Olfactory learning-induced long-lasting enhancement of descending and ascending synaptic transmission to the piriform cortex

Learning of a particularly difficult olfactory-discrimination (OD) task results in acquisition of rule learning. This remarkable enhancement in learning capability is accompanied by long-term enhancement of synaptic connectivity between piriform cortex (PC) pyramidal neurons. Because successful performance in the OD task requires integration of information about the identity and also about the reward value of odors, it is likely that a higher-order brain area would also be involved in rule learning acquisition and maintenance. The anterior PC (APC) receives a strong ascending input from the olfactory bulb, carrying information regarding olfactory cues in the environment. It also receives substantial descending input from the orbitofrontal cortex (OFC), which is thought to play an important role in encoding the predictive value of odor stimuli. Using in vivo recordings of evoked field postsynaptic potentials, we characterized the physiological properties of projections to APC from the OFC and examined whether descending and ascending synaptic inputs to the piriform cortex are modified after OD learning. We show that enhanced learning capability is accompanied by long-term enhancement of synaptic transmission in both the descending and ascending inputs. Long-term synaptic enhancement is not accompanied by modifications in paired-pulse facilitation, indicating that such modifications are likely postsynaptic. Predisposition for long-term potentiation induction was affected by previous learning, and surprisingly also by previous exposure to the odors and training apparatus. These data suggest that enhanced connectivity between the APC and its input sources is required for OD rule learning.