Infant experiences result in long-term adaptations that program brain development and alter later life behaviors. Although infants are biologically predisposed to attach to their caregiver, adverse early life experiences involving the caregiver negatively program neural systems controlling mood, memory, and emotion, and confer susceptibility to later life psychopathology. Clues from clinical and basic research suggest this is due to compromised brain development and disturbed emotion regulation, although the underlying mechanisms remain poorly understood. The studies conducted as part of this thesis employed complementary rodent models of infant trauma, which result in adverse and enduring effects that parallel the neurobiological sequelae of childhood abuse, to better understand the developmental mechanisms by which infant trauma programs a pathway to later life psychopathology.

Both infant trauma paradigms converged in producing a later life depressive-like behavioral phenotype characterized by impaired social interactions, high immobility in the Forced Swim Test (FST), and amygdala dysfunction. However, my thesis studies indicate that olfactory trauma-linked cues have an unexpected positive value in adulthood- they can actually repair the adult neurobehavioral dysregulation resulting from infant trauma. First, the infant trauma odor rescued behavioral indices of depressive-like behavior and reduced corticosterone (CORT) levels during the FST. Second, the infant trauma odor had robust effects on amygdala electrophysiology and normalized atypical amygdala paired pulse activity.

Third, the infant trauma odor altered amygdala gene expression relating to glucocorticoid and serotonin (5-HT) receptor signaling. Blocking amygdala 5-HT eliminated the rescue effect; increasing amygdala 5-HT and blocking CORT mimicked it, highlighting an amygdala 5-HT/CORT interaction as the mechanism underlying the infant trauma odor-mediated rescue of depressive-like behavior. These findings provide insights into the link between childhood abuse and later depression, but also suggest that trauma-linked cues share properties with antidepressants and safety signals, which alter amygdala activity to provide relief from stress and fearful states. In sum, infant trauma-linked cues modulate adult neurobehavioral function by controlling amygdala activity, thereby providing opportunities for intervention and possibly correction of maladaptive outcomes related to psychopathology resulting from infant trauma experienced within attachment.