Olfactory perception comprises the detection and processing of one or several odor molecules ending in the representation (sometimes identification) by the organism of a particular odor, which may be discriminated from another odor. Animals – including humans – detect odor molecules through receptor systems, in which higher organisms are expressed by receptor cells directly connected to the brain. The brain will analyze and interpret the incoming information and display a response if it is biologically relevant. The response may be physiological/neural, psychological (emotion), and/or behavioral. Responsiveness to the information may be either spontaneous (i.e., predisposed) or consecutive to a learning process. In the latter case, after acquisition, the information is stored by the brain and retrieved later on, therefore contributing to the animals’ acquired knowledge of the world.
Chemical senses, which comprise olfaction and taste, are likely to be the oldest senses evolved as they are found throughout the animal kingdom. In olfaction, this is true from single cell to higher vertebrates and aquatic to terrestrial organisms. So far no species has been shown to be completely anosmic, underlining the pivotal role of olfaction in survival of all animals.
Different Organs to Detect Odor Cues
Due to the overall importance of olfaction in the animal kingdom, organ systems have evolved convergently and show some similarities across taxa, e.g., between vertebrates and invertebrates (Eisthen 2002). The detection systems may be as simple as receptors expressed on the surface of a single-cell organism (Valentine et al. 2008). In insects, the olfactory receptor cells and olfactory sensilla, mainly found on the antennae (Hansson and Stensmyr 2011), detect olfactory cues and transfer the information to the antennal lobe, which processes and relays the learned and non-learned information to the mushroom bodies and/or the lateral horn. In vertebrates, odor molecules reach the nose directly through the nares (orthonasal processing) or indirectly via the mouth (retronasal processing). The vertebrate olfactory system has two major olfactory epithelia, the main and the accessory ones (Brennan and Kendrick 2006). While the first one is typically situated at the back of the nasal cavity and devoted to the detection of volatile cues, the second – vomeronasal organ – involved in the detection of nonvolatile cues is situated at the front of the nasal cavity stretching along the sides of the septum; it may open into the mouth and/or the nose via the nasopalatine ducts. Two other olfactory epithelia have been described in some mammals, the Grüneberg ganglion, which is situated near the entrance to the nasal cavity, and the septal organ, located bilaterally at the ventral base of the nasal septum. The olfactory receptor neurons from the main olfactory epithelium project to the main olfactory bulb, which is the first to relay information to the brain, while the vomeronasal receptor neurons project to the accessory olfactory bulb. From the olfactory bulb, the signal is conveyed to the primary olfactory cortex but also to other brain regions such as hypothalamic nuclei involved in autonomic functions and the amygdala and hippocampus involved in learning and memory. While the vomeronasal organ and accessory olfactory system have long been considered as dedicated to the detection of pheromones, this dogma has been refuted over the last decades through studies showing that they can also process common odor cues and that, conversely, the main olfactory system can process both common odorants and pheromones (Wyatt 2015).
Different Behaviors to Convey Odor Molecules to Sensory Organs
In order to make perception of odor molecules or odor mixtures possible, animals have developed diverse behaviors allowing sampling of the information emanating from the surroundings. These behaviors may help to detect the odor source and the direction to the source or allow for transport of the odor stimuli to specific parts of the olfactory detection organ in species with multiple receptor sides.
Single-cell organisms such as paramecium are unable to detect chemical gradients by simultaneous comparison of the chemical concentration at two parts of the body as observed in multicell organisms. The former possess only one receptor side, while the latter have paired olfactory organs, e.g., two main olfactory epithelia (one per nostril) (Valentine et al. 2008). In order to locate a food source, single-cell organisms use chemotaxis behavior, e.g., they show periods of movement in a straight line interrupted at intervals by a turn. They may “remember” whether the concentration previously experienced was higher or lower than the current concentration.
Multicell organisms can use osmotropotaxis (Gaudry et al. 2012). This strategy depends on measuring instantaneous concentration at two spatially separated odor sensors and turning toward the side of the higher concentration; it was, e.g., described for the fruit fly, which uses its pair of antennae to detect and follow odor cues. A second strategy, which is known as optomotor anemotaxis, involves flying upwind when an odor is sensed (Gaudry et al. 2012). Another orientation strategy is the counterturing, for instance, extensively studied in moths. If the odor of interest is lost, moths switch to cross-wind flight, which may help them track down the odor again. Similar behaviors have been shown also in crustaceans.
Vertebrates appear to combine the use of bilateral chemosensory cue detection with active sampling to localize an odor source. To direct nonvolatile odor molecules to specific receptor sides, specific behaviors have been developed at the receiver level, e.g., the tongue-flicking behavior observed in snakes and other reptiles: The split tip of the tongue allows peaking up nonvolatile molecules and delivering them to the opening of the vomeronasal organ (Daghfous et al. 2012). Similarly, a number of mammals (ruminants, equids, felids, tapirs, and certain marsupials such as kangaroos and wombats) are known to use flehmen behavior which also involves picking up odor molecules with the tongue and applying the attractive nonvolatile substance to the opening of the vomeronasal organ while the head is held up high and the upper lip is retracted. The Asian elephant uses its trunk to apply female urine to the opening of the vomeronasal organ. Furthermore, mammalian sampling of volatile odor molecules is carried out through a specific action, the sniffing behavior, which induces air entry (or amniotic fluid entry in fetuses) into the nostrils, then the nasal cavity, and, finally, the posterior part of the cavity, where fraction of the flow carrying odorants may reach the olfactory epithelium. Thus, a single sniff, a sniffing episode (successive sniffs), or sniffing cycles (successive episodes with number, frequency, velocity, and duration depending on the species, distance from the odor source, chemical complexity of the source, air turbulence, etc.) distribute the molecules to different populations of olfactory receptors. This allows for actively collecting odor information from the surroundings, analyzing complex olfactory scenes, and responding behaviorally to relevant stimuli (Coureaud and Datiche 2009). Importantly, sniffing also contributes to the temporal, spatial and mechanical coding of a stimulus, to the coding of its identity and intensity, and therefore to the representation of a particular percept for a given stimulus (Mainland and Sobel 2006).
Different Modes of Perception to Represent the World
A Complex Olfactory Environment
In ecological conditions, odors rarely result from single odorants but from mixtures of several – tens, hundreds, or more – odorants, and mixtures are themselves emitted among other mixtures coming from the same substrate or adjacent ones. Whatever the species and their aerial or aquatic living surroundings, animals therefore have to deal with an environment both chemically complex – in terms of number, nature, and diversity of volatile and nonvolatile molecules – and dynamic (e.g., daily, seasonal, anthropic and climatic variations). A common challenge shared by animals during their development, and crucial for survival and adaptation, is then to extract pertinent information from this complexity and to respond efficiently to the cues which are the most important for them (i.e., those carrying positive or negative hedonic value) by displaying motor actions allowing to meet their needs.
A Twofold Perceptual Strategy
In terms of perception, since odor mixtures constitute the common stimuli emanating from the physical (e.g., ocean, river, air, ground, rocks, etc.) and biological (e.g., plants, flowers, predators, preys, conspecifics, etc.) components of the environment, animals may simplify the amount of information contained in a mixture either by responding to certain of its elements only (elemental perception) or by responding to the mixture as a whole, i.e., by attributing a particular value to that odor object instead of its elements (configural perception). These two strategies are not necessarily exclusive, because for certain mixtures animals may respond both to a configural odor specific for the mixture and to the odor of one or several of its odorants (weak configural perception).
Elemental perception means that an organism will respond to one or several odorants of a mixture the same way as to the mixture itself or, at least for simple mixtures such as binary ones, that the sum of its responses to each constituent is equivalent to the responsiveness displayed to the mixture (while the level of response to each constituent is superior compared to control odorants) (Kay et al. 2005). This mode of perception makes it possible to reduce the complexity of a mixture by extracting only the information of interest. Elemental perception is, for instance, observed toward key odorants. By key odorants, here we mean particular odorants that convey by themselves, at least in part, the same odor quality as the mixture. For example, in a green apple, humans are particularly sensitive to hexyl acetate and trans-2-hexenal, two molecules that each appear to be strong contributors to the odor quality of that fruit (Bult et al. 2002). This elemental perceptual ability would allow for animals to respond to a complex stimulus through the rapid detection of one, some, or all of its constituents, in order to optimize its knowledge about that stimulus and capability to display preference for it among other stimuli contained in the same surroundings. In addition, it may allow generalizing its responses from one stimulus to another emitting some common elements (e.g., from one food to another food sharing some odorants and both providing nutritional qualities). In certain cases, key odorants present pheromonal properties and correspond to monomolecular pheromones. By pheromone, we mean an odor cue with communicative value, released by a sender and perceived by a receiver, both from the same species, in which the pheromone triggers an adaptive response (physiological and/or behavioral) independently of previous learning. This is typically the case of 2-methylbut-2-enal, the so-called mammary pheromone emitted by rabbit females in their milk among more than 150 other volatile components: the pheromone strongly triggers in newborn rabbits stereotyped orocephalic movements allowing for the pups to search for the nipples when the mother comes into the nest and to orally seize the nipples during a nursing episode (Coureaud et al. 2010) (Fig. 1d).
Configural perception means, conversely, that the perception of mixture elements is restricted to the benefit of a new odor quality, specific of the whole mixture and clearly distinct from the odor qualities of the elements. It is a way to allow grouping individual stimuli into a perceptual unit – a gestalt – and attributing a specific value to a mixture as a whole (compared to its components), which is represented in the brain as a single unit of information, i.e., as an odor object (Kay et al. 2005). This object then becomes prominent in the environment and easily identifiable by the animal in the midst of other stimuli (Staubli et al. 1987). Configural perception may occur for complex odors emitted from food sources (e.g., flowers or preys in animals, meals in humans) or for odors which carry a social value, as for pheromones constituted by a small number of molecules that blend into a given mixture (Badeke et al. 2016). Configural perception is, for instance, at work in humans, when we perceive the typical odor of coffee, while no molecules of coffee effluvium (bouquet of molecules emanating from the substrate) evoke that odor quality by themselves (Czerny et al. 1999). More largely, it is observed in both aquatic and terrestrial organisms, and in invertebrates (e.g., spiny lobsters, slugs, honeybees, moths) as in vertebrates (e.g., catfish, rabbits, rats, dogs). Configural odor perception has mainly been described in adults, but data in the rabbit pinpoint its functionality in the newborn (Coureaud et al. 2014; Schneider et al. 2016); the fact that very young organisms perceive certain mixtures as odor objects makes biological sense because of the chemical complexity of the perinatal environment and urgent necessity for individuals, during this early period of life, to extract information from complex odor substrates (amniotic fluid, maternal body, milk) in order to survive and learn about the surroundings. Interestingly, different species may process the same mixtures configurally, as it has been shown with binary and senary mixtures in rabbits and humans (Coureaud et al. 2014; Sinding et al. 2013), which suggests that the sensory systems of various animal species may have converged in the way they process certain complex stimuli, with a common goal: reducing perceptual complexity of their chemosensory environment (chemosensory Umwelt) to detect and behave selectively toward certain odor stimuli that contribute to their adaptation.
Differences in the neural processing supporting elemental versus configural odor perception, from the periphery of the olfactory system to central brain regions, remain to be clearly deciphered. However, certain results suggest that configural perception may occur as soon as odor molecules interact at the olfactory receptor/olfactory sensory neuron level, then in central regions where interactions between neurons occur (i.e., olfactory bulb in mammals and antennal lobe in insects, respectively) and in higher-order regions (i.e., piriform cortex in mammals and mushroom bodies in insects) (e.g., Rospars et al. 2008; Deisig et al. 2010; Gottfried 2010; Wilson and Sullivan 2011; Schneider et al. 2016; Singh et al. 2018).
Among factors that influence the mode of perception of odor mixtures is the number of components. If configural perception can occur even for very simple mixtures as binary mixtures, it is thought that the olfactory system presents elemental limits: when the number of odorants in a mixture becomes too high compared to that limit, perception would switch from the elemental to the configural mode. In humans, this limit seems to be low (around 4–5 odorants); it appears to be higher in other species (e.g., Sinding et al. 2013). Other factors involved in the way odor mixtures are perceived may also depend on the stimulus, e.g., the chemical nature of the individual components and their ratio in the mixture, or on the receiver, e.g., the animal’s experience of the mixture or its constituents. Thus, if certain mixtures are spontaneously processed in the elemental or configural ways, learning events may modulate this initial perception. The respective influences of all these factors in the final perception of odor mixtures remain to be clearly determined.
From invertebrates to vertebrates and throughout ontogenesis, perception of odor cues is of vital importance to help animals to adapt to the environment in which they are living by displaying responsiveness to certain odorants or mixtures of odorants carrying spontaneous or learned biological values and to build representations about the social and nonsocial components of the environment. Further investigations, from chemistry to behavioral neurosciences, are required to better understand these remarkable sensory and cognitive abilities shared by all species, including humans, aiming to improve their integration into the world through the olfactory modality, alone or in interaction with the other sensory modalities.