Review
Dynamic connectivity in the mitral cell–granule cell microcircuit

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Abstract

The interactions between excitatory mitral cells and inhibitory granule cells are critical for the regulation of olfactory bulb activity. Here we review anatomical and physiological data on the mitral cell–granule cell circuit and provide a quantitative estimate of how this connectivity varies as a function of distance between mitral cells. We also discuss the ways in which the functional connectivity can be altered rapidly during olfactory bulb activity.

Introduction

The synaptic interactions between mitral and granule cells are critical for the regulation of activity within and output from the olfactory bulb. The connections between these major cell types consist mostly of reciprocal dendrodendritic synapses. Several overlapping functions have been ascribed to these synapses: granule cell-mediated lateral inhibition could provide a “spatial” contrast mechanism that sharpens the tuning of mitral cell odorant receptive fields [1], [2], [3]. The reciprocal synapse is also implicated in the generation of intrinsic bulbar oscillations [4], [5], [6], [7] which could synchronize mitral cell firing [8], [9] and thus shape olfactory coding [10], [11]. These synapses also may store olfactory memory [12], [13].

Here we describe what is known about these unusual synapses and attempt to provide a rough, but quantitative picture of the anatomical connectivity between mitral and granule cells. Further, we discuss a variety of ways in which the anatomical connectivity between mitral and granule cells may be regulated dynamically by neuronal activity.

Section snippets

Mitral and tufted cells (MTCs)

The principal neurons of the olfactory bulb are known as the mitral and tufted cells (MTCs). These two cell types are both excitatory, using glutamate as their primary neurotransmitter, and number approximately 100,000 per bulb in the rat [14]. Mitral cells are found in a discreet layer (the mitral cell layer, MCL) located (in the mouse or rat) between 200 and 450 μm from the glomerular layer, whereas tufted cell bodies are located in the external plexiform layer (EPL) or even more superficially

Anatomical connectivity

As a first step towards quantifying the strength of lateral inhibition that can be exerted between any two MTCs or glomerular units (the collection of MTCs associated with one glomerulus), we now compute an estimate of their average dendrodendritic connectivity as a function of their distance. We use the known anatomical data, mostly from studies of rat (see Ref. [2] and Supplementary information). Here we only explain the main factors entering into this estimate and will publish a detailed

MTC dendritic excitability

Release from MTC dendrites requires substantial depolarization [22] and activation of high-threshold VDCCs [23]. Studies on the properties of MTC dendrites, using both dendritic recordings and imaging approaches, have begun to shed light on how the functional connectivity of MTCs and GCs may be shaped by their dendritic excitability. Primary dendrites of MTCs have high densities of sodium channels and action potentials (APs) propagate in these dendrites without attenuation [61], [62]. The

Dynamic connectivity

The anatomical and physiological properties of mitral and granule cells, in particular the fact that both release transmitter from their dendrites, suggest that the synaptic interactions between these two cell populations may conspire to generate a variable and highly dynamic pattern of functional connectivity—more so than in circuits that involve only axonal release. Such circuit-level dynamics may account for the rich and complicated patterns of odor-evoked mitral cell activity that have been

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