Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering

Aïn, Syrina Al; Perry, Rosemarie E.; Nuñez, Bestina; Kayser, Kassandra E.; Hochman, Chase; Brehman, Elizabeth; LaComb, Miranda; Wilson, Donald A.; Sullivan, Regina M.

doi:10.1080/17470919.2016.1159605

Cited by 63 publications

(26 citation statements)

References 173 publications

(269 reference statements)

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“…Animal models of caregiver nurturance and caregiver-infant synchrony are needed to better understand the mechanism by which these caregiver styles in early life promote optimal emotional development throughout the lifespan. However, insight can be drawn from existing rodent and primate studies related to mother-infant social buffering [23,48], and social learning [49], which provide evidence of strong maternal regulation of emotional states, emotional learning, and the associated underlying physiology in early life.…”

Section: Bodymentioning

confidence: 99%

Neurobiology of infant attachment: attachment despite adversity and parental programming of emotionality

Perry

Blair

Sullivan

2017

Current Opinion in Psychology

101

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We review recent findings related to the neurobiology of infant attachment, emphasizing the role of parenting quality in attachment formation and emotional development. Current findings suggest that the development of brain structures important for emotional expression and regulation (amygdala, prefrontal cortex, hippocampus) is deeply associated with the quality of care received in infancy, with sensitive caregiving providing regulation vital for programming these structures, ultimately shaping the development of emotion into adulthood. Evidence indicates that without sensitive caregiving, infants fail to develop mechanisms needed for later-life emotion and emotion regulation. Research suggests that a sensitive period exists in early life for parental shaping of emotional development, although further cross-species research is needed to discern its age limits, and thus inform interventions.

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Section: Bodymentioning

confidence: 99%

Neurobiology of infant attachment: attachment despite adversity and parental programming of emotionality

Perry

Blair

Sullivan

2017

Current Opinion in Psychology

101

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“…Previous work provides some insight into the mechanisms that support this learning in humans. For example, in humans and rodents, the mother’s natural odors and food odors experienced in utero are preferred after birth (Mennella 2014; Cooke & Fildes, 2011; Abate et al, 2008; Mennella et al, 2001; Varendi et al, 1996; Pedersen & Blass, 1982), although lack of subsequent exposure to these odors decrease this preference, and novel postnatal odors (natural, perfume) of the mother and other nonrelated caregivers are quickly learned (Al Ain et al, 2016; Schaal, 2015; Mennella et al, 2011; Schaal et al, 2009; Mennella & Beauchamp, 1999). Indeed, in newly born human infants a few minutes of simply pairing a novel odor with tactile stimulation on the first day of life causes that odor to be preferred but also elicits head turns towards that odor and mouthing (Sullivan et al, 1991).…”

Section: Neurobiology Of Attachment Learning: Odor Learning and Safetymentioning

confidence: 99%

The neurobiology of safety and threat learning in infancy

Dębiec

Sullivan

2017

Neurobiology of Learning and Memory

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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.

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“…It is important to note that none of the tested animals had experience with this type of odor. The odor guides the approach and avoidance behaviors that begin at birth in many mammals, including humans (Al Aïn et al, ; Moriceau & Sullivan, ). Olfactory cues are essential for newborn rodents to approach the mother and attach to the nipples and to suppress the ultrasonic vocalizations in the presence of a predator (Perry et al, ; Takahashi, ).…”

Section: Discussionmentioning

confidence: 99%

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

Finkler

Pardo

Lucion

2019

Developmental Psychobiology

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Disturbances in early mother–infant relationships are strongly associated with changes in the development of a number of physiological and behavioral systems in the neonate that can create a complex change in patterns of vulnerability throughout life. Institutionalized children, despite receiving adequate care, display important behavioral changes in adult life, and such changes are strongly associated with a lack of selective and consistent attachment to the maternal figure in early life. It is not yet clear how human adoption processes alter the mother–infant relationship early in life. Here, to mimic the situation of human adoption and explore the impact on the formation of attachment between the infant and a caregiver, we use a repeated cross‐fostering (RCF) model in rodents in two postnatal periods, postnatal days (PND) 1 to 3 (early RCF) and 9 to 11 (late RCF). Early exposure but not late exposure to RCF reduces the pups' preference for the odor of the mother figure. Moreover, early exposure and slightly later exposure to RCF reduce maternal care and motivation in collecting the pups and bringing them to the nest. The RCF protocol creates an unstable environment for mother–pup interaction, but it seems to affect learned attachment to the mother only when it occurs during the corresponding sensitive period of development.

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Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering

Cited by 63 publications

References 173 publications

Neurobiology of infant attachment: attachment despite adversity and parental programming of emotionality

Neurobiology of infant attachment: attachment despite adversity and parental programming of emotionality

The neurobiology of safety and threat learning in infancy

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

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