Dual circuitry for odor-shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala.
Rat pups must learn maternal odor to support attachment behaviors, including nursing and orientation toward the mother. Neonates have a sensitive period for rapid, robust odor learning characterized by increased ability to learn odor preferences and decreased ability to learn odor aversions. Specifically, odor-0.5 mA shock association paradoxically causes an odor preference and coincident failure of amygdala activation in pups until postnatal day 10 (P10). Because sensitive-period termination coincides with a declining "stress hyporesponsive period" when corticosterone release is attenuated, we explored the role of corticosterone in sensitive-period termination. Odor was paired with 0.5 mA shock in either sensitive-period (P8) or postsensitive-period (P12) pups while manipulating corticosterone. We then assessed preference/aversion learning and the olfactory neural circuitry underlying its acquisition. Although sensitive-period control paired odor-shock pups learned an odor preference without amygdala participation, systemic (3 mg/kg, i.p.; 24 h and 30 min before training) or intra-amygdala corticosterone (50 or 100 ng; during training) permitted precocious odor-aversion learning and evoked amygdala neural activity similar to that expressed by older pups. In postsensitive-period (P12) pups, control paired odor-shock pups showed an odor aversion and amygdala activation, whereas corticosterone-depleted (adrenalectomized) paired odor-shock pups showed odor-preference learning and activation of an odor learning circuit characteristic of the sensitive period. Intra-amygdala corticosterone receptor antagonist (0.3 ng; during training) infused into postsensitive-period (P12) paired odor-shock pups also showed odor-preference learning. These results suggest corticosterone is important in sensitive-period termination and developmental emergence of olfactory fear conditioning, acting via the amygdala as a switch between fear and attraction. Because maternal stimulation of pups modulates the pups' endogenous corticosterone, this suggests maternal care quality may alter sensitive-period duration.
Moriceau
Stephanie
S
Department of Zoology, University of Oklahoma, Norman, Oklahoma 73019, USA. smoriceau@ou.edu
Wilson
Donald A
DA
Levine
Seymour
S
Sullivan
Regina M
RM
D000315:Adrenalectomy / Q000379:methods; D000367:Age Factors; D000679:Amygdala / Q000187:drug effects / Q000502:physiology*; D000704:Analysis of Variance; D000818:Animals; D000831:Animals, Newborn; D001522:Behavior, Animal; D003214:Conditioning, Classical / Q000187:drug effects / Q000502:physiology*; D003345:Corticosterone / Q000378:metabolism* / Q000494:pharmacology; D003847:Deoxyglucose / Q000493:pharmacokinetics; D004644:Emotions; D005260:Female; D006727:Hormone Antagonists / Q000494:pharmacology; D008297:Male; D018782:Maze Learning / Q000187:drug effects / Q000502:physiology; D015735:Mifepristone / Q000494:pharmacology; D009415:Nerve Net / Q000187:drug effects / Q000502:physiology*; D009812:Odorants; D011863:Radioimmunoassay / Q000379:methods; D051381:Rats; D020318:Rats, Long-Evans; D012769:Shock
D006727:Hormone Antagonists; D015735:Mifepristone; D003847:Deoxyglucose; D003345:Corticosterone