Defining age limits of the sensitive period for attachment learning in rat pups

Abstract

Enhanced odor preference learning and attenuated fear learning characterizes rat pups' attachment learning Sensitive Period for learning the maternal odor. This period terminates at 10 days old (PN10) with increasing endogenous levels of the stress hormone, corticosterone. Increasing Sensitive Period pups' corticosterone prematurely terminates the Sensitive Period, while decreasing corticosterone in older pups delays Sensitive Period termination. Here we extend these findings and define the age range corticosterone alters learning and question whether corticosterone permanently terminates the Sensitive Period. Pups were odor-0.5 mA shock conditioned with either corticosterone increased (PN5-6; 4 mg/kg vs. saline) or decreased (PN15-16; naturally by maternal presence or corticosterone synthesis blocker, Metyrapone). Finally, PN7-8 pups were conditioned with corticosterone and reconditioned without corticosterone to assess whether the Sensitive Period was permanently terminated. Results indicate developmental limits for corticosterone regulation of pup learning are PN6 through PN15. Furthermore, inducing precocious corticosterone induced fear learning was not permanent, since reconditioning without corticosterone enabled odor preference learning. Results suggest pups are protected from learning aversions to maternal odor until approaching weaning.

FIGURE 1

Pups were odor-0.5mA shock conditioned at either PN5 or PN6 with either a saline or CORT (4 mg/kg; i.p.) injection. Pups were then tested in a Y-maze the next day. While both PN5 and PN6 pups learned an odor preference, the CORT

FIGURE 2

Pups were odor-0.5mA shock conditioned at either PN15 or PN16 with either a saline injection or one of two methods to reduce pups’ shock-induced CORT release (maternal presence, Metyrapone (50 mg/kg, i.p.) injection). Pups were then tested in a Y-maze the next day. Although both PN15 and PN16 pups are capable of learning odor aversion, only PN15 pups are capable of learning odor preference with attenuated CORT

FIGURE 3

Pups were odor-0.5mA shock conditioned twice, first at PN7 with CORT or saline injection and then conditioned again at PN8 with a saline injection to determine if preference learning would return. The PN7 conditioning with CORT produced an odor aversion, although additional conditioning at PN8 permitted pups to learn an odor preference. *p <.05, error bars indicate SEM; N = 6 pups per group.

FIGURE 4

Defining pup’s sensitive period: A graphic illustration of rat pup avoidance learning development prior to weaning. Here, the traditionally defined Sensitive Period age range (PN0–PN10) is divided into early and late to delineate an age range when CORT can induce odor-shock odor aversions. This may occur naturally when the SHRP is prematurely ended through stressful early life rearing. After PN10 until PN15, pups are able to learn both preference and avoidance during fear conditioning depending on maternal presence suppression of endogenous CORT release. As pups approach weaning, only aversion learning is available to pups even with lowered CORT levels.