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

Abstract

Mother-infant attachment is facilitated in altricial rodents through unique neural mechanisms that include impaired neonatal fear conditioning until the time that pups first begin to leave the nest (sensitive period). Here, we confirmed the developmental emergence of odor fear conditioning in neonatal rat pups, and examined synaptic plasticity of inputs to the basolateral amygdala in vitro. Coronal slices through the amygdala were obtained from sensitive (< 10 days) and post-sensitive (> 10, < 19 days) period pups. Field potentials were recorded in the basolateral amygdala in response to stimulation of either the external capsule (neocortical inputs) or fibers from the cortical nucleus of the amygdala (olfactory inputs). The effects of tetanic stimulation were examined in each pathway. In both pathways, tetanic stimulation induce significant long-term synaptic plasticity in post-sensitive period pups, but no significant plasticity in sensitive period pups incapable of learning odor aversions. GABA A receptor blockade in post-sensitive period slices reverts synaptic plasticity to sensitive period characteristics. The results suggest that sensitive period deficits in fear conditioning may be related to impaired amygdala synaptic plasticity and the immature state of GABAergic inhibition and/or it modulation in the neonatal amygdala.

Sensitive Periods in Affective Development: Nonlinear Maturation of Fear Learning

“…After P10, the odor-shock conditioning produces a conditioned odor aversion, reflecting the emergence of cued fear learning. This behavioral change coincides with the onset of learning-induced synaptic plasticity within the amygdala (Thompson et al, 2008). The timing of the functional maturation of the amygdala appears to be experience-dependent.…”

“…These changes appear to play a critical role in several of the qualitative changes in fear learning that occur during this stage. The switch from approach to avoidance responding to a conditioned stimulus that typically occurs at P10 in the rat is prevented by GABA A blockade (Sullivan et al, 2000;Thompson et al, 2008). Similarly, the rapid forgetting of fear learning early in development, referred to as infantile amnesia, is mediated by the GABA A receptor (Kim et al, 2006).…”

Postnatal development of the amygdala: A stereological study in rats

“…In cats, an increase in total dendritic length in the basal nucleus of the amygdala has been observed during the first postnatal month (Wakefield and Levine, 1985). Similarly, electrophysiological studies suggest major changes in intra-amygdala functional connectivity: Tetanic stimulation of the lateral nucleus does not produce long-term potentiation in the basal nucleus in amygdala slice preparations of P7-10 rat pups, whereas it does in P11-19 slices (Thompson et al, 2008). In addition, the amygdala is resistant to seizure induced by kindling stimulation in 10-and 14-day-old rats, but not in rats 21 days old and older (Gilbert and Cain, 1981;Terasawa and Timiras, 1968).…”

Attachment Figure's Regulation of Infant Brain and Behavior

“…The infant rodent amygdala is uniquely dependent upon stress hormones for engaging mechanisms for plasticity within the amygdala: the infant amygdala can be switched on and off simply based on the level of stress hormones with stress hormones being robustly controlled by the caregiver in early development (Barr et al, 2009;Moriceau, Wilson, Levine, & Sullivan, 2006;Shionoya et al, 2007;Thompson, Sullivan, & Wilson, 2008). Specifically, in rat pups, amygdala-dependent threat (fear) conditioning can be precociously induced by increasing systemic stress hormone corticosterone (analogous to cortisol in humans) by injecting pups, or through naturalistic means such as increasing pups' early life stress or by exposing pups to a mother releasing an alarm pheromone (Barr et al, 2009;Debiec & Sullivan, 2014;Moriceau et al, 2009).…”