No abstract

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.

To examine the contribution of whisker inputs to the initial emergence and subsequent refinement of the rodent whisking pattern we combined surgical treatments producing varying degrees of postnatal whisker deafferentation with observations and video analysis of whisking across the first month of life. Whisking emerges during the second postnatal week, preceding eye opening by a few days. In contrast to the absence of deafferentation effects in adults, whisker deafferentation in pups, if carried out between the second and third postnatal week, delays (but does not prevent) the emergence of whisker movements and disrupts the development of normal whisking kinematics and coordination. The extent of the delay varies directly with the reduction in whisker input. When regeneration of the nerve is prevented by a cyanoacrylate block emergence of the normal pattern may be delayed indefinitely. Moreover, section of the whisker motor nerve contralateral to the deafferented side, substantially potentiates the effects of the initial deafferentation. These results confirm and extend an earlier description of the development of whisking in normal rat pups (Welker, Behaviour 12:223-244, 1964), fix the time of its initial emergence more precisely at P (postnatal day) 11-13, and suggest a critical role for trigeminal afference in the development of the normal whisking pattern. They are discussed in relation to the development of pattern generating mechanisms in the rodent whisker system.

The present series of experiments assessed how information from the whiskers controls and modulates infant rat behavior during early learning and attachment. Passive vibrissal stimulation can elicit behavioral activity in pups throughout the first two postnatal weeks, although orienting to the source of stimulation is evident only after ontogenetic emergence of whisking. In addition, while pups were capable of demonstrating learning in a classical conditioning paradigm pairing vibrissa stimulation with electric shock, no corresponding changes were detected in the anatomy of the barrel cortex as determined by cytochrome oxidase (CO) staining. Finally, the role of whiskers in a more naturalistic setting was determined in postnatal day (PN)3-5 and PN11-12 pups. Our results showed that both nipple attachment and huddling were disrupted in whisker-clipped PN3-5 pups but only marginally altered in PN11-12 pups. Together, these results suggest that the neonatal whisker system is behaviorally functional and relevant for normal mother-infant interactions, though it lacks the sophistication of a mature whisker system that evokes very specific and directed responses.