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Survival of altricial infants depends on attachment to the caregiver – a process that requires infants to identify, learn, remember, and approach their attachment figure. Here we review the neurobiology of attachment in infant rats where learning about the caregiver is supported by a specialized attachment neural circuitry to promote the infant-caregiver relationship. Specifically, the attachment circuit relies on infants acquiring learned preferences to the maternal odor, and this behavior is supported by the hyperfunctioning locus coeruleus and generous amounts of norepinephrine to produce experience-induced changes in the olfactory bulb and anterior piriform cortex. Infants also possess a reduced ability to acquire learned aversions or fear, and this behavior is facilitated through attenuated amygdala plasticity to block fear learning. Presumably, this attachment circuitry constrains the infant animal to express only learned preferences regardless of the quality of care received. As pups mature, and begin to travel in and out of the nest, the specialized attachment learning becomes contextually confined to when pups are with the mother. Thus, when outside the nest, these older pups show learning more typical of adult learning, presumably to prepare for independent life outside the nest. The quality of attachment can alter this circuitry, with early life stress prematurely terminating the pups’ access to the attachment system through premature functional activation of the amygdala. Overall, the attachment circuit appears to have a dual function: to keep pups close to the caregiver but also to shape pups’ behavior to match the environment and define long-term emotion and cognition.

The following experiments determined that the somatosensory whisker system is functional and capable of experience-dependent behavioral plasticity in the neonate before functional maturation of the somatosensory whisker cortex. First, unilateral whisker stimulation caused increased behavioral activity in both postnatal day (P) 3–4 and P8 pups, whereas stimulation-evoked cortical activity (14C 2-deoxyglucose autoradiography) was detectable only in P8 pups. Second, neonatal rat pups are capable of forming associations between whisker stimulation and a reinforcer. A classical conditioning paradigm (P3–P4) showed that the learning groups (paired whisker stimulation–shock or paired whisker stimulation–warm air stream) exhibited significantly higher behavioral responsiveness to whisker stimulation than controls. Finally, stimulus-evoked somatosensory cortical activity during testing [P8; using14C 2-deoxyglucose (2-DG) autoradiography] was assessed after somatosensory conditioning from P1–P8. No learning-associated differences in stimulus-evoked cortical activity were detected between learning and nonlearning control groups. Together, these experiments demonstrate that the whisker system is functional in neonates and capable of experience-dependent behavioral plasticity. Furthermore, in contrast to adult somatosensory classical conditioning, these data suggest that the cortex is not required for associative somatosensory learning in neonates.

If a helpless newborn infant does not form an attachment to its care-giver, even an abusive one, its chances of survival diminish, so evolution should strongly favour attachment by the infant, regardless of the quality of care-giving(1). As a part of the brain called the amygdala is critical for learned fear in adult animals(2, 3, 4), we investigated whether the development of learned avoidance behaviour could be delayed by late maturation of amygdala function. We found that very young rat pups exposed to various odours associated with shock treatment learn an approach response to that odour, whereas older pups learn odour avoidance. We show that the origin and development of learned odour-avoidance behaviour is associated with enhanced neural responses in the amygdala during odour-shock conditioning.