Abstract
Identified neuron classes in vertebrate cortical [1-4] and subcortical [5-8] areas and invertebrate peripheral [9-11] and central [12-14] brain neuropils encode specific visual features of a panorama. How downstream neurons integrate these features to control vital behaviors, like escape, is unclear [15]. In Drosophila, the timing of a single spike in the giant fiber (GF) descending neuron [16-18] determines whether a fly uses a short or long takeoff when escaping a looming predator [13]. We previously proposed that GF spike timing results from summation of two visual features whose detection is highly conserved across animals [19]: an object's subtended angular size and its angular velocity [5-8, 11, 20, 21]. We attributed velocity encoding to input from lobula columnar type 4 (LC4) visual projection neurons, but the size-encodingsource remained unknown. Here, we show that lobula plate/lobula columnar, type 2 (LPLC2) visual projection neurons anatomically specialized to detect looming [22] provide the entire GF size component. We find LPLC2 neurons to be necessary for GF-mediated escape and show that LPLC2 and LC4 synapse directly onto the GF via reconstruction in a fly brain electron microscopy (EM) volume [23]. LPLC2 silencing eliminates the size component of the GF looming response in patch-clamp recordings, leaving only the velocity component. A model summing a linear function of angular velocity (provided by LC4) and a Gaussian function of angular size (provided by LPLC2) replicates GF looming response dynamics and predicts the peak response time. We thus present an identified circuit in which information from looming feature-detecting neurons is combined by a common post-synaptic target to determine behavioral output.
Highlights
We encountered synapses from LPLC2 directly onto lobula columnar type 4 (LC4). It was not possible from our traced data to provide an accurate estimate of the numeric strength of the LPLC2 to LC4 connection, the relatively large number of synapses we identified serendipitously (>175) suggests that LPLC2 are a strong input to LC4
Silencing LPLC2 significantly reduced excitatory giant fiber (GF) responses to looming (Figure 2D) across all looming r/v values (Figure 2E), but it did not alter either the mean tonic hyperpolarization (Figure 2F) or off-transient peak (Figure 2G). These results suggest that LPLC2 contribute a large portion of the excitatory GF looming response, but they do not contribute to the inhibitory components
We previously showed that the tonic hyperpolarization does not depend on LC4 because the size tuning of its amplitude in response to static disks is unchanged between control and LC4-silenced conditions [19]
Summary
Ache et al show that the Drosophila giant fiber descending neuron integrates synaptic input from LPLC2 and LC4 visual feature-detecting neurons to drive escape from approaching objects, such as an attacking predator. LPLC2 input to the giant fiber encodes the angular size of an approaching object, whereas LC4 input directly encodes looming speed. Highlights d LPLC2 and LC4 are the primary direct visual inputs to the giant fiber (GF). D The GF sums LPLC2 and LC4 input to drive escape from looming d LPLC2-GF input encodes looming size, whereas LC4-GF input encodes looming speed d A model summing looming size and speed optical variables reproduces GF responses. 2019, Current Biology 29, 1073–1081 March 18, 2019 a 2019 The Authors.
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