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

Abstract

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.

Impact of neuronal heterogeneity on correlated colored noise-induced synchronization

“…Two properties of the olfactory bulb nevertheless suggest that even this moderate effect can significantly influence patterns of oscillatory synchrony in the olfactory system. First, the reciprocal dendrodendritic connectivity between mitral cells and granule cells enables activity-dependent regulation of granule cell recruitment (Arevian et al, 2008), which can lead to amplification of granule cell-mediated correlated noise-induced synchronization (Marella and Ermentrout, 2010). Second, mitral cells separated by up to ~2 mm can engage in lateral inhibitory interactions (Egger and Urban, 2006), thus multiplying the synchrony-enhancing effect of cellular heterogeneity across a potentially large fraction of the ~40,000 total mitral cells per mouse olfactory bulb (Benson et al, 1984).…”

“…In many networks, synchronization is achieved via direct coupling such as through gap junctions and chemical synapses. However, there are several systems (notably, the mammalian olfactory bulb) where the mode of coupling is less clear and neural synchrony is hypothesized to arise from partially correlated presynaptic inputs (Galán et al, 2006; Marella and Ermentrout, 2010). Indeed, in non-oscillatory networks of neurons, such correlated input is largely responsible for the output correlations of the neurons (de la Rocha et al, 2007).…”

Mitral cell spike synchrony modulated by dendrodendritic synapse location

“…Computational studies have described how the granule cell inhibitory network may be involved in mitral cell synchrony (Rall and Shepherd, 1968; Davison et al, 2003; Bathellier et al, 2006; Galán et al, 2006; Marella and Ermentrout, 2010; Giridhar et al, 2011). The underlying mechanism of mitral cell synchrony in these reports is the correlated signal from shared granule cells.…”

Correlated firing in tufted cells of mouse olfactory bulb

“…Given the high levels of tonic activity of the mitral/tufted – granule cell network in awake, behaving animals (Davison and Katz, 2007; Doucette and Restrepo, 2008; Kay and Laurent, 1999; Rinberg et al, 2006a), we propose that in the normal basal state of the olfactory bulb circuit, strong tonic inhibition from granule cells constrains spike initiation to the apical tuft, thereby maintaining high precision (millisecond) intraglomerular spike synchrony of output neurons by default. Strong tonic granule cell activation may also promote, by correlated asynchronous feedback, precise inter-glomerular spike synchrony in the basal state (Marella and Ermentrout, 2010). …”