Olfactory navigation in arthropods

Abstract

Using odors to find food and mates is one of the most ancient and highly conserved behaviors. Arthropods from flies to moths to crabs use broadly similar strategies to navigate toward odor sources-such as integrating flow information with odor information, comparing odor concentration across sensors, and integrating odor information over time. Because arthropods share many homologous brain structures-antennal lobes for processing olfactory information, mechanosensors for processing flow, mushroom bodies (or hemi-ellipsoid bodies) for associative learning, and central complexes for navigation, it is likely that these closely related behaviors are mediated by conserved neural circuits. However, differences in the types of odors they seek, the physics of odor dispersal, and the physics of locomotion in water, air, and on substrates mean that these circuits must have adapted to generate a wide diversity of odor-seeking behaviors. In this review, we discuss common strategies and specializations observed in olfactory navigation behavior across arthropods, and review our current knowledge about the neural circuits subserving this behavior. We propose that a comparative study of arthropod nervous systems may provide insight into how a set of basic circuit structures has diversified to generate behavior adapted to different environments.

Keywords: Arthropod; Insect; Navigation; Neural circuits; Olfaction.

Fig. 1

Odor dispersal is driven by features of the environment. a Odors in water form filamentous plumes with packets of high odor concentration found downstream of the plume. b In air, increased diffusion generates odor plumes with a graded structure. c Plumes along substrates, close to a boundary layer, form orderly gradients. d Odor trails are deposited on a substrate and can be broken up by weathering. All images depict instantaneous odor structure. Colors represent normalized concentration as a fraction of source concentration. (Adapted from Weissburg , Webster and Weissburg , Connor et al. , Draft et al. 2018)

Fig. 2

Animals use diverse strategies for odor source localization. a Flow taxis is a common strategy for navigating turbulent plumes, as flow direction represents a more reliable signal of source direction than local concentration. b Spatial comparisons across antennae facilitate the detection of odor gradients and odor motion based on concentration and timing differences. c Integration of plume dynamics over time can be used to infer odor source location based on reliable plume statistics. d Many of these strategies imply the use of spatial memory to integrate sensory observations with movement of the antennae or body. For example, an ant using measurements over successive antennal sweeps to follow an odor trail must integrate local measurements of odor with knowledge of antennal motion to identify trail direction. Thus, a variety of cues, requiring different levels of computation, play a role in localizing an odor source

Fig. 3

High-level components of olfactory navigation are conserved across species. a Arthropods use a combination of surging, searching, and stopping to navigate to an odor source. b Surging consists of relatively straight, directional movements, that generally persist while contacts with odor are frequent. In different species, surging may be driven by different sensory signals (e.g., pulsed or constant plumes), and occur with different speeds due to locomotor differences. c Searching, or “casting”, follows loss of the plume and consists of increases in turning and path curvature. As with surging, the dynamics of searching vary between species—flying Manduca (left) perform the highly stereotyped casts typical of pheromone tracking in moths, while walking Drosophila (right) perform irregular searching on loss of odor. d Stopping may occur when odor contacts are infrequent, and can allow for evidence accumulation via active search (Drosophila larval head casting, left) or through observations over time (Callinectes adult, right)

Fig. 4

Odor and wind processing pathways in Drosophila. a Glomeruli in the antennal lobe integrate signals from antennal olfactory sensory neurons, and pass this information to two associative centers, the mushroom body and the lateral horn, which compute learned and innate valence, respectively. A subset of mushroom body and lateral horn outputs are combined with wind information in the fan-shaped body of the central complex to generate navigational signals. These signals are passed to the premotor lateral accessory lobe and ultimately drive behavior through motor neurons in the ventral nerve cord. Other mushroom body and lateral horn outputs bypass the central complex to drive behavior through direct pathways to the LAL or other descending inputs to the ventral nerve cord. b Stretch receptive Johnston’s organ neurons (JONs) that project to the antennal mechanosensory and motor center (AMMC) respond to displacement of the antennae due to wind. This information is passed to the wedge, where inputs from the two antennae are integrated to generate a representation of wind direction. Other WED neuron carry displacement information to the LAL and then to central complex. In the fan-shaped body of the central complex, wind direction and odor value information is integrated. This information is thought to descend via the LAL to drive activity in the VNC. c Anatomically distinct circuits for odor (pink) and wind (blue) sensing converge in navigation centers (purple, detailed in Fig. 5) to drive movement toward an odor source

Fig. 5

Olfactory navigation circuits within the central complex. The fan-shaped body has been proposed to integrate odor and wind direction signals to generate a goal-direction signal for navigation. a Compass neurons (EPGs, gray) carry a multimodal representation of heading and provide input to the fan-shaped body (FB) through the protocerebral bridge (PB). Columnar inputs to the fan-shaped body (PFNs, blue) receive heading input from the PB and airflow information from the noduli (NO). Tangential inputs to the fan-shaped body (red) carry non-directional odor information. Local neurons (h∆C, purple) receive input from both columnar neurons and tangential neurons and show odor-gated wind-direction tuned signals. b PFL3 neurons (green) receive phase-shifted heading information from the PB and indirect input from local neurons. They are proposed to control steering through their outputs to the LAL. c FB circuits integrate odor, airflow, and heading representation to direct navigation. (Adapted from Hulse et al. ; Lyu et al. ; Lu et al. ; Currier et al. ; Matheson et al. .)