The Coding of Temperature in the Drosophila Brain

Thermosensation is an indispensable sensory modality. Here, we study temperature coding in Drosophila, and show that temperature is represented by a spatial map of activity in the brain. First, we identify TRP channels that function in the fly antenna to mediate the detection of cold stimuli. Next,...

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Published in:Cell Vol. 144; no. 4; pp. 614 - 624
Main Authors: Gallio, Marco, Ofstad, Tyler A., Macpherson, Lindsey J., Wang, Jing W., Zuker, Charles S.
Format: Journal Article
Language:English
Published: United States Elsevier Inc 18-02-2011
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Abstract Thermosensation is an indispensable sensory modality. Here, we study temperature coding in Drosophila, and show that temperature is represented by a spatial map of activity in the brain. First, we identify TRP channels that function in the fly antenna to mediate the detection of cold stimuli. Next, we identify the hot-sensing neurons and show that hot and cold antennal receptors project onto distinct, but adjacent glomeruli in the Proximal-Antennal-Protocerebrum (PAP) forming a thermotopic map in the brain. We use two-photon imaging to reveal the functional segregation of hot and cold responses in the PAP, and show that silencing the hot- or cold-sensing neurons produces animals with distinct and discrete deficits in their behavioral responses to thermal stimuli. Together, these results demonstrate that dedicated populations of cells orchestrate behavioral responses to different temperature stimuli, and reveal a labeled-line logic for the coding of temperature information in the brain. [Display omitted] ► The antenna houses the Drosophila HOT and COLD temperature-sensing neurons ► The hot and cold cells project to separate brain targets in the Protocerebrum (PAP) ► Two-photon calcium imaging reveals a spatial map of temperature in the PAP ► Functional studies show labeled lines for processing thermal signals in the fly brain
AbstractList Thermosensation is an indispensable sensory modality. Here, we study temperature coding in Drosophila, and show that temperature is represented by a spatial map of activity in the brain. First, we identify TRP channels that function in the fly antenna to mediate the detection of cold stimuli. Next, we identify the hot-sensing neurons and show that hot and cold antennal receptors project onto distinct, but adjacent glomeruli in the Proximal-Antennal-Protocerebrum (PAP) forming a thermotopic map in the brain. We use two-photon imaging to reveal the functional segregation of hot and cold responses in the PAP, and show that silencing the hot- or cold-sensing neurons produces animals with distinct and discrete deficits in their behavioral responses to thermal stimuli. Together, these results demonstrate that dedicated populations of cells orchestrate behavioral responses to different temperature stimuli, and reveal a labeled-line logic for the coding of temperature information in the brain.
Thermosensation is an indispensable sensory modality. Here, we study temperature coding in Drosophila, and show that temperature is represented by a spatial map of activity in the brain. First, we identify new TRP channels and demonstrate they function in the fly antenna to mediate the detection of cold stimuli. Next, we identify the hot-sensing neurons and show that hot and cold antennal receptors project onto distinct, but adjacent glomeruli in the Proximal-Antennal-Protocerebrum (PAP) forming a thermotopic map in the brain. We use two-photon imaging to reveal the functional segregation of hot and cold responses in the PAP, and show that silencing the hot- or cold-sensing neurons produces animals with distinct and discrete deficits in their behavioral responses to thermal stimuli. Together, these results demonstrate that dedicated populations of cells orchestrate behavioral responses to different temperature stimuli, and reveal a labeled-line logic for the coding of temperature information in the brain.
Thermosensation is an indispensable sensory modality. Here, we study temperature coding in Drosophila, and show that temperature is represented by a spatial map of activity in the brain. First, we identify TRP channels that function in the fly antenna to mediate the detection of cold stimuli. Next, we identify the hot-sensing neurons and show that hot and cold antennal receptors project onto distinct, but adjacent glomeruli in the Proximal-Antennal-Protocerebrum (PAP) forming a thermotopic map in the brain. We use two-photon imaging to reveal the functional segregation of hot and cold responses in the PAP, and show that silencing the hot- or cold-sensing neurons produces animals with distinct and discrete deficits in their behavioral responses to thermal stimuli. Together, these results demonstrate that dedicated populations of cells orchestrate behavioral responses to different temperature stimuli, and reveal a labeled-line logic for the coding of temperature information in the brain. [Display omitted] ► The antenna houses the Drosophila HOT and COLD temperature-sensing neurons ► The hot and cold cells project to separate brain targets in the Protocerebrum (PAP) ► Two-photon calcium imaging reveals a spatial map of temperature in the PAP ► Functional studies show labeled lines for processing thermal signals in the fly brain
Author Wang, Jing W.
Macpherson, Lindsey J.
Zuker, Charles S.
Ofstad, Tyler A.
Gallio, Marco
AuthorAffiliation 1 Departments of Neurobiology and Neurosciences, University of California at San Diego, La Jolla, California 92093-0649, USA
2 Departments of Biochemistry and Molecular Biophysics and of Neuroscience, Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA
AuthorAffiliation_xml – name: 2 Departments of Biochemistry and Molecular Biophysics and of Neuroscience, Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA
– name: 1 Departments of Neurobiology and Neurosciences, University of California at San Diego, La Jolla, California 92093-0649, USA
Author_xml – sequence: 1
  givenname: Marco
  surname: Gallio
  fullname: Gallio, Marco
  organization: Departments of Neurobiology and Neurosciences, University of California at San Diego, La Jolla, California 92093, USA
– sequence: 2
  givenname: Tyler A.
  surname: Ofstad
  fullname: Ofstad, Tyler A.
  organization: Departments of Neurobiology and Neurosciences, University of California at San Diego, La Jolla, California 92093, USA
– sequence: 3
  givenname: Lindsey J.
  surname: Macpherson
  fullname: Macpherson, Lindsey J.
  organization: Departments of Neurobiology and Neurosciences, University of California at San Diego, La Jolla, California 92093, USA
– sequence: 4
  givenname: Jing W.
  surname: Wang
  fullname: Wang, Jing W.
  organization: Departments of Neurobiology and Neurosciences, University of California at San Diego, La Jolla, California 92093, USA
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  surname: Zuker
  fullname: Zuker, Charles S.
  email: cz2195@columbia.edu
  organization: Departments of Neurobiology and Neurosciences, University of California at San Diego, La Jolla, California 92093, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/21335241$$D View this record in MEDLINE/PubMed
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  year: 2011
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Snippet Thermosensation is an indispensable sensory modality. Here, we study temperature coding in Drosophila, and show that temperature is represented by a spatial...
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SubjectTerms Animals
Antennae
Brain
Brain - physiology
Brain mapping
Coding
cold
Cold stimuli
Cold Temperature
Drosophila
Drosophila - physiology
Drosophila Proteins - metabolism
heat
Hot Temperature
image analysis
Neuroimaging
Neurons
receptors
Sensory Receptor Cells - physiology
temperature
Temperature effects
Thermal stimuli
Thermosensing
transient receptor potential proteins
TRPP Cation Channels - metabolism
Title The Coding of Temperature in the Drosophila Brain
URI https://dx.doi.org/10.1016/j.cell.2011.01.028
https://www.ncbi.nlm.nih.gov/pubmed/21335241
https://search.proquest.com/docview/1017987329
https://search.proquest.com/docview/853223539
https://pubmed.ncbi.nlm.nih.gov/PMC3336488
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