neurobiological mechanisms for these enduring effects, however, remain to be identified.

Motherhood mitigates aging-related decrements in learning and memory and positively affects brain aging in the rat.

The current work examined spatial learning and memory (i.e., latencies to find a baited food well) in age-matched nulliparous, primiparous and multiparous (NULL, PRIM and MULT, zero, one or two pregnancies and lactations, respectively). We tested at 6, 12, 18 and 24 months of age in a dry land version of the Morris water maze (Main task), and at 12, 18 and 24 months in the same task in which the original location of the baited well was changed (Reversal task). We show that PRIM/MULT rats, compared to the age-matched NULL females, learned the spatial tasks significantly better and exhibited attenuated memory decline, up to 24 months of age. Furthermore, at the conclusion of behavioral testing, we investigated levels of these animals' hippocampal (CA1 and dentate gyrus) immunoreactive amyloid precursor protein (APP), a marker of neurodegeneration and age-related cognitive loss. MULTs had significantly reduced APP in both CA1 and DG, relative to PRIMs and NULLs, and PRIMs had a trend (p<0.06) toward a reduction in APP compared to NULLs in DG. Further, level of APP was negatively correlated with performance in the two tasks (viz., more APP, worse maze performance). Reproduction, therefore, with its attendant natural endocrine and postpartum sensory experiences, may facilitate lifelong learning and memory, and may mitigate markers of neural aging, in the rat. Combining natural hormonal exposure with subsequent substantial experience with stimuli from the offspring may preserve the aged parous female brain relative to that of NULL females.

The clinical neuroscience course: viewing mental health from neurobiological perspectives.

Although the field of neuroscience is booming, a challenge for researchers in mental health disciplines is the integration of basic research findings into applied clinical approaches leading to effective therapies. Recently the National Institute of Mental Health called for translational research grants to encourage collaboration between neuroscientists and mental health professionals. In order for this "clinical neuroscience" to emerge and thrive, an important first step is the provision of appropriate course offerings so that future neuroscience researchers and mental health practitioners will have a common neurobiological base from which to make informed decisions about the most efficacious treatments for mental illnesses. Accordingly, an integrative course, Clinical Neuroscience, was developed to address these issues. After reviewing the historical origins of this emerging discipline, students are exposed to fundamental overviews of neuroanatomy, neurochemistry, and neural development before approaching the neurobiological components of several disorders (e.g., schizophrenia, depression, Tourette's syndrome, drug abuse, obsessive compulsive disorder). Finally, the maintenance of mental health is emphasized as topics such as psychoneuroimmunology, coping with stress, and eating regulation are discussed. Important themes emphasized in this course include (1) the consideration of only empirically based evidence, (2) the view that mental illness represents a disruption of neurobiological homeostasis, (3) the acknowledgement that, because the brain is a plastic organ, the clinical relevance of environmental and behavioral influences is difficult to overestimate, and (4) the recognition of the value of ecologically relevant animal models in the investigation of various aspects of mental illness. Because of the importance of stress maintenance in mental health, exercises have been developed to increase students' awareness of their own coping strategies. Finally, several books and movies are incorporated to provide additional points of view of the topics discussed in the course.

Brains in the city: Neurobiological effects of urbanization.

With a majority of humans now living in cities, strategic research is necessary to elucidate the impact of this evolutionarily unfamiliar habitat on neural functions and well-being. In this review, both rodent and human models are considered in the evaluation of the changing physical and social landscapes associated with urban dwellings. Animal models assessing increased exposure to artificial physical elements characteristic of urban settings, as well as exposure to unnatural sources of light for extended durations, are reviewed. In both cases, increased biomarkers of mental illnesses such as major depression have been observed. Additionally, applied human research emphasizing the emotional impact of environmental threats associated with urban habitats is considered. Subjects evaluated in an inner-city hospital reveal the impact of combined specific genetic vulnerabilities and heightened stress responses in the expression of posttraumatic stress disorder. Finally, algorithm-based models of cities have been developed utilizing population-level analyses to identify risk factors for psychiatric illness. Although complex, the use of multiple research approaches, as described herein, results in an enhanced understanding of urbanization and its far-reaching effects--confirming the importance of continued research directed toward the identification of putative risk factors associated with psychiatric illness in urban settings.

The life and career of Paul MacLean. a journey toward neurobiological and social harmony.

Working as a physician, Paul MacLean's interests moved in the direction of the brain when he realized that most of his patients suffered from symptoms (e.g. anxiety, sleeping problems) that could not be traced to a known physiological cause. His curiosity about the neurological origins of these psychological symptoms led him to the laboratories of Stanley Cobb and James Papez, both of whom were influential in guiding MacLean's interests toward the temporal lobe. His neurobiological interest was not contained, however, to the temporal lobe. As his own family grew to include a wife and five children, his scholarly pursuits extended to social and familial relations and their accompanying underlying neuroanatomical circuits (i.e. the thalamocingulate system). Viewing the brain and behavior from an evolutionary perspective, MacLean introduced the concept of the "triune brain" to describe the evolutionarily distinct components of the mammalian brain and reintroduced Broca's term "limbic" to describe a neuroanatomical system involved in emotional functions. MacLean wrote that the development of social behaviors, such as mother-infant audiovocal communication and the separation cry of the offspring, served as the driving force in the evolution of the neocortex. MacLean's neuroevolutionary perspective and appreciation of the complexity and evolutionary significance of social systems offer valuable insights into the contemporary fields of behavioral neuroscience and biological psychiatry.

Single or multiple reproductive experiences attenuate neurobehavioral stress and fear responses in the female rat.

The female brain is a dynamic structure, which expresses its plasticity most readily following reproductive experience (RE). In Experiment 1, we generated nulliparous (NP), primiparous (PP), and multiparous (MP) females (none, one, and two litters, respectively). Two weeks following the weaning of the first/second six-pup litters, the age-matched MP and PP and the non-pup-exposed NP animals were subjected to a 60-min restraint stress paradigm (enclosure in a Plexiglas restraint tube). The brains were removed and processed for c-fos immunoreactivity (c-fos-IR) in CA3 region of the hippocampus (HI) and in basolateral amygdala (BLA). MP and PP females had very similar numbers of c-fos-IR neurons in both HI and BLA, whereas both were lower than NPs. In a second experiment, the same groups were generated, together with primigravid (PG; first pregnancy) and multigravid (MG; second pregnancy) females, tested in late pregnancy. The animals were exposed to a 30-min trial in an open field and were killed, and the brains were again examined for c-fos-IR. The parous and gravid animals displayed less reactivity to the stress of the open field (i.e., reductions in behavioral measures of anxiety) and significantly less c-fos expression in both CA3 and BLA. The gravid animals displayed significantly less c-fos expression in CA3 and BLA compared to parous females, although neither group differed as a result of a second RE. The data suggest that reproductive (viz., hormonal) and/or maternal (viz., pup exposure) experience may inure a female and her brain to stress, rendering her less susceptible to the behavioral-or other-disruptions that stress sensitivity can produce. Together, these data suggest that the experiences of motherhood (pregnancy, pup exposure, suckling stimulation, etc.) summate to produce reductions in anxiety and stress responsiveness that start before and last long after pup exposure and care. Such reductions may be adaptive in the face of demands placed upon the parous vs. the NP female.

Parity modifies endocrine hormones in urine and problem-solving strategies of captive owl monkeys (Aotus spp.).

Parental behavior modifies neural, physiologic, and behavioral characteristics of both maternal and paternal mammals. These parenting-induced modifications extend to brain regions not typically associated with parental responses themselves but that enhance ancillary responses, such as foraging efficiency and predator avoidance. Here we hypothesized that male and female owl monkeys (Aotus spp.) with reproductive experience (RE) would demonstrate more adaptive ancillary behavioral and neuroendocrine responses than those of their nonRE counterparts. To assess cognitive skills and coping flexibility, we introduced a foraging strategy task, including a set of novel objects (coin holders) marked with different symbols representing different food rewards, to the animals. To assess endocrine responses, urine samples were assayed for cortisol and dehydroepiandrosterone (DHEA) levels and their ratios to determine physiologic measures of emotional regulation in RE and nonRE owl monkeys. Compared with nonRE monkeys, experienced parents had higher DHEA:cortisol ratios after exposure to habituation training and on the first day of testing in the foraging task. Both hormones play critical roles in the stress response and coping mechanisms, and a high DHEA:cortisol ratio usually indicates increased coping skills. In addition, RE monkeys exhibited more efficient foraging responses (by 4-fold) than did the nonRE mating pairs. We conclude that RE modifies relevant behavioral and hormonal responses of both maternal and paternal owl monkeys exposed to a challenging cognitive paradigm. Corroborating previous research demonstrating adaptive modifications in foraging efficiency and emotional responses in reproductively experienced rodents, the current results extend these findings to a monogamous primate species.