Caregiver-associated cues, including those learned in abusive attachment, provide a sense of safety and security to the child. Here, we explore how cues associated with abusive attachment, such as maternal odor, can modify the enduring neurobehavioral effects of early-life abuse. Two early-life abuse models were used: a naturalistic paradigm, where rat pups were reared by an abusive mother; and a more controlled paradigm, where pups underwent peppermint odor-shock conditioning that produces an artificial maternal odor through engagement of the attachment circuit. Animals were tested for maternal odor preference in infancy, forced swim test (FST), social behavior, and sexual motivation in adulthood-in the presence or absence of maternal odors (natural or peppermint). Amygdala odor-evoked local field potentials (LFPs) via wireless electrodes were also examined in response to the maternal odors in adulthood. Both early-life abuse models induced preference for the maternal odors in infancy. In adulthood, these early-life abuse models produced FST deficits and decreased social behavior, but did not change sexual motivation. Presentation of the maternal odors rescued FST and social behavior deficits induced by early-life abuse and enhanced sexual motivation in all animals. In addition, amygdala LFPs from both abuse animal models showed unique activation within the gamma frequency (70-90 Hz) bands in response to the specific maternal odor present during early-life abuse. These results suggest that attachment-related cues learned during infancy have a profound ability to rescue neurobehavioral dysregulation caused by early-life abuse. Paradoxically, abuse-associated cues seem to acquire powerful and enduring antidepressive properties and alter amygdala modulation.

The bonding and early life attachment between the infant and caregiver is a dynamic, bidirectional process involving caregiver nurturing of the infant, as well as complementary infant behavior that elicits parental care. Attachment appears to have a dual function. The first function is to ensure the infant remains close to the caregiver in order to receive necessary care for survival. Interestingly, animal research has shown that both nurturing and painful stimuli associated with the caregiver support attachment. Secondly, the quality of attachment and its associated sensory stimuli organize the brain to define the infant's cognitive and emotional development. Specifically, the patterning and quality of care regulate the infant's brain function and behavioral expression that determines long-term emotional regulation. These issues, presented within an historical view of infant attachment, highlight the importance of integrating human and animal research in understanding infant care.