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 requires 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 infantcaregiver relationship regardless of the quality of care. With maturation and the end of the infantcaregiver 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 in respect to the amygdala, and these changes may provide important clues to understanding the lasting effects of early stress."…development is essentially a dynamic process that promotes reorganization and adaptation across time" (S. Levine, 1982) The maturing organism has the daunting task of frequently reorganizing behavior to meet not only the demands of a changing environment, but also those of physiological and neural maturation. The myriad processes by which an organism reorganizes its behavior are not well understood, but are thought to include complex interactions between experience, learning, as well as genetic and neural changes. Of course, each reorganization is likely to involve unique processes and can occur either rapidly or gradually. These periods of reorganization, which are also referred to as developmental transitions, are believed to represent periods of vulnerability and have received more experimental attention in recent years (for review see: Adriani and Laviola, 2004;Crews et al. 2007;Hensch, 2004;Hofer and Sullivan, 2008;Rice and Barone, 2000;Sullivan et al., 2009). However, Levine and others have long highlighted the importance of these transitions and the critical role of proper reorganization for normal development (Bell and Denenberg, 1962;Denenberg, 1963;Levine, 1982 Levine, , 2000. Correspondence: Regina M. Sullivan, Emotional Brain Institute, The Nathan S. Kline Institute for Psychiatric Research, 140 Old Orangeburg Road, Orangeburg, NY 10962, Office: 845-398-5511, lab: 845-398-6692, fax: 845-398-2193, regina.sullivan@nyumc.org. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal dis...

Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

“…Although FC occurred before breeding, mothers previously fear-conditioned showed less nurturing behaviors and rougher handling of pups during presentation of the CS (Table 1) and potentially throughout rearing. To control for the possibility that these altered maternal behaviors mediated pups fear to the CS, we used "substitute mothers," a manipulation made possible by maternal acceptance of all pups, as well as pups' failure to distinguish between their mother and a substitute mother matched for the same postpartum period and the same diet (12)(13)(14)(15). Substitute mothers received olfactory FC (or were exposed to the CS alone).…”

“…We have shown above that fear responses to a specific odor are acquired through coexposure to fearful mothers and the CS. Earlier studies demonstrate that social transmission of fear may occur through observational learning in older animals (16)(17)(18)(19), although infant rats lack functional visual and auditory sensory systems until they enter the third week of life (12). However, at birth, pups have a welldeveloped olfactory system, which supports olfactory learning and infant-mother communication (12)(13)(14)(15).…”

“…Earlier studies demonstrate that social transmission of fear may occur through observational learning in older animals (16)(17)(18)(19), although infant rats lack functional visual and auditory sensory systems until they enter the third week of life (12). However, at birth, pups have a welldeveloped olfactory system, which supports olfactory learning and infant-mother communication (12)(13)(14)(15). Olfaction remains important throughout life in rodents, including communicating fear using an alarm odor to support social transmission of fear (20)(21)(22).…”

“…Because the stress hormone CORT is increased by the alarm odor (21) and is critical for pups' fear learning (12)(13)(14), we next explored the possibility that the alarm odor induced an increase in pups' CORT and was critical for pups socially transmitted FC. It should be noted, however, that maternal presence typically socially buffers pups to suppress the US-induced CORT increase and blocks FC until PND 16, although these mothers did not express fear (15).…”

“…Animal studies indicate that the amygdala's lateral and basal nuclei (LBA) play an important role in FC (10). However, FC in infant rats is naturally attenuated until postnatal day (PND) 10 due to low levels of the stress hormone corticosterone (CORT) during the stress hyporesponsive period (11)(12)(13)(14)(15). This fear suppression continues in older pups (until PND 16) in the mother's presence due to social buffering (attenuation) of the shock-induced CORT increase (15).…”