Mechanisms of odor-tracking: multiple sensors for enhanced perception and behavior

Abstract

Early in evolution, the ability to sense and respond to changing environments must have provided a critical survival advantage to living organisms. From bacteria and worms to flies and vertebrates, sophisticated mechanisms have evolved to enhance odor detection and localization. Here, we review several modes of chemotaxis. We further consider the relevance of a striking and recurrent motif in the organization of invertebrate and vertebrate sensory systems, namely the existence of two symmetrical olfactory sensors. By combining our current knowledge about the olfactory circuits of larval and adult Drosophila, we examine the molecular and neural mechanisms underlying robust olfactory perception and extend these analyses to recent behavioral studies addressing the relevance and function of bilateral olfactory input for gradient detection. Finally, using a comparative theoretical approach based on Braitenberg's vehicles, we speculate about the relationships between anatomy, circuit architecture and stereotypical orientation behaviors.

Keywords: bilateral; chemotaxis; drosophila melanogaster; olfaction; orientation behavior; sensory perception.

Figure 1

Main orientation strategies underpinning chemotaxis in E. coli (A) and C. elegans (B). Trajectory segmentation models for E. coli and C. elegans (paths adapted from Berg and Brown, , and from Pierce-Shimomura et al., 1999) reveal that the probability of switching between “run” and “turn” modes is modulated by the time derivative of the concentration experienced by the organism. This simple mechanism leads to indirect navigation (kinesis) towards attractants and away from repellents.

Figure 2

Mechanisms of odor processing in the peripheral olfactory system of the larval and adult Drosophila. (A) The larval olfactory system is composed of two dorsal organs located at the tip of the head. Inset: Each dorsal organ is a central, multiporous “dome”. Odorant receptors (ORs) reside in the dendritic membranes of 21 olfactory receptor neurons (ORNs) which densely innervate the dome. (B) In adults, the 3rd antennal segments and maxillary palps are covered with olfactory sensilla. Inset: ORs reside in the dendritic membranes of ORNs housed within an individual porous sensillum. (C) The binding domains of ORs determine the specificity and affinity of an OR for specific odors. (D) Increasing the number of ORs in the ORN dendrites increases the number of available odor-binding sites, possibly enhancing ORN sensitivity. (E) Larval ORNs project ipsilaterally to discreet glomeruli within the larval antennal lobe (LAL) and synapse onto second-order olfactory projection neurons (PNs). In larvae, the ORN to glomerulus (GLOM) to PN ratio is 1:1:1. (F) Adult ORNs project bilaterally to discreet glomeruli within both the left and right antennal lobes (AL) and synapse onto PNs. In adults, the ORN to GLOM to PN ratio is ∼26:1:3. (G) In adults, increasing the number of ORN inputs enhances the PN signal-to-noise ratio (SNR). The maximum SNR increase achievable by pooling n inputs is √n. (H) In adults and larvae, inhibitory local interneurons (LNs) connect many glomeruli in the AL. These are thought to suppress PN output downstream of strong ORN input (inset, adapted from Olsen and Wilson, 2008). (I) In adults, excitatory LNs connect many glomeruli throughout the AL and enhance PN output downstream of weak ORN input (inset, adapted from Olsen et al., 2007). (J) The properties of OR specificity and affinity combined with lateral processing in the AL contribute to concentration invariant odor perception and behavior. Wild type flies may theoretically show stable behavioral attraction (positive response index (RI)) across a range of stimulus intensities (red). Detection over a range of concentrations might involve an array of narrowly tuned OR/ORN classes (say, 3) and individuals with only a single functional OR may be expected to respond across a narrow range of stimulus intensities (blue, green, maroon).

Figure 3

Behavioral performances of Drosophila with unilateral olfactory function. (A–C) Drosophila larvae do not require bilateral sensory input for chemotaxis. (A) Topographic reconstruction of a controlled exponential odor gradient based on infrared spectroscopy (for details see Louis et al., 2008a). The star represents the location in the arena where the larva is introduced. (B) Representative experimental trajectories of OR83b null mutants (red) and larvae with olfactory input rescued bilaterally (green) or unilaterally in a single functional OR42a-expressing ORN (left, orange; right, blue). (C) Quantification of chemotactic performance with a score measuring the overall alignment of the trajectory with the gradient (data of panels A–C are adapted from Louis et al., 2008a). (D–G) Adult flies use bilateral spatial comparisons of antennal inputs for spatial orientation in flight. (D) In a free-yaw magnetic tether flight arena, flies were positioned 90° to the right (+, blue arrows) or left (−, green arrows) of a spatially discreet odor plume (orange triangle). (E) The resulting flight trajectories, where color is used to discriminate between individuals, reveal that flies actively turn toward the odor plume. (F) Occluding the left 3rd antennal segment with UV activated glue (red) impairs olfactory orientation to the left (blue), but not to the right (green). (G) When exposed to a fixed head-on odor plume in a rigid tether flight arena, unilaterally occluded flies modulate left and right wing beat amplitude (WBA) in attempt to steer toward the intact antenna (data of panes D–G are adapted from Duistermars et al., 2009).

Figure 4

Design of three main classes of Braitenberg-like vehicles inspired by real biological systems. (A) Our type A vehicle is akin to E. coli and C. elegans and corresponds to the original Braitenberg's “Vehicle 1” (Braitenberg, , pp. 3–5). This vehicle has a single fixed sensor which directly activates a single motor. (B) Our type B vehicle, analogous to Drosophila larvae, is similar to Braitenberg's “Vehicle 3a” (Braitenberg, , pp. 10–12). It has two sensors in close proximity at the tip of a laterally swinging head and sensor activation influences motor activity when the head is engaged to one side. (C) Our type C vehicle is inspired by flying adult Drosophila and corresponds to Braitenberg's “Vehicle 2b” (Braitenberg, , p. 7). It is able to detect concentration gradients via two spatially distributed sensors which directly activate contralateral motors. Processors can contain sites for integration of proprioceptive feedback (type B) and include more realistic specific stimulus thresholds, filters, non-linear dependencies on stimulus intensity, and sites for elementary memory.

Figure 5

Vehicles in motion driven by an odor gradient. The type A vehicle relies on instantaneous olfactory perception and utilizes an indirect orientation mechanism where turning rate and velocity are a function of the stimulus concentration (kinesis). The underlying simple orientation rule is: If the concentration is low, turn frequently. Conversely, if the concentration is high, suppress random turns and go straight. This rule results in an indirect trajectory toward the odor source. The type B vehicle is equipped with a moveable head (side-to-side) with two sensors. The underlying orientation rule is: When the head is engaged to the side, inhibit the ipsilateral motor at a level proportional to the sensory input. This rule results in a trajectory sequentially aligned with the vector field of the stimulus gradient (taxis). The type C vehicle has the capacity to simultaneously measure concentrations at different points in space via purely spatial comparisons (osmotropotaxis). The underlying orientation rule is: If the difference in concentration across the two sensors is zero, increase the activation both motors at a level proportional to the sensory input. Conversely, if a concentration difference is measured across the two sensors, activate more strongly the motor opposite the side of highest odor concentration. This rule results in a trajectory aligned with the vector field of the stimulus gradient. Behaviors following source acquisition are illustrated in the panels on the right.