The neurobiology of safety and threat learning in infancy

Abstract

What an animal needs to learn to survive is altered dramatically as they change from dependence on the parent for protection to independence and reliance on self-defense. This transition occurs in most altricial animals, but our understanding of the behavioral neurobiology has mostly relied on the infant rat. The transformation from dependence to independence occurs over three weeks in pups and is accompanied by complex changes in responses to both natural and learned threats and the supporting neural circuitry. Overall, in early life, the threat system is quiescent and learning is biased towards acquiring attachment related behaviors to support attachment to the caregiver and proximity seeking. Caregiver-associated cues learned in infancy have the ability to provide a sense of safety throughout lifetime. This attachment/safety system is activated by learning involving presumably pleasurable stimuli (food, warmth) but also painful stimuli (tailpinch, moderate shock). At about the midway point to independence, pups begin to have access to the adult-like amygdala-dependent threat system and amygdala-dependent responses to natural dangers such as predator odors. However, pups have the ability to switch between the infant and adult-like system, which is controlled by maternal presence and modification of stress hormones. Specifically, if the pup is alone, it will learn fear but if with the mother it will learn attachment (10–15 days of age). As pups begin to approach weaning, pups lose access to the attachment system and rely only on the amygdala-dependent threat system. However, pups learning system is complex and exhibits flexibility that enables the mother to override the control of the attachment circuit, since newborn pups may acquire threat responses from the mother expressing fear in their presence. Together, these data suggest that the development of pups’ threat learning system is not only dependent upon maturation of the amygdala, but it is also exquisitely controlled by the environment. Most notably the mother can switch pup learning between attachment to threat learning in a moment’s notice. This enables the mother to navigate pup’s learning about the world and what is threatening and what is safe.

Social Fear Learning: from Animal Models to Human Function

“…Rodent studies show that early in infancy, learning is biased towards attachment to a caregiver and FC is quiescent [71]. However, from birth on pups can acquire threat responses from their mother through SFL [27, 33].…”

Repeated cross‐fostering affects maternal behavior and olfactory preferences in rat pups

“…It is noteworthy that the mother's odor has special control over the pups in the postnatal period 10–15. Specifically, at this age, the pups are crossing the transitional sensitive period, in which the maternal stimuli have the unique ability to prevent the learning of threats through suppression of amygdala activity mediated by the presence of the mother in the nest (Debiec & Sullivan, ; Opendak & Sullivan, ; Sullivan & Holman, ; Upton & Sullivan, ). Therefore, it is not uncommon for our results to show a strong olfactory preference for the odor of the adoptive and biological mother of the offspring who were submitted to the late RCF protocol of the postsensitive period.…”

“…The mother's odor is critical to the survival of rat pups, as it is through it that the pup seeks and approaches the mother to protect itself, warm up and feed itself. In addition, the maternal odor also regulates mother-infant interactions early in life, when attachment learning is fully favored and aversive learning is attenuated to prevent pups from avoiding their caregiver (Debiec & Sullivan, 2017; Al Aïn, Raineki, Sullivan, & Wilson, 2016;Raineki, Pickenhagen, et al, 2010). It is noteworthy that the mother's odor has special control over the pups in the postnatal period 10-15.…”

“…Several studies have consistently shown that mother–pup attachment is a learning process and consequently that this initial filial relationship depends on memory formation (Landers & Sullivan, ; Opendak & Sullivan, ; Sullivan & Wilson, ). In both humans and animals, attachment requires a brief learning experience of the sensory characteristics of the maternal figure (odor, texture, color, sound) that occurs during the infant's first interactions with its caregiver (Debiec & Sullivan, ; Raineki, Moriceau, & Sullivan, ; Sullivan & Holman, ).…”

“…In rats, the olfactory response of the pup to the odor of the mother is evaluated by orientation and approach behavior toward the odor source and is formed during the first 10 days of the pup's life. In this period, also called the attachment sensitive period, pups can easily be conditioned to a different odor than the maternal one, as long as it is paired with thermal and tactile stimuli (Debiec & Sullivan, ; Landers & Sullivan, ; Meyer & Alberts, ), indicating an associative learning process.…”