Licking-induced synchrony in the taste-reward circuit improves cue discrimination during learning

Animals learn which foods to ingest and which to avoid. Despite many studies, the electrophysiological correlates underlying this behavior at the gustatory-reward circuit level remain poorly understood. For this reason, we measured the simultaneous electrical activity of neuronal ensembles in the orbitofrontal cortex, insular cortex, amygdala, and nucleus accumbens while rats licked for taste cues and learned to perform a taste discrimination go/no-go task. This study revealed that rhythmic licking entrains the activity in all these brain regions, suggesting that the animal's licking acts as an "internal clock signal" against which single spikes can be synchronized. That is, as animals learned a go/no-go task, there were increases in the number of licking coherent neurons as well as synchronous spiking between neuron pairs from different brain regions. Moreover, a subpopulation of gustatory cue-selective neurons that fired in synchrony with licking exhibited a greater ability to discriminate among tastants than nonsynchronized neurons. This effect was seen in all four recorded areas and increased markedly after learning, particularly after the cue was delivered and before the animals made a movement to obtain an appetitive or aversive tastant. Overall, these results show that, throughout a large segment of the taste-reward circuit, appetitive and aversive associative learning improves spike-timing precision, suggesting that proficiency in solving a taste discrimination go/no-go task requires licking-induced neural ensemble synchronous activity.