Neural mechanisms underlying target detection in a dragonfly centrifugal neuron

Abstract

SUMMARY Visual identification of targets is an important task for many animals searching for prey or conspecifics. Dragonflies utilize specialized optics in the dorsal acute zone, accompanied by higher-order visual neurons in the lobula complex, and descending neural pathways tuned to the motion of small targets. While recent studies describe the physiology of insect small target motion detector (STMD) neurons, little is known about the mechanisms that underlie their exquisite sensitivity to target motion. Lobula plate tangential cells (LPTCs), a group of neurons in dipteran flies selective for wide-field motion, have been shown to take input from local motion detectors consistent with the classic correlation model developed by Hassenstein and Reichardt in the 1950s. We have tested the hypothesis that similar mechanisms underlie the response of dragonfly STMDs. We show that an anatomically characterized centrifugal STMD neuron (CSTMD1) gives responses that depend strongly on target contrast, a clear prediction of the correlation model. Target stimuli are more complex in spatiotemporal terms than the sinusoidal grating patterns used to study LPTCs, so we used a correlation-based computer model to predict response tuning to velocity and width of moving targets. We show that increasing target width in the direction of travel causes a shift in response tuning to higher velocities, consistent with our model. Finally, we show how the morphology of CSTMD1 allows for impressive spatial interactions when more than one target is present in the visual field.

Local and Large-Range Inhibition in Feature Detection

“…In the present study, we obtained recordings from 137 neurons classified as STMDs on the basis of their highly selective response to small targets. Larger features or bars elicited weaker responses, although unlike STMD neurons recently reported from the hoverfly lobula complex Barnett et al, 2007), responses of the dragonfly neurons are rarely completely suppressed by elongated targets (Geurten et al, 2007).…”

“…1 E) (Geurten et al, 2007) and a large axon linking the two visual hemifields. The receptive field of CSTMD1 is located contralateral to the recording site (Geurten et al, 2007).…”

“…The unique unilateral receptive field and spike shape allowed us to attribute 20 recordings to the recently described CSTMD1 ( Fig. 1) (Geurten et al, 2007), permitting pooling of data across multiple recordings. CSTMD1 shows peak sensitivity to small (1-3°) moving targets and suppressed responses to stimuli Ͼ10°.…”

“…Higher order visual neurons with receptive fields in this eye region and sensitive to small moving targets are found in both the third optic ganglion of the brain, the lobula (O'Carroll, 1993), and the descending nerve cord (Olberg, 1981(Olberg, , 1986. These small-target motion detectors (STMDs), recently shown to be physiological analogs of mammalian hypercomplex (end-stopped) neurons (Nordström and O'Carroll, 2009) have exquisite size selectivity with peak responses to moving targets subtending as little as 1-3°of the visual field with responses suppressed by bars Ͼ10° (O'Carroll, 1993;Geurten et al, 2007). In the dragonfly, target-selective descending neurons (TSDNs) respond to the motion of small moving targets.…”

“…CSTMD1 is an efferent neuron with inputs in the lateral protocerebrum and a large receptive field contralateral to the recording site (Geurten et al, 2007). It has a large axon that links the two visual hemifields, permitting stable intracellular recordings and making this an ideal model for studying local and global mechanisms of target selectivity.…”