Spatial information from the odour environment in mammalian olfaction

The sense of smell is an essential modality for many species, in particular nocturnal and crepuscular mammals, to gather information about their environment. Olfactory cues provide information over a large range of distances, allowing behaviours ranging from simple detection and recognition of objects, to tracking trails and navigating using odour plumes from afar. In this review, we discuss the features of the natural olfactory environment and provide a brief overview of how odour information can be sampled and might be represented and processed by the mammalian olfactory system. Finally, we discuss recent behavioural approaches that address how mammals extract spatial information from the environment in three different contexts: odour trail tracking, odour plume tracking and, more general, olfactory-guided navigation. Recent technological developments have seen the spatiotemporal aspect of mammalian olfaction gain significant attention, and we discuss both the promising aspects of rapidly developing paradigms and stimulus control technologies as well as their limitations. We conclude that, while still in its beginnings, research on the odour environment offers an entry point into understanding the mechanisms how mammals extract information about space.

Coupling of mouse olfactory bulb projection neurons to fluctuating odour pulses

Odours are transported by turbulent air currents, creating complex temporal fluctuations in odour concentration. Recently, we have shown that mice can discriminate odour stimuli based on their temporal structure, indicating that information present in the temporal structure of odour plumes may be extracted by the mouse olfactory system. Here using in vivo electrophysiological recordings, we show that mitral and tufted cells (M/TCs), the projection neurons of the mouse olfactory bulb, can encode the dominant temporal frequencies present in odour stimuli up to frequencies of at least 20 Hz. We show that M/TCs couple their membrane potential to odour concentration fluctuations; coupling was variable between M/TCs but independent of the odour presented and with TCs displaying slightly elevated coupling compared to MCs in particular for higher frequency stimulation (20Hz). Pharmacologically blocking the inhibitory circuitry strongly modulated frequency coupling. Together this suggests that both cellular and circuit properties contribute to the encoding of temporal odour features in the mouse olfactory bulb.

Efficiency of island homing by sea turtles under multimodal navigating strategies

A dot in the vastness of the Atlantic, Ascension Island remains a lifelong goal for the green sea turtles that hatched there, returning as adults every three or four years to nest. This navigating puzzle was brought to the scientific community’s attention by Charles Darwin and remains a topic of considerable speculation. Various cues have been suggested, with orientation to geomagnetic field elements and following odour plumes to their island source among the most compelling. Via a comprehensivein silicoinvestigation we test the hypothesis that multimodal cue following, in which turtles utilise multiple guidance cues, is the most effective strategy. Specifically, we combine agent-based and continuous-level modelling to simulate displaced virtual turtles as they attempt to return to the island. Our analysis shows how population homing efficiency improves as the number of utilised cues is increased, even under “extreme” scenarios where the overall strength of navigating information decreases. Beyond the paradigm case of green turtles returning to Ascension Island, we believe this could commonly apply throughout animal navigation.

Flexible weighing of olfactory and vector information in the desert ant Cataglyphis fortis

Desert ants, Cataglyphis fortis , are equipped with remarkable skills that enable them to navigate efficiently. When travelling between the nest and a previously visited feeding site, they perform path integration (PI), but pinpoint the nest or feeder by following odour plumes. Homing ants respond to nest plumes only when the path integrator indicates that they are near home. This is crucial, as homing ants often pass through plumes emanating from foreign nests and do not discriminate between the plume of their own and that of a foreign nest, but should absolutely avoid entering a wrong nest. Their behaviour towards food odours differs greatly. Here, we show that in ants on the way to food, olfactory information outweighs PI information. Although PI guides ants back to a learned feeder, the ants respond to food odours independently of whether or not they are close to the learned feeding site. This ability is beneficial, as new food sources—unlike foreign nests—never pose a threat but enable ants to shorten distances travelled while foraging. While it has been shown that navigating C. fortis ants rely strongly on PI, we report here that the ants retained the necessary flexibility in the use of PI.

Role of current and prey odour in the displacement behaviour of the sea star Asterias vulgaris

We performed a factorial experiment to investigate the effects of current and prey odours (mussels) on the displacement behaviour of the sea star Asterias vulgaris (Verrill, 1866). This sea star is a common subtidal predator of sessile and slow-moving animals in the western North Atlantic Ocean. In the presence of current and prey odours in a flume, sea stars oriented themselves upstream and 70% succeeded in finding the prey. Also, the degree of orientation toward the prey increased as the sea star approached the prey. In contrast, only 5% of individuals tested in still water found the prey. Thus, for A. vulgaris the presence of macroscale flow is an essential condition for locating distant prey. Sea stars tested in current alone showed rheotactic behaviour, moving diagonally upstream. This behaviour should enhance the probability of encountering prey odour plumes in the field. Sea stars moved faster and straighter in flowing water than in still water. The slow movement of A. vulgaris in still water probably minimizes costs of foraging when there is a low chance of finding prey and the straight diagonal movement in current should ensure that the sea star continuously samples new areas, rather than resampling the same odour-free area.