Serotonin modulates olfactory processing in the antennal lobe of drosophila

Andrew M. Dacks, David S. Green, Cory M. Root, Alan J Nighorn, Jing W. Wang

Research output: Contribution to journalArticle

60 Citations (Scopus)

Abstract

Sensory systems must be able to extract features of environmental cues within the context of the different physiological states of the organism and often temper their activity in a state-dependent manner via the process of neuromodulation. We examined the effects of the neuromodulator serotonin on a well-characterized sensory circuit, the antennal lobe of Drosophila melanogaster, using two-photon microscopy and the genetically expressed calcium indicator, G-CaMP. Serotonin enhances sensitivity of the antennal lobe output projection neurons in an odor-specific manner. For odorants that sparsely activate the antennal lobe, serotonin enhances projection neuron responses and causes an offset of the projection neuron tuning curve, most likely by increasing projection neuron sensitivity. However, for an odorant that evokes a broad activation pattern, serotonin enhances projection neuron responses in some, but not all, glomeruli. Further, serotonin enhances the responses of inhibitory local interneurons, resulting in a reduction of neurotransmitter release from the olfactory sensory neurons via GABAB receptor-dependent presynaptic inhibition, which may be a mechanism underlying the odorant-specific modulation of projection neuron responses. Our data suggest that the complexity of serotonin modulation in the antennal lobe accommodates coding stability in a glomerular pattern and flexible projection neuron sensitivity under different physiological conditions.

Original languageEnglish (US)
Pages (from-to)366-377
Number of pages12
JournalJournal of Neurogenetics
Volume23
Issue number4
DOIs
StatePublished - 2009

Fingerprint

Drosophila
Serotonin
Neurons
Neurotransmitter Agents
Olfactory Receptor Neurons
Presynaptic Receptors
Interneurons
Drosophila melanogaster
Photons
Cues
Microscopy
Calcium
Odorants

Keywords

  • Antennal lobes
  • Neuromodulation
  • Olfaction
  • Serotonin

ASJC Scopus subject areas

  • Cellular and Molecular Neuroscience
  • Genetics

Cite this

Serotonin modulates olfactory processing in the antennal lobe of drosophila. / Dacks, Andrew M.; Green, David S.; Root, Cory M.; Nighorn, Alan J; Wang, Jing W.

In: Journal of Neurogenetics, Vol. 23, No. 4, 2009, p. 366-377.

Research output: Contribution to journalArticle

Dacks, Andrew M. ; Green, David S. ; Root, Cory M. ; Nighorn, Alan J ; Wang, Jing W. / Serotonin modulates olfactory processing in the antennal lobe of drosophila. In: Journal of Neurogenetics. 2009 ; Vol. 23, No. 4. pp. 366-377.
@article{2da4f5632091428880dd8e2bff88999f,
title = "Serotonin modulates olfactory processing in the antennal lobe of drosophila",
abstract = "Sensory systems must be able to extract features of environmental cues within the context of the different physiological states of the organism and often temper their activity in a state-dependent manner via the process of neuromodulation. We examined the effects of the neuromodulator serotonin on a well-characterized sensory circuit, the antennal lobe of Drosophila melanogaster, using two-photon microscopy and the genetically expressed calcium indicator, G-CaMP. Serotonin enhances sensitivity of the antennal lobe output projection neurons in an odor-specific manner. For odorants that sparsely activate the antennal lobe, serotonin enhances projection neuron responses and causes an offset of the projection neuron tuning curve, most likely by increasing projection neuron sensitivity. However, for an odorant that evokes a broad activation pattern, serotonin enhances projection neuron responses in some, but not all, glomeruli. Further, serotonin enhances the responses of inhibitory local interneurons, resulting in a reduction of neurotransmitter release from the olfactory sensory neurons via GABAB receptor-dependent presynaptic inhibition, which may be a mechanism underlying the odorant-specific modulation of projection neuron responses. Our data suggest that the complexity of serotonin modulation in the antennal lobe accommodates coding stability in a glomerular pattern and flexible projection neuron sensitivity under different physiological conditions.",
keywords = "Antennal lobes, Neuromodulation, Olfaction, Serotonin",
author = "Dacks, {Andrew M.} and Green, {David S.} and Root, {Cory M.} and Nighorn, {Alan J} and Wang, {Jing W.}",
year = "2009",
doi = "10.3109/01677060903085722",
language = "English (US)",
volume = "23",
pages = "366--377",
journal = "Journal of Neurogenetics",
issn = "0167-7063",
publisher = "Informa Healthcare",
number = "4",

}

TY - JOUR

T1 - Serotonin modulates olfactory processing in the antennal lobe of drosophila

AU - Dacks, Andrew M.

AU - Green, David S.

AU - Root, Cory M.

AU - Nighorn, Alan J

AU - Wang, Jing W.

PY - 2009

Y1 - 2009

N2 - Sensory systems must be able to extract features of environmental cues within the context of the different physiological states of the organism and often temper their activity in a state-dependent manner via the process of neuromodulation. We examined the effects of the neuromodulator serotonin on a well-characterized sensory circuit, the antennal lobe of Drosophila melanogaster, using two-photon microscopy and the genetically expressed calcium indicator, G-CaMP. Serotonin enhances sensitivity of the antennal lobe output projection neurons in an odor-specific manner. For odorants that sparsely activate the antennal lobe, serotonin enhances projection neuron responses and causes an offset of the projection neuron tuning curve, most likely by increasing projection neuron sensitivity. However, for an odorant that evokes a broad activation pattern, serotonin enhances projection neuron responses in some, but not all, glomeruli. Further, serotonin enhances the responses of inhibitory local interneurons, resulting in a reduction of neurotransmitter release from the olfactory sensory neurons via GABAB receptor-dependent presynaptic inhibition, which may be a mechanism underlying the odorant-specific modulation of projection neuron responses. Our data suggest that the complexity of serotonin modulation in the antennal lobe accommodates coding stability in a glomerular pattern and flexible projection neuron sensitivity under different physiological conditions.

AB - Sensory systems must be able to extract features of environmental cues within the context of the different physiological states of the organism and often temper their activity in a state-dependent manner via the process of neuromodulation. We examined the effects of the neuromodulator serotonin on a well-characterized sensory circuit, the antennal lobe of Drosophila melanogaster, using two-photon microscopy and the genetically expressed calcium indicator, G-CaMP. Serotonin enhances sensitivity of the antennal lobe output projection neurons in an odor-specific manner. For odorants that sparsely activate the antennal lobe, serotonin enhances projection neuron responses and causes an offset of the projection neuron tuning curve, most likely by increasing projection neuron sensitivity. However, for an odorant that evokes a broad activation pattern, serotonin enhances projection neuron responses in some, but not all, glomeruli. Further, serotonin enhances the responses of inhibitory local interneurons, resulting in a reduction of neurotransmitter release from the olfactory sensory neurons via GABAB receptor-dependent presynaptic inhibition, which may be a mechanism underlying the odorant-specific modulation of projection neuron responses. Our data suggest that the complexity of serotonin modulation in the antennal lobe accommodates coding stability in a glomerular pattern and flexible projection neuron sensitivity under different physiological conditions.

KW - Antennal lobes

KW - Neuromodulation

KW - Olfaction

KW - Serotonin

UR - http://www.scopus.com/inward/record.url?scp=70349476754&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=70349476754&partnerID=8YFLogxK

U2 - 10.3109/01677060903085722

DO - 10.3109/01677060903085722

M3 - Article

C2 - 19863268

AN - SCOPUS:70349476754

VL - 23

SP - 366

EP - 377

JO - Journal of Neurogenetics

JF - Journal of Neurogenetics

SN - 0167-7063

IS - 4

ER -