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Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit

Nature Neuroscience volume 8, pages 354–364 (2005)Cite this article

Abstract

Microcircuits composed of principal neuron and interneuron dendrites have an important role in shaping the representation of sensory information in the olfactory bulb. Here we establish the physiological features governing synaptic signaling in dendrodendritic microcircuits of olfactory bulb glomeruli. We show that dendritic γ-aminobutyric acid (GABA) release from periglomerular neurons mediates inhibition of principal tufted cells, retrograde inhibition of sensory input and lateral signaling onto neighboring periglomerular cells. We find that L-type dendritic Ca2+ spikes in periglomerular cells underlie dendrodendritic transmission by depolarizing periglomerular dendrites and activating P/Q type channels that trigger GABA release. Ca2+ spikes in periglomerular cells are evoked by powerful excitatory inputs from a single principal cell, and glutamate release from the dendrites of single principal neurons activates a large ensemble of periglomerular cells.

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Figure 1: Multiple types of GABAergic signaling in olfactory glomeruli.
Figure 2: Factors governing the time course of periglomerular signaling.
Figure 3: Ca2+ spikes mediated by dihydropyridine-sensitive channels are more effective triggers of periglomerular GABA release than fast Na+ spikes.
Figure 4: Ca2+ spikes generate more Ca2+ influx than action potentials in periglomerular dendrites.
Figure 5: Low voltage–activated dihydropyridine sensitive Ca2+ currents in periglomerular cells.
Figure 6: L-type Ca2+ channels are required for tufted cell–periglomerular cell (TC-PG) dendrodendritic inhibition but are not normally coupled to exocytosis.
Figure 7: Individual tufted cells (TCs) activate an ensemble of periglomerular (PG) cells.
Figure 8: Dendritic glutamate release from a tufted cell generates an all-or-none Ca2+ spike in synaptically coupled periglomerular neurons.

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Acknowledgements

We thank M. Scanziani, P. Sah and K. Franks for helpful discussions. G.J.M. received support from an NRSA predoctoral fellowship (NIDCD; DC005679). J.S.I. received support from a McKnight Scholar Award, Klingenstein Award, Burroughs-Wellcome Career Award and the NIH (RO1 DC04682).

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  1. Neuroscience Graduate Program and Department of Neuroscience, University of California, San Diego, La Jolla, 92093-0608, California, USA

    Gabe J Murphy, Daniel P Darcy & Jeffry S Isaacson

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Correspondence to Jeffry S Isaacson.

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Supplementary information

Supplementary Fig. 1

We quantified the impact of AP-evoked release from PG cells by measuring the probability that single APs evoked a response in postsynaptic neurons. (PDF 71 kb)

Supplementary Fig. 2

P/Q-type Ca2+ channels govern GABA release between periglomerular and tufted cells. (PDF 185 kb)

Supplementary Fig. 3

Kinetics of PG cell activation during DDI. (PDF 272 kb)

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Murphy, G., Darcy, D. & Isaacson, J. Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit. Nat Neurosci 8, 354–364 (2005). https://doi.org/10.1038/nn1403

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