Physiol. Res. 65: 369-390, 2016 https://doi.org/10.33549/physiolres.932955 REVIEW Olfactory Sensitivity in Mammalian Species M. WACKERMANNOVÁ1, L. PINC2, †L. JEBAVÝ3 1Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Czech Republic, 2Canine Behavior Research Center, Department of Animal Science and Ethology, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Czech Republic, 3Department of Animal Science and Ethology, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Czech Republic Received November 13, 2014 Accepted February 5, 2016 On-line April 12, 2016 Summary Corresponding author Olfaction enables most mammalian species to detect and M. Wackermannová, Department of Zoology and Fisheries, discriminate vast numbers of chemical structures called odorants Faculty of Agrobiology, Food and Natural Resources, Czech and pheromones. The perception of such chemical compounds is University of Life Sciences Prague, Kamycka 129, 160 00 mediated via two major olfactory systems, the main olfactory Prague 6, Czech Republic. E-mail: [email protected] system and the vomeronasal system, as well as minor systems, such as the septal organ and the Grueneberg ganglion. Distinct Introduction differences exist not only among species but also among individuals in terms of their olfactory sensitivity; however, little is Chemosensory systems develop very early in known about the mechanisms that determine these differences. ontogeny and are found in almost every animal. The In research on the olfactory sensitivity of mammals, scientists mammalian sense of smell detects and discriminates thus depend in most cases on behavioral testing. In this article, between innumerable substances that have very diverse we reviewed scientific studies performed on various mammalian chemical structures and features (Corcelli et al. 2010). species using different methodologies and target chemical The omnipresent chemical stimuli enable detection substances. Human and non-human primates as well as rodents and discrimination of home range, conspecifics, and dogs are the most frequently studied species. Olfactory mates, mother, food resources, predators, and prey. threshold studies on other species do not exist with the exception Chemosensation is critical for survival and reproductive of domestic pigs. Olfactory testing performed on seals, elephants, success (Wilson 2006). Many species use chemical cues and bats focused more on discriminative abilities than on to recognize genetically related kin, even the identity of sensitivity. An overview of olfactory sensitivity studies as well as conspecifics using individual olfactory cues in order to olfactory detection ability in most studied mammalian species is avoid inbreeding as well as to determine the animal’s presented here, focusing on comparable olfactory detection reproductive status (Wilson 2006, Cometto-Muniz and thresholds. The basics of olfactory perception and olfactory Abraham 2008). Olfaction also helps protects the entire sensitivity factors are also described. organism as this system provides an early warning system for the detection of health hazards and imminent threats Key words (fire, leaking natural gas, rotten food, or toxins) and plays Olfaction • Sensitivity • Odor detection threshold • Mammals a critical role in nutrition (Laska and Hudson 1993, Hawkes and Doty 2009). The sensory and hedonic PHYSIOLOGICAL RESEARCH • ISSN 0862-8408 (print) • ISSN 1802-9973 (online) 2016 Institute of Physiology of the Czech Academy of Sciences, Prague, Czech Republic Fax +420 241 062 164, e-mail: [email protected], www.biomed.cas.cz/physiolres 370 Wackermannová et al. Vol. 65 evaluations of most food-related flavors are mainly mechanism evolved from the “lock and key” theories that dependent on olfactory perception (Nevitt 2000). claim molecular shape determines odor (Wright 1977, Chemosensory-based communication is a vital Frater 1998) over odotope theory-based identification of signaling tool (Frasnelli et al. 2011). From the most receptor subtypes responding not to one but to many gregarious to the most solitary, all animals need to odorants (Mori 1994, Malnic et al. 1999) to vibration coordinate their activities with others of the same species. theory (Turin and Yoshii 2003). This theory, based on the This coordination is based on communication (Laberge molecular vibrations of odorants, was first described in and Hara 2004), which involves utilization of chemical 1938 (Dyson 1938) and has been newly extended by signals known as pheromones (sexual attractant Turin (2002). This theory states that odor is determined pheromones, mammary pheromones, aggression by the vibration spectrum of the molecule. The detection pheromones, alarm pheromones, marking pheromones) mechanism is based on inelastic electron tunneling, and (Brennan 2010). the vibration spectra of the odorants determine their odor Olfactory sensitivity in mammals has been (Turin and Yoshii 2003), but after clean chemical studied since the 1960s, but experiments focused on an deuteration studies (Block et al. 2015) the vibration exact olfactory threshold are rare. The small number of theory should be reexamined (Vosshal 2015). In these experiments differs in methods as well as in results. conclusion, no theory explaining the principles of the The main aim of this review is to present the olfactory odorant-receptor interaction has been proved to be thresholds of mammalian species and to show the entirely plausible (Zarzo 2007). exclusivity of the olfactory system in mammals, despite Individual variations in the limits of detection the differences in the results of individual studies. for different stimuli have been known for a long time. There has been a long-term effort to compare Although individual odor thresholds vary, studies have odor perception in humans and animals. The comparison indicated the variations within an individual are may develop scientific evidence concerning hypotheses comparable to variations between individuals (Cain about relative olfactory powers in humans and other 1989). The olfactory threshold is the minimum mammalian species. An important criterion is the concentration of a target stimulus an individual is able to integration of human psychophysical results with animal reliably differentiate from a blank sample (deionized results in similar studies, as animal results may water in most studies). In recent experiments that focused approximate the neural mechanism and olfactory on olfactory sensitivity in mammalian species, the perception in humans (Walker and Jennings 1991). olfactory detection threshold (ODT) was considered the limit of olfactory sensitivity. What is olfaction? Olfactory subsystems Olfaction mediates the perception of volatile chemicals, which convey information about the In mammals, the olfactory, gustatory, and environment to the receiver. Variations in the precise trigeminal systems are involved in chemical senses (sense structure of individual odorant molecules, of smell, taste, somatosensation). The nose, the main concentrations of those molecules, and specific olfactory organ, consists of multiple olfactory combinations and relative concentrations of components subsystems, among which the main olfactory epithelium in a mixture of odorant molecules provide crucial (MOE) and the vomeronasal organ (VNO) have been the information about the surrounding world. Given that most studied (Trotier 2011). The MOE is composed of most odors are complex mixtures of a number of single two types of cells, microvillar cells and olfactory sensory components, the discrimination of one odor from neurons (OSNs), which express G-protein-coupled another is difficult, and previous experience enhances odorant receptors. The VNO contains two olfactory odor discrimination in mammalian species (Firestein subsystems (apical and basal) and two classes of 2001, Croy et al. 2015). vomeronasal receptors (V1Rs and V2Rs) (Young et al. Over time, a number of theories have been 2010). Although human embryonic VNO exerts attempted to explain the relationship between the a developmental track common to microsmatic mammals, molecular structure and odor in the primary olfactory after the initial development, the VNO regresses, with reception mechanism. The view of the reception only a few vestiges persisting in adults and most 2016 Olfactory Sensitivity in Mammalian Species 371 chemoreceptor cells within the persistent vomeronasal perhaps, determining relative stimulus intensity; and duct (VND) wear off. By the absence of neurons and 4) assigning meaning to the stimulus (Wilson 2006, vomeronasal nerve bundles it can be deduced that the Wilson and Mainen 2006). Detection is the degree of vomeronasal epithelium is not a sensory organ in adult presence, while recognition involves matching input, and humans (Trotier et al. 2000). The genes that code for the identification is the assignment of meaning. These three V1R-type and V2R-type receptor proteins are mostly different functions do not necessarily correlate with nonfunctional in humans (Mohedano-Moriano et al. specific anatomical locations (Mombaerts 2001). 2008). Although vomeronasal ducts and pits have been Repeated exposure is an important factor in observed in humans (Moran et al. 1991, Stensaas et al. developing olfactory sensitivity, so learning is evidently 1991, Boehm and Gasser 1993, Trotier and Doving a vital