Infantile Experience with Suckling Odors Determines Adult Sexual Behavior in Male Rats

Fillion, Thomas J.; Blass, Elliott M.

doi:10.1126/science.3945807

Cited by 182 publications

(113 citation statements)

References 20 publications

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“…Specifically, low levels of endogenous CORT maintain pups' unique ability to learn predominantly approach responses to their mother. This unique neonatal learning produces neural changes in the olfactory bulb that are still present in adulthood and that may underlie the neonatal attachment odor's ability to enhance mate choice and sexual and maternal behavior (Fillion & Blass, 1986;Fleming, O'Day, Kraemer, 1999;Moore et al, 1996). Mean (± SEM) number of conditioned odor choices in a Y-maze test (total of five trials) for (A) sensitive-period Postnatal Day (PN) 8 pups and (B) post-sensitive-period PN12 pups.…”

Section: Discussionmentioning

confidence: 99%

Corticosterone Influences on Mammalian Neonatal Sensitive-Period Learning.

Moriceau

Sullivan

2004

Behavioral Neuroscience

104

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Infant rats exhibit sensitive-period odor learning characterized by olfactory bulb neural changes and odor preference acquisitions critical for survival. This sensitive period is coincident with low endogenous corticosterone (CORT) levels and stress hyporesponsivity. The authors hypothesized that low corticosterone levels modulate sensitive-period learning. They assessed the effects of manipulating CORT levels by increasing and removing CORT during (Postnatal Day 8) and after (Postnatal Day 12) the sensitive period. Results show that (a) exogenous CORT prematurely ends sensitive-period odor-shock-induced preferences; (b) adrenalectomy developmentally extends the sensitive period as indicated by odor-shock-induced odor-preference learning in older pups, whereas CORT replacement can reinstate fear learning; and (c) CORT manipulation modulates olfactory bulb correlates of sensitive-period odor learning in a manner consistent with behavior.Sensitive periods for enhanced learning have been documented in a wide range of species. For example, language acquisition in humans is more easily learned prior to puberty, the ewe has a few hours postpartum when she may bond with her lamb, and imprinting in avian species occurs during the first few hours posthatching. However, sensitive periods can also involve suppression of other types of learning that could interfere with attachment and learning about the mother, such as fear conditioning, inhibitory conditioning, and passive avoidance

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Section: Discussionmentioning

confidence: 99%

Corticosterone Influences on Mammalian Neonatal Sensitive-Period Learning.

Moriceau

Sullivan

2004

Behavioral Neuroscience

104

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“…Infant experiences result in long-term adaptations that program subsequent behavioral, endocrine, and neural function (3,14,57,61). In addition, infant odors have a powerful modulatory influence on adult behaviors (62,63). This phenomenon is not exclusive to odors associated with typical attachment experiences; it extends to trauma experienced within the context of attachment because the odor learned through our infant-trauma paradigm reduces adult fear learning, attenuates amygdala activity, rescues depressive-like behavior in the sucrose consumption test and FST, and decreases CORT (Fig.…”

Section: Mechanisms Underlying Modulation Of Adult Neurobehavioral Fumentioning

confidence: 99%

Enduring good memories of infant trauma: Rescue of adult neurobehavioral deficits via amygdala serotonin and corticosterone interaction

Rincón-Cortés

Barr

Mouly

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Children form a strong attachment to their caregiver-even when that caretaker is abusive. Paradoxically, despite the trauma experienced within this relationship, the child develops a preference for trauma-linked cues-a phenomenon known as trauma bonding. Although infant trauma compromises neurobehavioral development, the mechanisms underlying the interaction between infant trauma bonding (i.e., learned preference for trauma cues) and the long-term effects of trauma (i.e., depressive-like behavior, amygdala dysfunction) are unknown. We modeled infant trauma bonding by using odor-shock conditioning in rat pups, which engages the attachment system and produces a life-long preference for the odor that was paired with shock. In adulthood, this trauma-linked odor rescues depressive-like behavior and amygdala dysfunction, reduces corticosterone (CORT) levels, and exerts repair-related changes at the molecular level. Amygdala microarray after rescue implicates serotonin (5-HT) and glucocorticoids (GCs), and a causal role was verified through microinfusions. Blocking amygdala 5-HT eliminates the rescue effect; increasing amygdala 5-HT and blocking systemic CORT mimics it. Our findings suggest that infant trauma cues share properties with antidepressants and safety signals and provide insight into mechanisms by which infant trauma memories remain powerful throughout life.E arly-life trauma is associated with compromised neurobehavioral development and vulnerability to later-life psychiatric disorders like depression (1-5). Long-lasting effects of infant trauma relevant to depression include disruptions in social behavior, alterations in the serotonin (5-HT) system, and amygdala dysfunction (2, 5-8), which have been replicated by animal models (9-15). Paradoxically, trauma-linked cues-even those associated with abusive attachment-can elicit strong attraction and feelings of comfort in humans (16,17). Furthermore, a lifelong attraction to trauma-linked cues has also been demonstrated in rodent models of infant trauma, which suggests that sensory cues learned during infancy alter adult behaviors and amygdala activity (12,18,19).To explore the enduring effects of infant trauma and the mechanisms underlying their modulation by infant trauma-linked cues, we used an odor-learning paradigm during the sensitive period for attachment learning in rat pups, postnatal (PN) days 8-12, which is characterized by rapid and robust odor-preference learning that extends to aversive stimuli (14,(20)(21)(22). Specifically, we used infant olfactory classical conditioning in which a novel peppermint odor is paired with a mild shock (0.5 mA, 1s) to produce a preferred odor that functions behaviorally as a maternal odor and results in neural activation comparable with that induced by natural maternal odor (20,(23)(24)(25). During the sensitive period, low endogenous levels of corticosterone (CORT) and attenuated shock-induced CORT release prevent the infant amygdala from exhibiting the learning-induced plasticity required for avoidance learning (1...

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“…Em ratos, o imprinting sexual tem sido mostrado por meio de experimentos no qual um odor cítrico foi colocado no ventre de ratas lactantes durante todo o período de lactação. Os filhotes dessas ratas, quando adultos, passaram a ter clara preferência por ratas sexualmente receptivas que apresentavam o mesmo odor cítrico que suas mães (FILLION;BLASS, 1986).…”

Section: Discussionunclassified

Efeitos Do Estresse Pré-Natal Sobre O Comportamento De Preferência Sexual De Ratos Machos Na Idade Adulta

et al. 2015

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RESUMOO objetivo deste estudo foi analisar os efeitos do estresse pré-natal repetido por contenção sobre a preferência sexual de ratos Wistar na idade adulta, quando somente as mães e/ou filhotes foram submetidos à intervenção. Para esse experimento, ratas da linhagem Wistar foram expostas a 30 minutos de estresse por contenção 4 vezes por dia na última semana de gravidez. No primeiro dia de vida pós-parto, os filhotes foram submetidos à adoção cruzada e divididos nos seguintes grupos: filhotes não-estressados prenatalmente adotados por mães não-estressadas prenatalmente (C-c), filhotes não estressados prenatalmente adotados por mães estressadas (Ep-c), filhotes estressados prenatalmente adotados por mães não-estressadas (C-ep) e filhotes estressados prenatalmente adotados por mães também estressadas prenatalmente (Ep-ep). Para avaliação da preferência sexual, os filhotes machos adultos dos quatro grupos formados foram expostos simultaneamente a fêmeas receptivas e não receptivas (castradas). Os resultados mostraram que o estresse pré-natal realizado na última semana de gestação foi capaz de prejudicar a preferência sexual somente de machos dos grupos Ep-ep e C-ep. Todavia, não foram observadas diferenças para os demais grupos. Assim, nosso estudo mostrou que o ambiente pós-natal não foi capaz de reverter os efeitos produzidos pelo estresse gestacional sobre o comportamento de preferência sexual de filhotes na idade adulta. Palavras-chave: Ratos Wistar. Estresse pré-natal. Adoção cruzada. Preferência sexual. ABSTRACTThe purpose of this study was to analyze the effects of repeated prenatal restraint stress on sexual partner preference in Wistar rats in adulthood, when only mothers and/or offspring were submitted to intervention. In this study, female Wistar rats were exposed to 30 minutes of restraint stress 4 times per day in the last week of pregnancy. On the first day of postnatal life, pups were cross-fostered and assigned to the following

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Infantile Experience with Suckling Odors Determines Adult Sexual Behavior in Male Rats

Cited by 182 publications

References 20 publications

Corticosterone Influences on Mammalian Neonatal Sensitive-Period Learning.

Corticosterone Influences on Mammalian Neonatal Sensitive-Period Learning.

Enduring good memories of infant trauma: Rescue of adult neurobehavioral deficits via amygdala serotonin and corticosterone interaction

Efeitos Do Estresse Pré-Natal Sobre O Comportamento De Preferência Sexual De Ratos Machos Na Idade Adulta

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