Activity-dependent lateral inhibition enables ensemble synchronization of odor-activated neurons in the olfactory bulb

Abstract

Information in the brain is represented by the activity of neuronal ensembles. These ensembles are adaptive and dynamic, formed and truncated based on the animal’s experience. One mechanism by which spatially distributed neurons form an ensemble is synchronizing their spiking activity in response to a sensory event. In the olfactory bulb, odor stimulation evokes rhythmic gamma activity in spatially distributed mitral and tufted cells (MTCs). This rhythmic activity is thought to enhance the relay of odor information to the downstream olfactory targets. However, how only the odor-activated MTCs are synchronized is unknown. Here, we demonstrate that light activating one set of MTCs can gamma-entrain the spiking activity of another set. This lateral synchronization was particularly effective when both MTCs fired at the gamma rhythm, facilitating the synchronization of only the odor-activated MTCs. Furthermore, we show that lateral synchronization did not depend on the distance between the MTCs and is mediated by Granule cells. In contrast, lateral inhibition between MTCs that reduced their firing rates was spatially restricted to adjacent MTCs and was not mediated by Granule cells. Our findings reveal a simple yet robust mechanism by which spatially distributed neurons entrain each other’s spiking activity to form an ensemble.