Abstract
Early life trauma alters later life emotions, including fear. To better understand mediating mechanisms, we subjected pups to either predictable or unpredictable trauma, in the form of paired or unpaired odor-0.5 mA shock conditioning which, during a sensitive period, produces an odor preference and no learning respectively. Fear conditioning and its neural correlates were then assessed after the sensitive period at postnatal day (PN)13 or in adulthood, ages when amygdala-dependent fear occurs. Our results revealed that paired odor-shock conditioning starting during the sensitive period (PN8–12) blocked fear conditioning in older infants (PN13) and pups continued to express olfactory bulb-dependent odor preference learning. This PN13 fear learning inhibition was also associated with suppression of shock-induced corticosterone, although the age appropriate amygdala-dependent fear learning was reinstated with systemic corticosterone (3 mg/kg) during conditioning. On the other hand, sensitive period odor-shock conditioning did not prevent adult fear conditioning, although freezing, amygdala and hippocampal 2-DG uptake and corticosterone levels were attenuated compared to adult conditioning without infant conditioning. Normal levels of freezing, amygdala and hippocampal 2-DG uptake were induced with systemic corticosterone (5 mg/kg) during adult conditioning. These results suggest that the contingency of early life trauma mediates at least some effects of early life stress through learning and suppression of corticosterone levels. However, developmental differences between infants and adults are expressed with PN13 infants' learning consistent with the original learned preference, while adult conditioning overrides the original learned preference with attenuated amygdala-dependent fear learning.
Highlights
Life maltreatment and stress influence the normal development of neural systems – more the amygdala and the hippocampus – and are associated with both infant and adult mental health vulnerability (Glaser, 2000; Grossman et al, 2003; Teicher et al, 2003; Hammock and Levitt, 2006; Gunnar and Quevedo, 2007)
We found that infant odor conditioning attenuated adult fear conditioning and amygdala 2-DG uptake if the same CS odor was used in infancy and adulthood, or the infant odor was present as context during adult conditioning with a novel odor CS
EXPERIMENT 1: EXPERIENCE WITH SENSITIVE PERIOD ODOR-SHOCK MAINTAINS THE ODOR PREFERENCE AND BLOCKS FEAR LEARNING IN PUPS This experiment assessed whether extended, daily conditioning initiated during the sensitive period (PN9 is the last day of odor-shock preference learning) could switch the preference learning to odor aversion learning if the conditioning was continued in postsensitive period pups (PN10 and older)
Summary
Life maltreatment and stress influence the normal development of neural systems – more the amygdala and the hippocampus – and are associated with both infant and adult mental health vulnerability (Glaser, 2000; Grossman et al, 2003; Teicher et al, 2003; Hammock and Levitt, 2006; Gunnar and Quevedo, 2007). The amygdala’s failure to be recruited during odor-shock conditioning in pups may ensure that infants maintain a preference for the neonatally
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