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The Journal of Neuroscience, June 21, 2006, 26(25):6737-6748; doi:10.1523/JNEUROSCI.0499-06.2006

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Development/Plasticity/Repair
Dual Circuitry for Odor–Shock Conditioning during Infancy: Corticosterone Switches between Fear and Attraction via Amygdala

Stephanie Moriceau,¹ Donald A. Wilson,¹ Seymour Levine,² and Regina M. Sullivan¹

¹Department of Zoology, University of Oklahoma, Norman, Oklahoma 73019, and ²Department of Psychiatry, University of California–Davis, Davis, California 95817

Correspondence should be addressed to Dr. Stephanie Moriceau, Department of Zoology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019. Email: smoriceau{at}ou.edu

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.

Key words: attachment; learning; corticosterone; stress; fear conditioning; olfaction; infant rat; sensitive period; olfactory bulb; piriform cortex; amygdala

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Received Feb. 2, 2006; revised April 11, 2006; accepted May 17, 2006.

Correspondence should be addressed to Dr. Stephanie Moriceau, Department of Zoology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019. Email: smoriceau{at}ou.edu

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