Maternal presence serves as a switch between learning fear and attraction in infancy

Abstract

Odor-shock conditioning produces either olfactory preference or aversion in preweanling (12-15 days old) rats, depending on the context. In the mother's absence, odor-shock conditioning produces amygdala activation and learned odor avoidance. With maternal presence, this same conditioning yields an odor preference without amygdala activation. Maternal presence acts through modulation of pup corticosterone and corticosterone's regulation of amygdala activity. Over-riding maternal suppression of corticosterone through intra-amygdala corticosterone infusions permits fear conditioning and amygdala activation.

Figure 1

Pup learning from odor-shock conditioning (0.5-mA shock) changes over development and is influenced by maternal (anesthetized) presence. Behavior was examined using a Y-maze test, (a) 8-d-old rats learned to prefer an odor paired with a shock, with or without maternal presence, (b) When conditioned without maternal presence, 12- to 15-d-old pups subjected to paired odor-shock learned an odor aversion. Pups that were conditioned with maternal presence learned an odor preference. (c) Pups of weaning age (21 to 23 d old) learned odor avoidance with or without maternal presence. *P < 0.05. Error bars represent s.e.m.

Figure 2

Maternal presence activates a non-amygdala dependent odor-shock circuit and yields odor preference, (a) Olfactory bulb activity during odor-shock acquisition was assessed by relative ¹⁴C 2-deoxyglucose (¹⁴C 2-DG) uptake. Enhanced uptake was found in pups subjected to paired odor-shocks with maternal presence that expressed an odor preference, (b) Activity in the basolateral and lateral nuclei of the amygdala were enhanced during odor-shock presentation only without maternal presence, as assessed by relative ¹⁴C 2-DG uptake. Additional amygdala nuclei and a representative ¹⁴C 2-DG/Nissl-stained amygdala section are shown in Supplementary Figs. 1 and 2, respectively. (c) Reversibly silencing the amygdala with the GABA agonist muscimol disrupted the odor aversion learning in pups subjected to odor-shock pairings without maternal presence but had no effect on the pups subjected to odor-shock pairings with maternal presence. *P < 0.05. Error bars represent s.e.m.

Figure 3

Assessment of the association between corticosterone, learning and the amygdala, (a) Radioimmunoassay (RIA) corticosterone levels were low in pups receiving shock with maternal presence, but high in those receiving shock without maternal presence, (b) Pups subject to paired odor-shock with maternal presence were given systemic corticosterone 30 min before conditioning. These pups showed odor aversion learning, (c) Intra-amygdala corticosterone permitted these pups to learn an odor aversion. *P < 0.05. Error bars represent s.e.m.