Corticosterone Influences on Mammalian Neonatal Sensitive-Period Learning.

Abstract

Infant rats exhibit sensitive-period odor learning characterized by olfactory bulb neural changes and odor preference acquisitions critical for survival. This sensitive period is coincident with low endogenous corticosterone (CORT) levels and stress hyporesponsivity. The authors hypothesized that low corticosterone levels modulate sensitive-period learning. They assessed the effects of manipulating CORT levels by increasing and removing CORT during (Postnatal Day 8) and after (Postnatal Day 12) the sensitive period. Results show that (a) exogenous CORT prematurely ends sensitive-period odor-shock-induced preferences; (b) adrenalectomy developmentally extends the sensitive period as indicated by odor-shock-induced odor-preference learning in older pups, whereas CORT replacement can reinstate fear learning; and (c) CORT manipulation modulates olfactory bulb correlates of sensitive-period odor learning in a manner consistent with behavior.Sensitive periods for enhanced learning have been documented in a wide range of species. For example, language acquisition in humans is more easily learned prior to puberty, the ewe has a few hours postpartum when she may bond with her lamb, and imprinting in avian species occurs during the first few hours posthatching. However, sensitive periods can also involve suppression of other types of learning that could interfere with attachment and learning about the mother, such as fear conditioning, inhibitory conditioning, and passive avoidance

Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity

“…For example, corticosterone (CORT) modulates GABAergic inhibition and principal cell excitability in the adult amygdala (Duvarci and Pare, 2007) and other limbic regions (Verkuyl et al, 2005). Elevating CORT levels within the amygdala of sensitive period pups allows precocial emergence of fear conditioning (Moriceau and Sullivan, 2004a), while reducing CORT levels in post-sensitive period pups either by adrenalectomy or maternal presence (Wiedenmayer et al, 2003) reinstates the sensitive period blockade on fear conditioning Sullivan, 2004b, Moriceau andSullivan, 2006).…”

“…For rat pups, the temporal association of maternal odor with a variety of other maternally generated stimuli, such as grooming, warmth, or milk results in learned approach, nipple attachment and behavioral activation responses by the neonate on subsequent presentation of that odor (Galef and Sherry, 1973, Johanson and Hall, 1979, Johanson and Teicher, 1980, Brake, 1981, Pedersen et al, 1982, Alberts and May, 1984, Sullivan et al, 1986a, Sullivan et al, 1986b, Wilson and Sullivan, 1994. Importantly, the range of interactions with the mother includes painful stimuli, such as biting and being stepped upon, yet neonates fail to learn an aversion to odors paired with such painful stimulation and instead learn to prefer the odor (Haroutunian and Campbell, 1979, Sullivan et al, 1986a, Sullivan et al, 1986b, Camp and Rudy, 1988, Sullivan et al, 2000, Moriceau and Sullivan, 2004a, Roth and Sullivan, 2005. As pups mature and begin to explore the extra-nest environment around postnatal day (PN) 10 ( Bolles and Woods, 1964), more 'adult-like' fear and inhibitory learning emerges (Haroutunian and Campbell, 1979, Blozovski and Dumery, 1987, Camp and Rudy, 1988, Sullivan et al, 2000, Moriceau and Sullivan, 2004a, Roth and Sullivan, 2005).…”

“…Importantly, the range of interactions with the mother includes painful stimuli, such as biting and being stepped upon, yet neonates fail to learn an aversion to odors paired with such painful stimulation and instead learn to prefer the odor (Haroutunian and Campbell, 1979, Sullivan et al, 1986a, Sullivan et al, 1986b, Camp and Rudy, 1988, Sullivan et al, 2000, Moriceau and Sullivan, 2004a, Roth and Sullivan, 2005. As pups mature and begin to explore the extra-nest environment around postnatal day (PN) 10 ( Bolles and Woods, 1964), more 'adult-like' fear and inhibitory learning emerges (Haroutunian and Campbell, 1979, Blozovski and Dumery, 1987, Camp and Rudy, 1988, Sullivan et al, 2000, Moriceau and Sullivan, 2004a, Roth and Sullivan, 2005). …”

Ontogeny of odor-LiCl vs. odor-shock learning: Similar behaviors but divergent ages of functional amygdala emergence

“…In contrast to adult odor-LiCl learning, which relies on the amygdala (Touzani and Sclafani 2005), this early-life, odoraversion learning relies on the olfactory bulb until the pup approaches weaning age, when the amygdala is incorporated into the learning circuitry (Shionoya et al 2006). In contrast, if infant rats receive an odor paired with a moderately painful stimulus (0.5-mA foot or tail shock, or tail pinch) the amygdala appears to be incorporated into this learning circuitry around postnatal day Here we expand assessment of the developing pups' odoraversion learning circuit by including the anterior and posterior piriform cortex, which have previously been demonstrated to be important for both pup and adult odor learning (Litaudon et al 1997;Barkai and Saar 2001;Mouly et al 2001;Mouly and Gervais 2002;Tronel and Sara 2002;Moriceau and Sullivan 2004;Sevelinges et al 2004;Wilson et al 2004;Roth et al 2006). We also extend the assessment of the development of odor-aversion learning by directly comparing a range of odor-aversion learning paradigms and including different intensities of shock.…”

“…Here we expand assessment of the developing pups' odoraversion learning circuit by including the anterior and posterior piriform cortex, which have previously been demonstrated to be important for both pup and adult odor learning (Litaudon et al 1997;Barkai and Saar 2001;Mouly et al 2001;Mouly and Gervais 2002;Tronel and Sara 2002;Moriceau and Sullivan 2004;Sevelinges et al 2004;Wilson et al 2004;Roth et al 2006). We also extend the assessment of the development of odor-aversion learning by directly comparing a range of odor-aversion learning paradigms and including different intensities of shock.…”