Amplification of Asynchronous Inhibition-Mediated Synchronization by Feedback in Recurrent Networks

Synchronization of 30–80 Hz oscillatory activity of the principle neurons in the olfactory bulb (mitral cells) is believed to be important for odor discrimination. Previous theoretical studies of these fast rhythms in other brain areas have proposed that principle neuron synchrony can be mediated by short-latency, rapidly decaying inhibition. This phasic inhibition provides a narrow time window for the principle neurons to fire, thus promoting synchrony. However, in the olfactory bulb, the inhibitory granule cells produce long lasting, small amplitude, asynchronous and aperiodic inhibitory input and thus the narrow time window that is required to synchronize spiking does not exist. Instead, it has been suggested that correlated output of the granule cells could serve to synchronize uncoupled mitral cells through a mechanism called “stochastic synchronization”, wherein the synchronization arises through correlation of inputs to two neural oscillators. Almost all work on synchrony due to correlations presumes that the correlation is imposed and fixed. Building on theory and experiments that we and others have developed, we show that increased synchrony in the mitral cells could produce an increase in granule cell activity for those granule cells that share a synchronous group of mitral cells. Common granule cell input increases the input correlation to the mitral cells and hence their synchrony by providing a positive feedback loop in correlation. Thus we demonstrate the emergence and temporal evolution of input correlation in recurrent networks with feedback. We explore several theoretical models of this idea, ranging from spiking models to an analytically tractable model.Author Summary: Neurons in many parts of the brain fire spikes rhythmically and synchronously in many behaviorally and functionally relevant contexts. There are many mechanisms for producing oscillatory synchronization between populations of biological oscillators. One way to produce synchrony is that the population of oscillators receives common correlated input. In this paper, we study a population of oscillating neurons (mitral cells) that are not directly coupled to each other but receive broadband correlated input from a second population of neurons (granule cells). The granule cell population, in turn, receives inputs from the mitral cells; hence, the mitral and granule cells are reciprocally connected. Correlated input to the oscillating mitral cells produces tighter synchrony in the activity of the mitral cell population. We hypothesize that this increased mitral cell synchrony will evoke greater activity in specific groups of granule cells and that these specific granule cells, in turn, become the source of the correlated input to the mitral cells. That is, the synchronous input from the mitral cells increases the fraction of correlated feedback. Thus, we close the correlation loop. We show through analysis and simulations that this feedback mechanism can lead to the spontaneous appearance of highly synchronous activity within the mitral cells. We show that there is good experimental support for this mechanism in the circuitry of the olfactory bulb. We speculate that such mechanisms could also arise in other parts of the brain.