Linear Summation Underlies Direction Selectivity in Drosophila

While linear mechanisms lay the foundations of feature selectivity in many brain areas, direction selectivity in the elementary motion detector (EMD) of the fly has become a paradigm of nonlinear neuronal computation. We have bridged this divide by demonstrating that linear spatial summation can gen...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2018-08, Vol.99 (4), p.680-688.e4
Main Authors: Wienecke, Carl F.R., Leong, Jonathan C.S., Clandinin, Thomas R.
Format: Article
Language:English
Subjects:
Algorithms
Animals
Calcium
Calcium channels (voltage-gated)
direction selectivity
Drosophila
Experiments
feature selectivity
Genetic transformation
Insects
linear filtering
Linear Models
Microscopy, Fluorescence, Multiphoton - methods
Motion Perception - physiology
motion processing
neural computation
Neuroimaging
Neurons
Photic Stimulation - methods
sensory processing
Studies
two-photon imaging
Vertebrates
vision
Visual cortex
Visual Cortex - chemistry
Visual Cortex - physiology
Visual Pathways - chemistry
Visual Pathways - physiology
voltage imaging
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Summary:While linear mechanisms lay the foundations of feature selectivity in many brain areas, direction selectivity in the elementary motion detector (EMD) of the fly has become a paradigm of nonlinear neuronal computation. We have bridged this divide by demonstrating that linear spatial summation can generate direction selectivity in the fruit fly Drosophila. Using linear systems analysis and two-photon imaging of a genetically encoded voltage indicator, we measure the emergence of direction-selective (DS) voltage signals in the Drosophila OFF pathway. Our study is a direct, quantitative investigation of the algorithm underlying directional signals, with the striking finding that linear spatial summation is sufficient for the emergence of direction selectivity. A linear stage of the fly EMD strongly resembles similar computations in vertebrate visual cortex, demands a reappraisal of the role of upstream nonlinearities, and implicates the voltage-to-calcium transformation in the refinement of feature selectivity in this system. [Display omitted] •Voltage signals in T5 are direction selective•Direction selectivity in Drosophila OFF pathway emerges from linear input summation•Flies share a simple motion-processing algorithm with vertebrates Direction-selective responses to visual motion in the OFF pathway of Drosophila emerge from simple linear input summation.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2018.07.005