Abstract
Growing evidence shows that top-down projections from excitatory neurons in piriform cortex selectively synapse onto local inhibitory granule cells in the main olfactory bulb, effectively gating their own inputs by controlling inhibition. An open question in olfaction is the role this feedback plays in shaping the dynamics of local circuits, and the resultant computational benefits it provides. Using rate models of neuronal firing in a network consisting of excitatory mitral and tufted cells, inhibitory granule cells and top-down piriform cortical neurons, we found that changes in the weight of feedback to inhibitory neurons generated diverse network dynamics and complex transitions between these dynamics. Changes in the weight of top-down feedback supported a number of computations, including both pattern separation and oscillatory synchrony. Additionally, the network could generate gamma oscillations though a mechanism we termed Top-down control of Inhibitory Neuron Gamma (TING). Collectively, these functions arose from a codimension-2 bifurcation in the dynamical system. Our results highlight a key role for this top-down feedback, gating inhibition to facilitate often diametrically different computations.
Highlights
Growing evidence suggests that top-down centrifugal feedback from higher cortical areas target inhibitory interneurons in primary sensory regions
To visualize the collective behaviors of M, G, and P populations to these different stimuli, we turned to a three dimensional dynamical system representation of the model where the time evolution of the firing rates was a trajectory in the phase space (r1, r2, r3) and the tangent vector defining the velocity of each point along a trajectory was given by the vector field f = f1, f2, f3 T of Equation (1)
Using a three-node model, which included top-down projections from piriform cortical cells onto inhibitory granule cells in the main olfactory bulb, we identified a network capable of complex dynamic behaviors, ranging from an attractor to stable oscillations across a range of frequencies and amplitudes
Summary
Growing evidence suggests that top-down centrifugal feedback from higher cortical areas target inhibitory interneurons in primary sensory regions. Axons from excitatory neurons in the piriform cortex (PCx) synapse onto the inhibitory granule cells in olfactory bulb (OB), whereby they can modulate the function of the mitral/tufted cells (M/T), the principal relays of olfactory information from the bulb to the brain (Shipley and Adamek, 1984; Boyd et al, 2012; Markopoulos et al, 2012; Oswald and Urban, 2012b; Padmanabhan et al, 2016, 2019) This circuit motif results in piriform cortical neurons receiving input from only excitatory M/T cells but exerting influence on the local circuit dynamics in the OB via inhibitory populations. How the local E-I network’s activity in the bulb is changed by centrifugal input, what these changes mean more broadly for neural dynamics in the early olfactory system, and the role of these dynamics play in neural computation remains an open question
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