2017Journal of NeurophysiologyOpen access

Inhibitory circuits of the mammalian main olfactory bulb

Shawn D. Burton

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Abstract

Synaptic inhibition critically influences sensory processing throughout the mammalian brain, including the main olfactory bulb (MOB), the first station of sensory processing in the olfactory system. Decades of research across numerous laboratories have established a central role for granule cells (GCs), the most abundant GABAergic interneuron type in the MOB, in the precise regulation of principal mitral and tufted cell (M/TC) firing rates and synchrony through lateral and recurrent inhibitory mechanisms. In addition to GCs, however, the MOB contains a vast diversity of other GABAergic interneuron types, and recent findings suggest that, while fewer in number, these oft-ignored interneurons are just as important as GCs in shaping odor-evoked M/TC activity. Here I challenge the prevailing centrality of GCs. In this review, I first outline the specific properties of each GABAergic interneuron type in the rodent MOB, with particular emphasis placed on direct interneuron recordings and cell type-selective manipulations. On the basis of these properties, I then critically reevaluate the contribution of GCs vs. other interneuron types to the regulation of odor-evoked M/TC firing rates and synchrony via lateral, recurrent, and other inhibitory mechanisms. This analysis yields a novel model in which multiple interneuron types with distinct abundances, connectivity patterns, and physiologies complement one another to regulate M/TC activity and sensory processing.

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What this paper is about

Synaptic inhibition critically influences sensory processing throughout the mammalian brain, including the main olfactory bulb (MOB), the first station of sensory processing in the olfactory system. Decades of research across numerous laboratories have established a central role for granule cells (GCs), the most abundant GABAergic interneuron type in the MOB, in the precise regulation of principal mitral and tufted cell (M/TC) firing rates and synchrony through lateral and recurrent inhibitory mechanisms. In addition to GCs, however, the MOB contains a vast diversity of other GABAergic interneuron types, and recent findings suggest that, while fewer in number, these oft-ignored interneurons are just as important as GCs in shaping odor-evoked M/TC activity. Here I challenge the prevailing centrality of GCs. In this review, I first outline the specific properties of each GABAergic interneuron type in the rodent MOB, with particular emphasis placed on direct interneuron recordings and cell type-selective manipulations. On the basis of these properties, I then critically reevaluate the contribution of GCs vs. other interneuron types to the regulation of odor-evoked M/TC firing rates and synchrony via lateral, recurrent, and other inhibitory mechanisms. This analysis yields a novel model in which multiple interneuron types with distinct abundances, connectivity patterns, and physiologies complement one another to regulate M/TC activity and sensory processing.

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Available abstract

Synaptic inhibition critically influences sensory processing throughout the mammalian brain, including the main olfactory bulb (MOB), the first station of sensory processing in the olfactory system. Decades of research across numerous laboratories have established a central role for granule cells (GCs), the most abundant GABAergic interneuron type in the MOB, in the precise regulation of principal mitral and tufted cell (M/TC) firing rates and synchrony through lateral and recurrent inhibitory mechanisms. In addition to GCs, however, the MOB contains a vast diversity of other GABAergic interneuron types, and recent findings suggest that, while fewer in number, these oft-ignored interneurons are just as important as GCs in shaping odor-evoked M/TC activity. Here I challenge the prevailing centrality of GCs. In this review, I first outline the specific properties of each GABAergic interneuron type in the rodent MOB, with particular emphasis placed on direct interneuron recordings and cell type-selective manipulations. On the basis of these properties, I then critically reevaluate the contribution of GCs vs. other interneuron types to the regulation of odor-evoked M/TC firing rates and synchrony via lateral, recurrent, and other inhibitory mechanisms. This analysis yields a novel model in which multiple interneuron types with distinct abundances, connectivity patterns, and physiologies complement one another to regulate M/TC activity and sensory processing.

Key concepts: Interneuron, Olfactory bulb, Neuroscience, GABAergic, Inhibitory postsynaptic potential, Biology, Sensory processing, Sensory system

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