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Effects of Mechanosensory Input on the Tracking of Pulsatile Odor Stimuli by Moth Antennal Lobe Neurons

Air turbulence ensures that in a natural environment insects tend to encounter odor stimuli in a pulsatile fashion. The frequency and duration of odor pulses varies with distance from the source, and hence successful mid-flight odor tracking requires resolution of spatiotemporal pulse dynamics. This...

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Autores principales: Tuckman, Harrison, Patel, Mainak, Lei, Hong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8529024/
https://www.ncbi.nlm.nih.gov/pubmed/34690678
http://dx.doi.org/10.3389/fnins.2021.739730
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author Tuckman, Harrison
Patel, Mainak
Lei, Hong
author_facet Tuckman, Harrison
Patel, Mainak
Lei, Hong
author_sort Tuckman, Harrison
collection PubMed
description Air turbulence ensures that in a natural environment insects tend to encounter odor stimuli in a pulsatile fashion. The frequency and duration of odor pulses varies with distance from the source, and hence successful mid-flight odor tracking requires resolution of spatiotemporal pulse dynamics. This requires both olfactory and mechanosensory input (from wind speed), a form of sensory integration observed within the antennal lobe (AL). In this work, we employ a model of the moth AL to study the effect of mechanosensory input on AL responses to pulsatile stimuli; in particular, we examine the ability of model neurons to: (1) encode the temporal length of a stimulus pulse; (2) resolve the temporal dynamics of a high frequency train of brief stimulus pulses. We find that AL glomeruli receiving olfactory input are adept at encoding the temporal length of a stimulus pulse but less effective at tracking the temporal dynamics of a pulse train, while glomeruli receiving mechanosensory input but little olfactory input can efficiently track the temporal dynamics of high frequency pulse delivery but poorly encode the duration of an individual pulse. Furthermore, we show that stronger intrinsic small-conductance calcium-dependent potassium (SK) currents tend to skew cells toward being better trackers of pulse frequency, while weaker SK currents tend to entail better encoding of the temporal length of individual pulses. We speculate a possible functional division of labor within the AL, wherein, for a particular odor, glomeruli receiving strong olfactory input exhibit prolonged spiking responses that facilitate detailed discrimination of odor features, while glomeruli receiving mechanosensory input (but little olfactory input) serve to resolve the temporal dynamics of brief, pulsatile odor encounters. Finally, we discuss how this hypothesis extends to explaining the functional significance of intraglomerular variability in observed phase II response patterns of AL neurons.
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spelling pubmed-85290242021-10-22 Effects of Mechanosensory Input on the Tracking of Pulsatile Odor Stimuli by Moth Antennal Lobe Neurons Tuckman, Harrison Patel, Mainak Lei, Hong Front Neurosci Neuroscience Air turbulence ensures that in a natural environment insects tend to encounter odor stimuli in a pulsatile fashion. The frequency and duration of odor pulses varies with distance from the source, and hence successful mid-flight odor tracking requires resolution of spatiotemporal pulse dynamics. This requires both olfactory and mechanosensory input (from wind speed), a form of sensory integration observed within the antennal lobe (AL). In this work, we employ a model of the moth AL to study the effect of mechanosensory input on AL responses to pulsatile stimuli; in particular, we examine the ability of model neurons to: (1) encode the temporal length of a stimulus pulse; (2) resolve the temporal dynamics of a high frequency train of brief stimulus pulses. We find that AL glomeruli receiving olfactory input are adept at encoding the temporal length of a stimulus pulse but less effective at tracking the temporal dynamics of a pulse train, while glomeruli receiving mechanosensory input but little olfactory input can efficiently track the temporal dynamics of high frequency pulse delivery but poorly encode the duration of an individual pulse. Furthermore, we show that stronger intrinsic small-conductance calcium-dependent potassium (SK) currents tend to skew cells toward being better trackers of pulse frequency, while weaker SK currents tend to entail better encoding of the temporal length of individual pulses. We speculate a possible functional division of labor within the AL, wherein, for a particular odor, glomeruli receiving strong olfactory input exhibit prolonged spiking responses that facilitate detailed discrimination of odor features, while glomeruli receiving mechanosensory input (but little olfactory input) serve to resolve the temporal dynamics of brief, pulsatile odor encounters. Finally, we discuss how this hypothesis extends to explaining the functional significance of intraglomerular variability in observed phase II response patterns of AL neurons. Frontiers Media S.A. 2021-10-07 /pmc/articles/PMC8529024/ /pubmed/34690678 http://dx.doi.org/10.3389/fnins.2021.739730 Text en Copyright © 2021 Tuckman, Patel and Lei. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Tuckman, Harrison
Patel, Mainak
Lei, Hong
Effects of Mechanosensory Input on the Tracking of Pulsatile Odor Stimuli by Moth Antennal Lobe Neurons
title Effects of Mechanosensory Input on the Tracking of Pulsatile Odor Stimuli by Moth Antennal Lobe Neurons
title_full Effects of Mechanosensory Input on the Tracking of Pulsatile Odor Stimuli by Moth Antennal Lobe Neurons
title_fullStr Effects of Mechanosensory Input on the Tracking of Pulsatile Odor Stimuli by Moth Antennal Lobe Neurons
title_full_unstemmed Effects of Mechanosensory Input on the Tracking of Pulsatile Odor Stimuli by Moth Antennal Lobe Neurons
title_short Effects of Mechanosensory Input on the Tracking of Pulsatile Odor Stimuli by Moth Antennal Lobe Neurons
title_sort effects of mechanosensory input on the tracking of pulsatile odor stimuli by moth antennal lobe neurons
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8529024/
https://www.ncbi.nlm.nih.gov/pubmed/34690678
http://dx.doi.org/10.3389/fnins.2021.739730
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