UC San Diego

In sensory areas of cortex, inhibitory neurons play a critical role in regulating the activity of principal cells in space and time. The diversity of intrinsic electrical properties and connectivity patterns among inhibitory cells suggests that different cell types contribute specific functions to the processing of sensory information by cortical circuits. In pyramidal cells of primary olfactory (piriform) cortex, odors evoke widespread and broadly-tuned inhibition, but the cells producing this inhibition are not known. Here, using acute slices of piriform cortex, we identify three inhibitory circuits that are recruited by activation of sensory afferents and act over distinct spatial and temporal domains. We find that physiologically realistic burst stimulation of mitral and tufted (M/T) cell axons results in early but transient dendritic inhibition progressing to somatic feedback inhibition in pyramidal cells of piriform cortex. Interneurons in layer 1a (L1a) receive highly convergent M/T cell input and govern feedforward inhibition onto the dendrites, but short-term synaptic depression decreases their influence as the burst progresses. Dendritic inhibition from L1a interneurons is branch-specific and locally blocks the calcium transients associated with back-propagating action potentials. The late-onset feedback inhibitory circuit is composed of layer 3 (L3) fast-spiking and low threshold-spiking cells that target pyramidal cell bodies and basal dendrites. L3 interneurons are highly interconnected with local pyramidal cells and we demonstrate that activation of pyramidal cells leads to recurrent inhibition that dominates excitation. Our results reveal the diversity of inhibitory circuits in olfactory cortex and suggest that separate classes of interneurons may have distinct functional roles regulating spike timing, odor tuning, and plasticity. This work defines a basic set of features by which inhibitory circuits can be identified in piriform cortex and demonstrates a diversity of functional roles played by distinct interneuron cell types. Our findings offer testable hypotheses regarding the influence of specific inhibitory circuits in olfactory information processing and odor representations in the piriform cortex