Divergent maternal behavioral patterns in two genetic animal models of depression

Braw, Yoram; Malkesman, Oz; Merenlender, Avia; Dagan, M.; Bercovich, A.; Lavi-Avnon, Yael; Weller, Aron

doi:10.1016/j.physbeh.2008.10.002

Cited by 15 publications

(12 citation statements)

References 49 publications

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“…Abusive behavior has been referred to as the de facto stressor in limited bedding studies using rats (Roth and Sullivan, 2005 ; Raineki et al, 2010 , 2012 ). Since reports of mouse studies did not reveal any changes in total on-nest time and licking/grooming behaviors (Baram et al, 2012 ) previously observed in rats (Roth and Sullivan, 2005 ; Braw et al, 2009 ; Raineki et al, 2010 , 2012 ; Dalle Molle et al, 2012 ), it was thought that limited nesting materials induces stress in mice through different means, namely fragmented maternal care. Our results, however, indicate that ELS mouse pups are negatively affected by increased nest entries as they vocalize immediately after the dam enters the nest, while the longer on-nest periods are unaffected.…”

Section: Discussionmentioning

confidence: 95%

Early-Life Stress Paradigm Transiently Alters Maternal Behavior, Dam-Pup Interactions, and Offspring Vocalizations in Mice

Heun-Johnson

Levitt

2016

Front. Behav. Neurosci.

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Animal models can help elucidate the mechanisms through which early-life stress (ELS) has pathophysiological effects on the developing brain. One model that has been developed for rodents consists of limiting the amount of bedding and nesting material during the first postnatal weeks of pup life. This ELS environment has been shown to induce “abusive” behaviors by rat dams towards pups, while mouse dams have been hypothesized to display “fragmented care”. Here, as part of an ongoing study of gene-environment interactions that impact brain development, we analyzed long observation periods of wild-type C57Bl/6J dams caring for wild-type and Met heterozygous pups. Met encodes for the MET receptor tyrosine kinase, which is involved in cortical and hippocampal synaptogenesis. Dams with limited resources from postnatal day (P)2 to P9 preserved regular long on-nest periods, and instead increased the number of discrete dam-pup interactions during regular off-nest periods. Immediately after dams entered the nest during off-nest periods in this ELS environment, pups responded to these qualitatively different interactions with an increased number of ultrasonic vocalizations (USV) and audible vocalizations (AV), communication signals that have been associated with aversive and painful stimuli. After returning to control conditions, nest entry behaviors normalized, and dams did not show altered anxiety-like or contextual fear learning behaviors after pup weaning. Furthermore, female mice that had undergone ELS as pups did not show atypical nest entry behaviors in control conditions in adulthood, suggesting that these specific maternal behaviors are not learned during the ELS period. The results suggest that atypical responses of both mother and pups during exposure to this ELS environment likely contribute to long-term negative outcomes in mice, and that these responses more closely resemble the effects of limited bedding on rat dams and pups than was previously suggested. Discerning how different early-life stressors mediate changes in maternal-pup interactions can help elucidate the mechanisms of ELS on brain development and behavior.

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Section: Discussionmentioning

confidence: 95%

Early-Life Stress Paradigm Transiently Alters Maternal Behavior, Dam-Pup Interactions, and Offspring Vocalizations in Mice

Heun-Johnson

Levitt

2016

Front. Behav. Neurosci.

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“…These data agree with our previous work using a similar model [ 41 ], but appear to be in contrast with other results [ 61 ]. Although in other studies the restriction of nesting material did not change arched-back or licking-grooming behavior [ 62 ], the ability to develop adequate maternal care in absence of nesting material varies between strains [ 63 , 64 ].…”

Section: Discussionmentioning

confidence: 99%

Sex-dependent impact of early-life stress and adult immobilization in the attribution of incentive salience in rats

et al. 2018

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Early life stress (ELS) induces long-term effects in later functioning and interacts with further exposure to other stressors in adulthood to shape our responsiveness to reward-related cues. The attribution of incentive salience to food-related cues may be modulated by previous and current exposures to stressors in a sex-dependent manner. We hypothesized from human data that exposure to a traumatic (severe) adult stressor will decrease the attribution of incentive salience to reward-associated cues, especially in females, because these effects are modulated by previous ELS. To study these factors in Long-Evans rats, we used as an ELS model of restriction of nesting material and concurrently evaluated maternal care. In adulthood, the offspring of both sexes were exposed to acute immobilization (IMO), and several days after, a Pavlovian conditioning procedure was used to assess the incentive salience of food-related cues. Some rats developed more attraction to the cue predictive of reward (sign-tracking) and others were attracted to the location of the reward itself, the food-magazine (goal-tracking). Several dopaminergic markers were evaluated by in situ hybridization. The results showed that ELS increased maternal care and decreased body weight gain (only in females). Regarding incentive salience, in absolute control animals, females presented slightly greater sign-tracking behavior than males. Non-ELS male rats exposed to IMO showed a bias towards goal-tracking, whereas in females, IMO produced a bias towards sign-tracking. Animals of both sexes not exposed to IMO displayed an intermediate phenotype. ELS in IMO-treated females was able to reduce sign-tracking and decrease tyrosine hydroxylase expression in the ventral tegmental area and dopamine D1 receptor expression in the accumbens shell. Although the predicted greater decrease in females in sign-tracking after IMO exposure was not corroborated by the data, the results highlight the idea that sex is an important factor in the study of the long-term impact of early and adult stressors.

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“…Although these factors may be important, other unpublished data from our lab suggest that our strain/type of dams showed consistent compensatory maternal behavior during diverse types of ELS treatments, and compensatory maternal behavior may differ among strains (Millstein and Holmes, 2007). Furthermore, the capability to develop adequate maternal care in absence of nesting material varies profoundly between the strains of mice (Wei et al, 2010) and rats (Braw et al, 2009). …”

Section: Discussionmentioning

confidence: 99%

Sex-dependent effects of an early life treatment in rats that increases maternal care: vulnerability or resilience?

Fuentes

Daviu

Gagliano

et al. 2014

Front. Behav. Neurosci.

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Early life stress (ELS) in rodents has profound long-term effects that are partially mediated by changes in maternal care. ELS not only induces “detrimental” effects in adulthood, increasing psychopathology, but also promotes resilience to further stressors. In Long-Evans rats, we evaluated a combination of two procedures as a model of ELS: restriction of bedding during the first post-natal days and exposure to a “substitute” mother. The maternal care of biological and “substitute” mothers was measured. The male and female offspring were evaluated during adulthood in several contexts. Anxiety was measured by the elevated plus-maze (EPM), acoustic startle response (ASR) and forced swim test (FST). In other group of animals, novelty-seeking was measured (activity in an inescapable novel environment, preference for novel environments and exploration of novel objects). Plasmatic ACTH and corticosterone in basal conditions and in response to stress were also measured. Cognitive impulsivity was assessed by a delay-discounting paradigm, and impulsive action, attention and compulsive-like behavior by a five choice serial reaction time task (5CSRTT). ELS decreased pup body weight and increased the care of the biological mother; however, the “substitute” mother did not exhibit overt maltreatment. A mixture of “detrimental” and “beneficial” effects was shown. In the 5CSRTT, attention was impaired in both genders, and in females, ELS increased compulsive-like behavior. Novel object exploration was only increased by ELS in males, but the preference for novel spaces decreased in both genders. Baseline anxiety (EPM and ASR) and recognition memory were not affected. Unexpectedly, ELS decreased the ACTH response to novelty and swim stress and increased active coping in the FST in both genders. Cognitive impulsivity was decreased only in females, but impulsive action was not affected. The enhancement in maternal care may “buffer” the effects of ELS in a context-dependent manner.

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Divergent maternal behavioral patterns in two genetic animal models of depression

Cited by 15 publications

References 49 publications

Early-Life Stress Paradigm Transiently Alters Maternal Behavior, Dam-Pup Interactions, and Offspring Vocalizations in Mice

Early-Life Stress Paradigm Transiently Alters Maternal Behavior, Dam-Pup Interactions, and Offspring Vocalizations in Mice

Sex-dependent impact of early-life stress and adult immobilization in the attribution of incentive salience in rats

Sex-dependent effects of an early life treatment in rats that increases maternal care: vulnerability or resilience?

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