Experience-dependent critical period for synaptic plasticity in the rat olfactory amygdala

The amygdala is involved in processing and memory of emotional stimuli. The cortical regions of the amygdala are situated medially to the piriform cortex (PC) and are also considered part of the olfactory system, which may explain why scents can evoke strong emotional responses and trigger vivid memories. Similarly to the PC, the anterior cortical nucleus of the amygdala (ACo) is a three-layered structure receiving direct input from the main olfactory bulb (MOB) through the lateral olfactory tract (LOT), without a thalamic relay. While activity processing, plasticity and behavioral relevance of the PC have been extensively studied, evidence on the functional properties of the olfactory amygdala is scarce. ACo participates in the innate response to aversive stimuli and could be involved in olfactory emotional learning. Primary cortices of different sensory modalities display early periods in which afferent connections are particularly plastic, and this is crucial for network maturation. Here, we studied the plastic properties of LOT-ACo synapses during olfactory system maturation, by assessing long-term potentiation (LTP) induction during the first weeks of life.

We performed field recordings of LOT-ACo synaptic potentials in brain slices from rats of 6 to 35 postnatal days (P6-P35) to assess LTP induction by theta-burst stimulation. To investigate if the developmental regulation of plasticity can be altered by early sensory deprivation, we performed unilateral naris occlusion.

We found that LTP was significantly higher between P16-P25 (reaching ~30%) compared to earlier or later stages. Interestingly, LTP was missing around the end of the first postnatal month (P26-35). Furthermore, we demonstrated that LTP induction at one month of age was recovered in both hemispheres in rats that were subjected to unilateral sensory deprivation.

This result suggests the existence of a critical period for LTP induction in olfactory connections to the amygdala. Therefore, ACo may not only be involved in innate responses to biologically relevant odorants, but could also participate in early experience-dependent associative learning. Moreover, olfactory deprivation could extend the critical period for plasticity, making the system prone to undergo plastic changes at later developmental stages.