A Hard-Wired Glutamatergic Circuit Pools and Relays UV Signals to Mediate Spectral Preference in Drosophila

Thangavel Karuppudurai; Tzu Yang Lin; Chun Yuan Ting; Randall Pursley; Krishna V. Melnattur; Fengqiu Diao; Benjamin H. White; Lindsey J. Macpherson; Marco Gallio; Thomas Pohida; Chi Hon Lee

doi:10.1016/j.neuron.2013.12.010

A Hard-Wired Glutamatergic Circuit Pools and Relays UV Signals to Mediate Spectral Preference in Drosophila

Thangavel Karuppudurai, Tzu Yang Lin, Chun Yuan Ting, Randall Pursley, Krishna V. Melnattur, Fengqiu Diao, Benjamin H. White, Lindsey J. Macpherson, Marco Gallio, Thomas Pohida, Chi Hon Lee^*

^*Corresponding author for this work

Neurobiology

Research output: Contribution to journal › Article › peer-review

86 Scopus citations

Abstract

Many visual animals have innate preferences for particular wavelengths of light, which can be modified by learning. Drosophila's preference for UV over visible light requires UV-sensing R7 photoreceptors and specific wide-field amacrine neurons called Dm8. Here we identify three types of medulla projection neurons downstream of R7 and Dm8 and show that selectively inactivating one of them (Tm5c) abolishes UV preference. Using a modified GRASP method to probe synaptic connections at the single-cell level, we reveal that each Dm8 neuron forms multiple synaptic contacts with Tm5c in the center of Dm8's dendritic field but sparse connections in the periphery. By single-cell transcript profiling and RNAi-mediated knockdown, we determine that Tm5c uses the kainate receptor Clumsy to receive excitatory glutamate input from Dm8. We conclude that R7s→Dm8→Tm5c form a hard-wired glutamatergic circuit that mediates UV preference by pooling ~16 R7 signals for transfer to the lobula, a higher visual center.

Original language	English (US)
Pages (from-to)	603-615
Number of pages	13
Journal	Neuron
Volume	81
Issue number	3
DOIs	https://doi.org/10.1016/j.neuron.2013.12.010
State	Published - Feb 5 2014

Funding

We thank Shinya Takemura and Dmitri Chklovskii for communicating results prior to publication; Tzumin Lee, Kristin Scott, Stephan Sigrist, Aaron DiAntonio, Gerald Rubin, and Claude Desplan for providing critical reagents; and Mark Mayer and Alan Hinnebusch for helpful discussion. This work was supported by the Intramural Research Programs of the National Institutes of Health (NIH), Eunice Kennedy Shriver National Institute of Child Health and Human Development (grant Z01-HD008776 to C.-H.L), National Institute of Mental Health (project 1ZIA-MH-002800-07 to B.H.W.), and Center for Information Technology (to R.P. and T.P.). L.J.M. and M.G.’s research was supported by NIH grants (RC1-NS069014 and R01-NS076774) to Charles Zuker.

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2013.12.010

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title = "A Hard-Wired Glutamatergic Circuit Pools and Relays UV Signals to Mediate Spectral Preference in Drosophila",

abstract = "Many visual animals have innate preferences for particular wavelengths of light, which can be modified by learning. Drosophila's preference for UV over visible light requires UV-sensing R7 photoreceptors and specific wide-field amacrine neurons called Dm8. Here we identify three types of medulla projection neurons downstream of R7 and Dm8 and show that selectively inactivating one of them (Tm5c) abolishes UV preference. Using a modified GRASP method to probe synaptic connections at the single-cell level, we reveal that each Dm8 neuron forms multiple synaptic contacts with Tm5c in the center of Dm8's dendritic field but sparse connections in the periphery. By single-cell transcript profiling and RNAi-mediated knockdown, we determine that Tm5c uses the kainate receptor Clumsy to receive excitatory glutamate input from Dm8. We conclude that R7s→Dm8→Tm5c form a hard-wired glutamatergic circuit that mediates UV preference by pooling ~16 R7 signals for transfer to the lobula, a higher visual center.",

author = "Thangavel Karuppudurai and Lin, {Tzu Yang} and Ting, {Chun Yuan} and Randall Pursley and Melnattur, {Krishna V.} and Fengqiu Diao and White, {Benjamin H.} and Macpherson, {Lindsey J.} and Marco Gallio and Thomas Pohida and Lee, {Chi Hon}",

note = "Funding Information: We thank Shinya Takemura and Dmitri Chklovskii for communicating results prior to publication; Tzumin Lee, Kristin Scott, Stephan Sigrist, Aaron DiAntonio, Gerald Rubin, and Claude Desplan for providing critical reagents; and Mark Mayer and Alan Hinnebusch for helpful discussion. This work was supported by the Intramural Research Programs of the National Institutes of Health (NIH), Eunice Kennedy Shriver National Institute of Child Health and Human Development (grant Z01-HD008776 to C.-H.L), National Institute of Mental Health (project 1ZIA-MH-002800-07 to B.H.W.), and Center for Information Technology (to R.P. and T.P.). L.J.M. and M.G.{\textquoteright}s research was supported by NIH grants (RC1-NS069014 and R01-NS076774) to Charles Zuker. ",

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doi = "10.1016/j.neuron.2013.12.010",

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AU - Karuppudurai, Thangavel

AU - Lin, Tzu Yang

AU - Ting, Chun Yuan

AU - Pursley, Randall

AU - Melnattur, Krishna V.

AU - Diao, Fengqiu

AU - White, Benjamin H.

AU - Macpherson, Lindsey J.

AU - Gallio, Marco

AU - Pohida, Thomas

AU - Lee, Chi Hon

N1 - Funding Information: We thank Shinya Takemura and Dmitri Chklovskii for communicating results prior to publication; Tzumin Lee, Kristin Scott, Stephan Sigrist, Aaron DiAntonio, Gerald Rubin, and Claude Desplan for providing critical reagents; and Mark Mayer and Alan Hinnebusch for helpful discussion. This work was supported by the Intramural Research Programs of the National Institutes of Health (NIH), Eunice Kennedy Shriver National Institute of Child Health and Human Development (grant Z01-HD008776 to C.-H.L), National Institute of Mental Health (project 1ZIA-MH-002800-07 to B.H.W.), and Center for Information Technology (to R.P. and T.P.). L.J.M. and M.G.’s research was supported by NIH grants (RC1-NS069014 and R01-NS076774) to Charles Zuker.

PY - 2014/2/5

Y1 - 2014/2/5

N2 - Many visual animals have innate preferences for particular wavelengths of light, which can be modified by learning. Drosophila's preference for UV over visible light requires UV-sensing R7 photoreceptors and specific wide-field amacrine neurons called Dm8. Here we identify three types of medulla projection neurons downstream of R7 and Dm8 and show that selectively inactivating one of them (Tm5c) abolishes UV preference. Using a modified GRASP method to probe synaptic connections at the single-cell level, we reveal that each Dm8 neuron forms multiple synaptic contacts with Tm5c in the center of Dm8's dendritic field but sparse connections in the periphery. By single-cell transcript profiling and RNAi-mediated knockdown, we determine that Tm5c uses the kainate receptor Clumsy to receive excitatory glutamate input from Dm8. We conclude that R7s→Dm8→Tm5c form a hard-wired glutamatergic circuit that mediates UV preference by pooling ~16 R7 signals for transfer to the lobula, a higher visual center.

AB - Many visual animals have innate preferences for particular wavelengths of light, which can be modified by learning. Drosophila's preference for UV over visible light requires UV-sensing R7 photoreceptors and specific wide-field amacrine neurons called Dm8. Here we identify three types of medulla projection neurons downstream of R7 and Dm8 and show that selectively inactivating one of them (Tm5c) abolishes UV preference. Using a modified GRASP method to probe synaptic connections at the single-cell level, we reveal that each Dm8 neuron forms multiple synaptic contacts with Tm5c in the center of Dm8's dendritic field but sparse connections in the periphery. By single-cell transcript profiling and RNAi-mediated knockdown, we determine that Tm5c uses the kainate receptor Clumsy to receive excitatory glutamate input from Dm8. We conclude that R7s→Dm8→Tm5c form a hard-wired glutamatergic circuit that mediates UV preference by pooling ~16 R7 signals for transfer to the lobula, a higher visual center.

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DO - 10.1016/j.neuron.2013.12.010

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JO - Neuron

JF - Neuron

IS - 3

ER -

A Hard-Wired Glutamatergic Circuit Pools and Relays UV Signals to Mediate Spectral Preference in Drosophila

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