Wide-field feedback neurons dynamically tune early visual processing.
An important strategy for efficient neural coding is to match the range of cellular responses to the distribution of relevant input signals. However, the structure and relevance of sensory signals depend on behavioral state. Here, we show that behavior modifies neural activity at the earliest stages of fly vision. We describe a class of wide-field neurons that provide feedback to the most peripheral layer of the Drosophila visual system, the lamina. Using in vivo patch-clamp electrophysiology, we found that lamina wide-field neurons respond to low-frequency luminance fluctuations. Recordings in flying flies revealed that the gain and frequency tuning of wide-field neurons change during flight, and that these effects are mimicked by the neuromodulator octopamine. Genetically silencing wide-field neurons increased behavioral responses to slow-motion stimuli. Together, these findings identify a cell type that is gated by behavior to enhance neural coding by subtracting low-frequency signals from the inputs to motion detection circuits.
HHMI/Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, VA 20147, USA.
John C
JC
Tuthill
HHMI/Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, VA 20147, USA.
Aljoscha
A
Nern
HHMI/Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, VA 20147, USA.
Gerald M
GM
Rubin
HHMI/Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, VA 20147, USA. Electronic address: reiserm@janelia.hhmi.org.
Michael B
MB
Reiser
D000316:Adrenergic alpha-Agonists / Q000494:pharmacology; D000779:Anesthetics, Local / Q000494:pharmacology; D000818:Animals; D030801:Animals, Genetically Modified; D001921:Brain / Q000166:cytology* / Q000502:physiology; D002795:Choline O-Acetyltransferase / Q000378:metabolism; D004330:Drosophila; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D056228:Feedback, Sensory / Q000187:drug effects / Q000502:physiology*; D005426:Flight, Animal / Q000502:physiology; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D008564:Membrane Potentials / Q000187:drug effects; D009039:Motion Perception / Q000187:drug effects / Q000502:physiology*; D009474:Neurons / Q000187:drug effects / Q000502:physiology*; D009655:Octopamine / Q000494:pharmacology; D010775:Photic Stimulation; D013779:Tetrodotoxin / Q000494:pharmacology; D014157:Transcription Factors / Q000235:genetics; D014795:Visual Pathways / Q000166:cytology / Q000502:physiology*
D000316:Adrenergic alpha-Agonists; D000779:Anesthetics, Local; D029721:Drosophila Proteins; C557617:GAL4 protein, Drosophila; D014157:Transcription Factors; D049452:Green Fluorescent Proteins; D009655:Octopamine; D013779:Tetrodotoxin; D002795:Choline O-Acetyltransferase