Fast-spiking interneuron detonation drives high-fidelity inhibition in the olfactory bulb

Inhibitory circuits in the mammalian olfactory bulb (OB) dynamically reformat olfactory information as it propagates from peripheral receptors to downstream cortex. To gain mechanistic insight into how specific OB interneuron types support this sensory processing, we examine unitary synaptic interactions between excitatory mitral and tufted cells (MTCs), the OB projection neurons, and a conserved population of anaxonic external plexiform layer interneurons (EPL-INs) using pair and quartet whole-cell recordings in acute mouse brain slices. Physiological, morphological, neurochemical, and synaptic analyses divide EPL-INs into distinct subtypes and reveal that parvalbumin-expressing fast-spiking EPL-INs (FSIs) perisomatically innervate MTCs with release-competent dendrites and synaptically detonate to mediate fast, short-latency recurrent and lateral inhibition. Sparse MTC synchronization supralinearly increases this high-fidelity inhibition, while sensory afferent activation combined with single-cell silencing reveals that individual FSIs account for a substantial fraction of total network-driven MTC lateral inhibition. OB output is thus powerfully shaped by detonation-driven high-fidelity perisomatic inhibition.

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Publication Details

Journal
PLoS Biology
Published
2024-08-26
DOI
https://doi.org/10.1371/journal.pbio.3002660
Citations
4
Primary Topic
Olfactory and Sensory Function Studies
Type
article
Field-Weighted Citation Impact
1.44

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article

Fast-spiking interneuron detonation drives high-fidelity inhibition in the olfactory bulb

Nathaniel N. Urban, Shawn D. Burton, Christina M. Malyshko
4 citations
PLoS Biology
Olfactory and Sensory Function Studies
1.44
article

Fast-spiking interneuron detonation drives high-fidelity inhibition in the olfactory bulb

Nathaniel N. Urban, Shawn D. Burton, Christina M. Malyshko
article en
4 citations

Abstract

Inhibitory circuits in the mammalian olfactory bulb (OB) dynamically reformat olfactory information as it propagates from peripheral receptors to downstream cortex. To gain mechanistic insight into how specific OB interneuron types support this sensory processing, we examine unitary synaptic interactions between excitatory mitral and tufted cells (MTCs), the OB projection neurons, and a conserved population of anaxonic external plexiform layer interneurons (EPL-INs) using pair and quartet whole-cell recordings in acute mouse brain slices. Physiological, morphological, neurochemical, and synaptic analyses divide EPL-INs into distinct subtypes and reveal that parvalbumin-expressing fast-spiking EPL-INs (FSIs) perisomatically innervate MTCs with release-competent dendrites and synaptically detonate to mediate fast, short-latency recurrent and lateral inhibition. Sparse MTC synchronization supralinearly increases this high-fidelity inhibition, while sensory afferent activation combined with single-cell silencing reveals that individual FSIs account for a substantial fraction of total network-driven MTC lateral inhibition. OB output is thus powerfully shaped by detonation-driven high-fidelity perisomatic inhibition.

PLoS BiologyVol. 22(8)
Lehigh University (US)
National Institute on Deafness and Other Communication Disorders
Openalex Percentile: Top 20%
Olfactory and Sensory Function Studies
1.44
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Fast-spiking interneuron detonation drives high-fidelity inhibition in the olfactory bulb — Nathaniel N. Urban, Shawn D. Burton, et al. · PLoS Biology (2024) | TGRS Research Map | TGRS