Transitions in sensitive period attachment learning in infancy: the role of corticosterone

Abstract

Survival of altricial infants, including humans and rats, depends on attachment to the caregiver - a process that requires infants to recognize, learn, and remember their attachment figure. The demands of a dynamic environment combined with a maturing organism require frequent neurobehavioral reorganization. This restructuring of behavior and its supporting neural circuitry can be viewed through the unique lens of attachment learning in rats in which preference learning is enhanced and aversion learning is attenuated. Behavioral restructuring is well adapted to securing the crucial infant-caregiver relationship regardless of the quality of care. With maturation and the end of the infant-caregiver attachment learning period, the complex interplay of neural structures, hormones, and social behavior coordinates the developing rat's eventual transition to life outside of the nest. Nevertheless, early-life environmental and physiological stressors can alter the resilient nature of this system, particularly with respect to the amygdala, and these changes may provide important clues to understanding the lasting effects of early stress.

Figure 1

During a sensitive period, pups approach the natural maternal odor or odors paired with stroking or painful 0.5mA shock as demonstrated by a Y- Maze test (A). Pups cannot nipple attach when the maternal odor is removed, although nipple attachment can be reinstated if the maternal odor, or a classically conditioned odor is presented via an air stream into the testing chamber (B). The natural and artificial maternal odors produce enhanced olfactory bulb responding, as shown here with c-Fos immunohistochemistry (C). Note that mere experience with a novel odor or unpaired presentations of the novel odor and reward does not support learning and does not produce the behavioral changes. Asterisk indicates p<0.05.

Figure 2

Pup attachment learning changes over development. During the earliest days of life, pups have a sensitive period when odor-shock conditioning produces an odor preference. At 10-days of age, pups begin the Transitional Sensitive Period, when pups endogenous corticosterone levels have increased sufficiently to enable amygdala dependent fear/avoidance learning. However, with the mother present at this age pups will revert back to the approach learning of the sensitive period. That is, the mother’s presence will socially buffer pups (i.e. attenuate pups shock-induced corticosterone release) and pups learn a preference. As pups mature, maternal social buffering continues to lower corticosterone but pups only have access to the amygdala dependent fear learning (Moriceau and Sullivan 2006; Raineki et al. 2009; Shionoya et al. 2007; Sullivan et al., 2000a).