Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit.

Inhibitory interneurons play critical roles in shaping the firing patterns of principal neurons in many brain systems. Despite difference in the anatomy or functions of neuronal circuits containing inhibition, two basic motifs repeatedly emerge: feed-forward and feedback. In the locust, it was propo...

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Main Authors: Tiffany Kee, Pavel Sanda, Nitin Gupta, Mark Stopfer, Maxim Bazhenov
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-10-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC4601731?pdf=render
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spelling doaj-44b8c9de0d344f50b33089b0095000692020-11-24T21:56:05ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582015-10-011110e100453110.1371/journal.pcbi.1004531Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit.Tiffany KeePavel SandaNitin GuptaMark StopferMaxim BazhenovInhibitory interneurons play critical roles in shaping the firing patterns of principal neurons in many brain systems. Despite difference in the anatomy or functions of neuronal circuits containing inhibition, two basic motifs repeatedly emerge: feed-forward and feedback. In the locust, it was proposed that a subset of lateral horn interneurons (LHNs), provide feed-forward inhibition onto Kenyon cells (KCs) to maintain their sparse firing--a property critical for olfactory learning and memory. But recently it was established that a single inhibitory cell, the giant GABAergic neuron (GGN), is the main and perhaps sole source of inhibition in the mushroom body, and that inhibition from this cell is mediated by a feedback (FB) loop including KCs and the GGN. To clarify basic differences in the effects of feedback vs. feed-forward inhibition in circuit dynamics we here use a model of the locust olfactory system. We found both inhibitory motifs were able to maintain sparse KCs responses and provide optimal odor discrimination. However, we further found that only FB inhibition could create a phase response consistent with data recorded in vivo. These findings describe general rules for feed-forward versus feedback inhibition and suggest GGN is potentially capable of providing the primary source of inhibition to the KCs. A better understanding of how inhibitory motifs impact post-synaptic neuronal activity could be used to reveal unknown inhibitory structures within biological networks.http://europepmc.org/articles/PMC4601731?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Tiffany Kee
Pavel Sanda
Nitin Gupta
Mark Stopfer
Maxim Bazhenov
spellingShingle Tiffany Kee
Pavel Sanda
Nitin Gupta
Mark Stopfer
Maxim Bazhenov
Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit.
PLoS Computational Biology
author_facet Tiffany Kee
Pavel Sanda
Nitin Gupta
Mark Stopfer
Maxim Bazhenov
author_sort Tiffany Kee
title Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit.
title_short Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit.
title_full Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit.
title_fullStr Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit.
title_full_unstemmed Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit.
title_sort feed-forward versus feedback inhibition in a basic olfactory circuit.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2015-10-01
description Inhibitory interneurons play critical roles in shaping the firing patterns of principal neurons in many brain systems. Despite difference in the anatomy or functions of neuronal circuits containing inhibition, two basic motifs repeatedly emerge: feed-forward and feedback. In the locust, it was proposed that a subset of lateral horn interneurons (LHNs), provide feed-forward inhibition onto Kenyon cells (KCs) to maintain their sparse firing--a property critical for olfactory learning and memory. But recently it was established that a single inhibitory cell, the giant GABAergic neuron (GGN), is the main and perhaps sole source of inhibition in the mushroom body, and that inhibition from this cell is mediated by a feedback (FB) loop including KCs and the GGN. To clarify basic differences in the effects of feedback vs. feed-forward inhibition in circuit dynamics we here use a model of the locust olfactory system. We found both inhibitory motifs were able to maintain sparse KCs responses and provide optimal odor discrimination. However, we further found that only FB inhibition could create a phase response consistent with data recorded in vivo. These findings describe general rules for feed-forward versus feedback inhibition and suggest GGN is potentially capable of providing the primary source of inhibition to the KCs. A better understanding of how inhibitory motifs impact post-synaptic neuronal activity could be used to reveal unknown inhibitory structures within biological networks.
url http://europepmc.org/articles/PMC4601731?pdf=render
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