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

BRIEF COMMUNICATIONSMaternal presence serves as

a switch between learning fear

and attraction in infancy.com/natureneuroscience Nature Publishing Group Stephanie Moriceau & Regina M SullivanOdor-shock conditioning produces either olfactory preference

or aversion in preweanling (1215 days old) rats, depending on

the context. In the mothers absence, odor-shock conditioning

produces amygdala activation and learned odor avoidance.

With maternal presence, this same conditioning yields anodor preference without amygdala activation. Maternal

presence acts through modulation of pup corticosterone and

corticosterones regulation of amygdala activity. Over-riding

maternal suppression of corticosterone through intra-amygdala

corticosterone infusions permits fear conditioning and

amygdala activation.Here we show two circuits for odor-shock conditioning, with maternal

presence providing the switch by lowering pups corticosterone

levels. Because pups must learn the diet-dependent maternal odor

for interactions with the mother (such as nipple attachment and

approach), this system ensures that pups only learn to approach

maternal odor. The mothers ability to modify fear learning circuitry

may provide clues to abusive attachment and predisposition for

mental illness and altered emotional expression later in life13.

The validity of an animal model of abusive attachment is strengthened by the wide phylogenetic representation of abusive attachment,

which has been documented in chicks, infant dogs, rodents

and nonhuman primates4,5. Moreover, these data provide insight

into the timing and mechanisms of functional emergence of brain

areas during development.During early life when pups are confined to the nest (the sensitive

period), they exhibit potentiated preference learning and attenuated

aversion learning, characterized by odor preferences induced by conditioning with an odor and a 0.5-mA shock68. This paradoxical

learning does not reflect the pups inability to feel pain or threshold

differences9, but reflects the inability of odor-shock conditioning to

engage the amygdala8,1012. The sensitive period ends as the pups

ability to walk emerges and life outside the nest begins (at age 10 d),

with a rapid transition to independence by age 2123 d. In this

postsensitive period, preweanling rats are in a transitional period

from dependence to independence. At this stage, the pups need both

continued interactions with the mother as well as the engagement of

contingency-dependent learning for survival outside the nest. The

effects of maternal presence on odor-pain conditioning may ensure

that pups continue to only learn approach responses to her odors,

whereas in her absence they...