Object-Detecting Neurons in Drosophila

Abstract

SUMMARY Many animals rely on vision to detect objects such as conspecifics, predators, and prey. Hypercomplex cells found in feline cortex and small target motion detectors found in dragonfly and hoverfly optic lobes demonstrate robust tuning for small objects with weak or no response to larger objects or movement of the visual panorama [1–3]. However, the relationship between anatomical, molecular, and functional properties of object detection circuitry is not understood. Here, we characterize a specialized object detector in Drosophila, the lobula columnar neuron LC11 [4]. By imaging calcium dynamics with two-photon excitation microscopy we show that LC11 responds to the omni-directional movement of a small object darker than the background, with little or no responses to static flicker, vertically elongated bars, or panoramic gratings. LC11 dendrites innervate multiple layers of the lobula, and each dendrite spans enough columns to sample 75-degrees of visual space, yet the area that evokes calcium responses is only 20-degrees wide, and shows robust responses to a 2.2-degree object spanning less than half of one facet of the compound eye. The dendrites of neighboring LC11s encode object motion retinotopically, but the axon terminals fuse into a glomerular structure in the central brain where retinotopy is lost. Blocking inhibitory ionic currents abolishes small object sensitivity and facilitates responses to elongated bars and gratings. Our results reveal high acuity object motion detection in the Drosophila optic lobe.

Visual Input to the Drosophila Central Complex by Developmentally and Functionally Distinct Neuronal Populations

“…However, the topographical organization of TuBu s neuron terminals (Fig. 5) suggests that retinotopy is conserved and thus could serve spatial navigation, unlike other small-object visual projection neurons (VPNs) of the lobula and lobula plate where the retinotopy is apparently lost within the intermingled axon terminals of individual small-field columnar neurons [52,53]. …”

“…Calcium imaging was conducted as previously described [53]. Briefly, calcium-dependent fluorescent signals were detected using a two-photon excitation scanning microscope (3i, Boulder, CO) with Slidebook 6 software (3i, CO), at an image acquisition rate of 10 frames/sec.…”

Drosophila Spatiotemporally Integrates Visual Signals to Control Saccades

“…We posit that the object-tracking tracking system should 1) exhibit no directional selectivity (Figure S1A), 2) have narrow bilateral receptive fields offset by approximately ±45° (Figure 2A), 3) be sensitive to bar motion irrespective of wide-field motion (Figure 5), and 4) integrate position error (Figure 2E). Small-object sensitive neurons have recently been discovered in the lobula of Drosophila therefore the lobula may be a good candidate to implement tuning of visually-guided saccades during object fixation [45, 46]. In contrast, the wide-field system should respond weakly to bar motion (Figure 4A) and integrate wide-field motion velocity.…”

The Neuronal Basis of an Illusory Motion Percept Is Explained by Decorrelation of Parallel Motion Pathways

“…For instance, behavioral loom responses could preferentially combine local T5 motion signals across the four layers of the lobula plate without regard for T4 signals [43]. Small object tracking provides another example in which local single-edge-motion detectors could be individually exploited and combined into useful information about the visual world [87, 88]. Note that although certain stimuli did activate both T4 channels and both T5 channels in our experiments (Figures S2, S5), our analysis indicates that this effect lessens under natural conditions (Figure 5D).…”