Multisensory control of navigation in the fruit fly

Abstract

Spatial navigation is influenced by cues from nearly every sensory modality and thus provides an excellent model for understanding how different sensory streams are integrated to drive behavior. Here we review recent work on multisensory control of navigation in the model organism Drosophila melanogaster, which allows for detailed circuit dissection. We identify four modes of integration that have been described in the literature-suppression, gating, summation, and association-and describe regions of the larval and adult brain that have been implicated in sensory integration. Finally we discuss what circuit architectures might support these different forms of integration. We argue that Drosophila is an excellent model to discover these circuit and biophysical motifs.

Figure 1.. Modes of multisensory integration during navigation.

(A) Suppression occurs when two cues drive mutually exclusive behavioral states. A hungry fly will track odor in the absence of other cues. Activation of taste receptors reduces or halts locomotion, although odor is still present. Adapted from Sayin et al., 2019. (B) Gating occurs when one cue modifies a fly’s response to a second cue. Flies orient downwind in the absence of odor. Addition of odor (orange) induces upwind orientation. Adapted from Alvarez-Salvado et al., 2018. (C) Summation occurs when two cues influence the same navigation parameter. In this case, a strongly attractive visual stimulus (purple) and a weakly aversive wind stimulus (green) each bias turn rate and direction. The strong drive to turn toward the visual cue is summed with the weak drive to turn away from the wind cue. The result (gray) is a turn of intermediate angular velocity toward the stronger (visual) cue. Adapted from Currier & Nagel, 2018. (D) Association occurs when a cue that promotes innate attraction or aversion is paired with an innocuous cue from another modality. Here, noxious heat (red) is paired with orientation toward a visual pattern. The visual stimulus becomes associated with heat avoidance, causing the fly to turn away from the visual cue presented alone. Adapted from Liu et al., 2006.

Figure 2.. Multiple sites of multisensory integration in the fly brain.

(A) Primary sensory regions in the adult fly brain. Visual information is processed by the optic lobes (purple), mechanosensory cues (such as wind and sound) by the antennal mechanosensory and motor center (AMMC, green), and taste stimuli by the sub-esophageal zone (SEZ, blue). Odor, temperature, and humidity signals are all processed in the antennal lobes (orange). (B) Key sites of multisensory integration. Colored arrows (as in panel A) indicate the modalities integrated in each region. The mushroom body receives both olfactory and visual information at its input layer in the calyx (Vogt et al. 2016). Taste information provides valence input to dopamine neurons that control mushroom body output (Kim/Scott 2017). The ventral lateral horn receives input from olfactory, visual, mechanosensory, and taste regions (Dolan 2019). The posterior slope contains the post-synaptic compartments of many descending neurons (DNs, gray) that provide motor commands to the ventral nerve cord. Many DNs receive input from both mechanosensory regions and from lobula columnar cells carrying visual information (Namiki 2017). Finally, the central complex receives visual input through ring neurons of the ellipsoid body (Omoto 2017, Sun 2017). Mechanosensory signals have been observed in the fan-shaped body (Ritzmann 2008), and olfactory neurons have downstream partners there (Scalpen 2019).

Figure 3.. Hypothesized circuit and synaptic mechanisms of integration.

(A) Cross-modal suppression through reciprocal inhibition. Networks driving feeding and locomotion are linked by mutual inhibition (barred connections). Sensory input that drives feeding (tastant, blue) or locomotion (odor, orange) evokes winner-take-all dynamics. (B) Summation through convergent sensory input. Neurons carrying visual (purple) and wind (green) information both make excitatory synapses (arrows) onto a neuron that controls orientation (gray). (C) Gating through presynaptic inhibition. Wind signals (green) provide input to a neuron that controls orientation (gray). Odor information (orange) presynaptically shunts wind input to the orientation control neuron through an inhibitory connection (bar). (D) Cross-modal association through modulation. The simultaneous presentation of noxious heat (red) and a visual stimulus strengthens the synapse from the visual input neuron onto the orientation control neuron through release of a neuromodulator from the heat-sensitive neuron (circle). Subsequent presentations of the visual stimulus alone are sufficient to drive activity in the orientation control cell. Inset shows the strength (w) of the synapse before and after pairing.