Neural correlates of behavior in the moth Manduca sexta in response to complex odors

Jeffrey A. Riffell, Hong Lei, John G. Hildebrand

Research output: Contribution to journalArticle

87 Citations (Scopus)

Abstract

With Manduca sexta as a model system, we analyzed how natural odor mixtures that are most effective in eliciting flight and foraging behaviors are encoded in the primary olfactory center in the brain, the antennal lobe. We used gas chromatography coupled with multiunit neural-ensemble recording to identify key odorants from flowers of two important nectar resources, the desert plants Datura wrightii and Agave palmeri, that elicited responses from individual antennal-lobe neurons. Neural-ensemble responses to the A. palmeri floral scent, comprising >60 odorants, could be reproduced by stimulation with a mixture of six of its constituents that had behavioral effectiveness equivalent to that of the complete scent. Likewise, a mixture of three floral volatiles from D. wrightii elicited normal flight and feeding behaviors. By recording responses of neural ensembles to mixtures of varying behavioral effectiveness, we analyzed the coding of behaviorally "meaningful" odors. We considered four possible ensemble-coding mechanisms - mean firing rate, mean instantaneous firing rate, pattern of synchronous ensemble firing, and total net synchrony of firing - and found that mean firing rate and the pattern of ensemble synchrony were best correlated with behavior (R = 41% and 43%, respectively). Stepwise regression analysis showed that net synchrony and mean instantaneous firing rate contributed little to the variation in the behavioral results. We conclude that a combination of mean-rate coding and synchrony of firing of antennal-lobe neurons underlies generalization among related, behaviorally effective floral mixtures while maintaining sufficient contrast for discrimination of distinct scents.

Original languageEnglish (US)
Pages (from-to)19219-19226
Number of pages8
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number46
DOIs
StatePublished - Nov 17 2009
Externally publishedYes

Fingerprint

Manduca
Moths
Agave
Datura
Plant Nectar
Neurons
Feeding Behavior
Gas Chromatography
Regression Analysis
Odorants
Brain

Keywords

  • Floral scent
  • Insect behavior
  • Neural codes
  • Neural synchrony
  • Olfaction

ASJC Scopus subject areas

  • General

Cite this

Neural correlates of behavior in the moth Manduca sexta in response to complex odors. / Riffell, Jeffrey A.; Lei, Hong; Hildebrand, John G.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 46, 17.11.2009, p. 19219-19226.

Research output: Contribution to journalArticle

@article{75165074f59d45aaa75d7c5285a39061,
title = "Neural correlates of behavior in the moth Manduca sexta in response to complex odors",
abstract = "With Manduca sexta as a model system, we analyzed how natural odor mixtures that are most effective in eliciting flight and foraging behaviors are encoded in the primary olfactory center in the brain, the antennal lobe. We used gas chromatography coupled with multiunit neural-ensemble recording to identify key odorants from flowers of two important nectar resources, the desert plants Datura wrightii and Agave palmeri, that elicited responses from individual antennal-lobe neurons. Neural-ensemble responses to the A. palmeri floral scent, comprising >60 odorants, could be reproduced by stimulation with a mixture of six of its constituents that had behavioral effectiveness equivalent to that of the complete scent. Likewise, a mixture of three floral volatiles from D. wrightii elicited normal flight and feeding behaviors. By recording responses of neural ensembles to mixtures of varying behavioral effectiveness, we analyzed the coding of behaviorally {"}meaningful{"} odors. We considered four possible ensemble-coding mechanisms - mean firing rate, mean instantaneous firing rate, pattern of synchronous ensemble firing, and total net synchrony of firing - and found that mean firing rate and the pattern of ensemble synchrony were best correlated with behavior (R = 41{\%} and 43{\%}, respectively). Stepwise regression analysis showed that net synchrony and mean instantaneous firing rate contributed little to the variation in the behavioral results. We conclude that a combination of mean-rate coding and synchrony of firing of antennal-lobe neurons underlies generalization among related, behaviorally effective floral mixtures while maintaining sufficient contrast for discrimination of distinct scents.",
keywords = "Floral scent, Insect behavior, Neural codes, Neural synchrony, Olfaction",
author = "Riffell, {Jeffrey A.} and Hong Lei and Hildebrand, {John G.}",
year = "2009",
month = "11",
day = "17",
doi = "10.1073/pnas.0910592106",
language = "English (US)",
volume = "106",
pages = "19219--19226",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "46",

}

TY - JOUR

T1 - Neural correlates of behavior in the moth Manduca sexta in response to complex odors

AU - Riffell, Jeffrey A.

AU - Lei, Hong

AU - Hildebrand, John G.

PY - 2009/11/17

Y1 - 2009/11/17

N2 - With Manduca sexta as a model system, we analyzed how natural odor mixtures that are most effective in eliciting flight and foraging behaviors are encoded in the primary olfactory center in the brain, the antennal lobe. We used gas chromatography coupled with multiunit neural-ensemble recording to identify key odorants from flowers of two important nectar resources, the desert plants Datura wrightii and Agave palmeri, that elicited responses from individual antennal-lobe neurons. Neural-ensemble responses to the A. palmeri floral scent, comprising >60 odorants, could be reproduced by stimulation with a mixture of six of its constituents that had behavioral effectiveness equivalent to that of the complete scent. Likewise, a mixture of three floral volatiles from D. wrightii elicited normal flight and feeding behaviors. By recording responses of neural ensembles to mixtures of varying behavioral effectiveness, we analyzed the coding of behaviorally "meaningful" odors. We considered four possible ensemble-coding mechanisms - mean firing rate, mean instantaneous firing rate, pattern of synchronous ensemble firing, and total net synchrony of firing - and found that mean firing rate and the pattern of ensemble synchrony were best correlated with behavior (R = 41% and 43%, respectively). Stepwise regression analysis showed that net synchrony and mean instantaneous firing rate contributed little to the variation in the behavioral results. We conclude that a combination of mean-rate coding and synchrony of firing of antennal-lobe neurons underlies generalization among related, behaviorally effective floral mixtures while maintaining sufficient contrast for discrimination of distinct scents.

AB - With Manduca sexta as a model system, we analyzed how natural odor mixtures that are most effective in eliciting flight and foraging behaviors are encoded in the primary olfactory center in the brain, the antennal lobe. We used gas chromatography coupled with multiunit neural-ensemble recording to identify key odorants from flowers of two important nectar resources, the desert plants Datura wrightii and Agave palmeri, that elicited responses from individual antennal-lobe neurons. Neural-ensemble responses to the A. palmeri floral scent, comprising >60 odorants, could be reproduced by stimulation with a mixture of six of its constituents that had behavioral effectiveness equivalent to that of the complete scent. Likewise, a mixture of three floral volatiles from D. wrightii elicited normal flight and feeding behaviors. By recording responses of neural ensembles to mixtures of varying behavioral effectiveness, we analyzed the coding of behaviorally "meaningful" odors. We considered four possible ensemble-coding mechanisms - mean firing rate, mean instantaneous firing rate, pattern of synchronous ensemble firing, and total net synchrony of firing - and found that mean firing rate and the pattern of ensemble synchrony were best correlated with behavior (R = 41% and 43%, respectively). Stepwise regression analysis showed that net synchrony and mean instantaneous firing rate contributed little to the variation in the behavioral results. We conclude that a combination of mean-rate coding and synchrony of firing of antennal-lobe neurons underlies generalization among related, behaviorally effective floral mixtures while maintaining sufficient contrast for discrimination of distinct scents.

KW - Floral scent

KW - Insect behavior

KW - Neural codes

KW - Neural synchrony

KW - Olfaction

UR - http://www.scopus.com/inward/record.url?scp=73349136809&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=73349136809&partnerID=8YFLogxK

U2 - 10.1073/pnas.0910592106

DO - 10.1073/pnas.0910592106

M3 - Article

VL - 106

SP - 19219

EP - 19226

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 46

ER -