High beta rhythm amplitude in olfactory learning signs a well-consolidated and non-flexible behavioral state

International audienceBeta rhythm (15-30 Hz) is a major candidate underlying long-range communication in the brain. In olfactory tasks, beta activity is strongly modulated by learning but its condition of expression and the network(s) responsible for its generation are unclear. Here we analyzed the emergence of beta activity in local field potentials recorded from olfactory, sensorimotor and limbic structures of rats performing an olfactory task. Rats performed successively simple discrimination, rule transfer, memory recall tests and contingency reversal. Beta rhythm amplitude progressively increased over learning in most recorded areas. Beta amplitude reduced to baseline when new odors were introduced, but remained high during memory recall. Intra-session analysis showed that even expert rats required several trials to reach a good performance level, with beta rhythm amplitude increasing in parallel. Notably, at the beginning of the reversal task, beta amplitude remained high while performance was low and, in all tested animals, beta amplitude decreased before rats were able to learn the new contingencies. connectivity analysis showed that beta activity was highly coherent between all structures where it was expressed. Overall, our results suggest that beta rhythm is expressed in a highly coherent network when context learning-including both odors and reward-is consolidated and signals behavioral inflexibility. Beta rhythm has been suggested as a major candidate supporting long range information transfer through functional coupling of neurons across distant brain regions 1. In the sensorimotor cortex, it may reflect cortical idling 2,3. Engel and Fries (2010) suggested beta activity could be related to signaling the status quo 4 , i.e. the maintenance of the sensorimotor set during the next processing step. In the olfactory system, beta activity is a major rhythm 5. However, disparities in the literature have hindered attempts of a unifying hypothesis, either for the condition of its expression or for determining the network(s) involved in its generation. In anesthetized rats, beta expression is promoted by odorant stimulation with low vapor pressure molecules 6. In awake animals, however, it is expressed in the olfactory areas during passive exposure to aversive, highly volatile , or biologically significant odorants 7-10. Oscillations in the beta band are also modulated by learning and beta amplitude in the olfactory bulb (OB) was found to increase with improved performance in a Go/No-Go task 11. Conversely, in a two alternative choice (TAC) discrimination, OB local field potentials (LFP) were dominated by gamma (40-90 Hz) oscillations during fine odor discrimination 12. No modulation in the power of OB beta oscillations (15-28 Hz) was shown over learning although beta band activity defined a coherent network between OB and piriform cortex 13. It was later suggested such differences between studies could be explained by task demand, phase of training, and/or odor set discrepancies 14. Relative to the network involved in the generation/expression of beta activity, the only converging data is that beta expression in OB and piriform cortex is strongly impaired if the connection between OB and cortex is disrupted 15,16. Importantly, most studies using multisite recordings reported that, when expressed, beta oscillations appear across a large network. Rats expressed enhanced beta activity in the OB and both dorsal and ventral parts of the hippocampus during odor sampling in an odor discrimination task 17. In a conditioned odor aversion task