Olfactory learning induces differential long-lasting changes in rat central olfactory pathways.

In the present work, we investigated lasting changes induced by olfactory learning at different levels of the olfactory pathways. For this, evoked field potentials induced by electrical stimulation of the olfactory bulb were recorded simultaneously in the anterior piriform cortex, the posterior piriform cortex, the lateral entorhinal cortex and the dentate gyrus. The amplitude of the evoked field potential's main component was measured in each site before, immediately after, and 20 days after completion of associative learning. Evoked field potential recordings were carried out under two experimental conditions in the same animals: awake and anesthetized. In the learning task, rats were trained to associate electrical stimulation of one olfactory bulb electrode with the delivery of sucrose (positive reward), and stimulation of a second olfactory bulb electrode with the delivery of quinine (negative reward). In this way, stimulation of the same olfactory bulb electrodes used for inducing field potentials served as a discriminative cue in the learning paradigm. The data showed that positively reinforced learning resulted in a lasting increase in evoked field potential amplitude restricted to posterior piriform cortex and lateral entorhinal cortex. In contrast, negatively reinforced learning was mainly accompanied by a decrease in evoked field potential amplitude in the dentate gyrus. Moreover, the expression of these learning-related changes occurred to be modulated by the animals arousal state. Indeed, the comparison between anesthetized versus awake animals showed that although globally similar, the changes were expressed earlier with respect to learning, under anesthesia than in the awake state. From these data we suggest that associative olfactory learning involves different neural circuits depending on the acquired value of the stimulus. Furthermore, they show the existence of a functional dissociation between anterior and posterior piriform cortex in mnesic processes, and stress the importance of the animal's arousal state on the expression of learning-induced plasticity.