Olfaction in the Multisensory Processing of Faces: A Narrative Review of the Influence of Human Body Odors

A recent body of research has emerged regarding the interactions between olfaction and other sensory channels to process social information. The current review examines the influence of body odors on face perception, a core component of human social cognition. First, we review studies reporting how body odors interact with the perception of invariant facial information (i.e., identity, sex, attractiveness, trustworthiness, and dominance). Although we mainly focus on the influence of body odors based on axillary odor, we also review findings about specific steroids present in axillary sweat (i.e., androstenone, androstenol, androstadienone, and estratetraenol). We next survey the literature showing body odor influences on the perception of transient face properties, notably in discussing the role of body odors in facilitating or hindering the perception of emotional facial expression, in relation to competing frameworks of emotions. Finally, we discuss the developmental origins of these olfaction-to-vision influences, as an emerging literature indicates that odor cues strongly influence face perception in infants. Body odors with a high social relevance such as the odor emanating from the mother have a widespread influence on various aspects of face perception in infancy, including categorization of faces among other objects, face scanning behavior, or facial expression perception. We conclude by suggesting that the weight of olfaction might be especially strong in infancy, shaping social perception, especially in slow-maturing senses such as vision, and that this early tutoring function of olfaction spans all developmental stages to disambiguate a complex social environment by conveying key information for social interactions until adulthood.

Tadpole-transporting frogs use stagnant water odor to find pools in the rainforest

Breeding sites are often a limited and ephemeral resource for rainforest frogs. This resource limitation has driven the evolution of diverse reproductive strategies that increase offspring survival. For example, poison frogs shuttle their tadpoles from terrestrial clutches to aquatic rearing sites, using various cues to assess pool suitability. Yet, how frogs find new pools is unknown. We tested the role of odor cues in the process of finding tadpole deposition sites by the poison frog Allobates femoralis. We created 60 artificial pools grouped into three conditions: stagnant water, tadpole water, and clean water control. Fifteen pools were discovered within six days, with more tadpoles and more frogs directly observed at pools with stagnant odor cues. Our findings suggest that frogs use odor cues associated with stagnant water for the initial discovery of new breeding pools. These cues may be good indicators of pool stability and increased likelihood of tadpole survival.

Exploring the Role of Cognition in the Annual Fall Migration of the Monarch Butterfly (Danaus plexippus)

Each fall, monarch butterflies in eastern North America undergo an extraordinary long-distance migration to wintering areas in central Mexico, where they remain until returning northward in the spring. Migrants survive the overwintering period by metabolizing lipid reserves accumulated exclusively though floral nectar; however, there is little known about how individuals maximize foraging efficiency in the face of floral environments that constantly change in complex and unpredictable ways along their migratory route. Here, a proboscis extension paradigm is used to investigate the role of cognition during the foraging phase of monarch migration. Male and female migratory butterflies were consecutively trained to discriminate between two color and odor cues and then tested for their ability to simultaneously retain the information on the reward value of each cue in memory without reinforcement over a period of 7 days. To gain further insight into cognitive abilities of monarchs as a migratory species, a second set of captive-reared males and females were tested under harnessed conditions at the same time as wild-caught fall migrants. Results showed that male and female migrants can learn the reward properties of color and odor cues with over 75% accuracy after less than 40 s of exposure and can simultaneously retain visual and olfactory information predicting the availability of floral rewards in memory without reinforcement for at least 7 days. Captive-reared male butterflies also showed the ability to retain visual and olfactory information in long-term memory for 7 days; however, 80% of captive-reared females could not retain color cues in long-term memory for more than 24 h. These novel findings are consistent with the view that monarch butterflies, as a migratory species, have enhancements to long-term memory that enable them to minimize the amount of time and energy wasted searching for suitable nectar sources during their annual fall migration, thereby optimizing migratory performance and increasing the chance of overwinter survival. The possibility that female monarchs undergo a seasonal change in visual long-term memory warrants further empirical investigation.

Red Junglefowl Chicks Seek Contact With Humans During Foraging Task

Contact seeking with humans is documented in some domestic animals, mainly dogs, which have advanced communication skills. Domestication as a companion animal is thought to underlie this ability. However, also domesticated horses and goats display similar human-directed behaviors. This suggests either a broader effect of domestication on contact-seeking behavior, or alternatively, that social interactions with humans can result in the development of human contact seeking. As part of another study, we observed contact-seeking behavior in juvenile red junglefowl (Gallus gallus) chicks exposed to behavioral training since hatching, during a foraging task, where chicks were singly required to collect food rewards in a familiar arena using odor cues. If chicks left the arena, we recorded if they approached and looked up at the experimenter, or if they approached other objects (including another human). Chicks approached the experimenter significantly more often than they approached other objects. This behavior was not linked to a fast performance in the test arena, which gave some birds more time to explore the surroundings, or to learning ability measured in a cognitive task. Yet, the preference for the experimenter was lower for chicks that were handled more prior to the experiment. Also, approach probability was positively correlated with escape attempts in a novel arena test. The observed variation in approach behavior suggests a link to aspects of personality, and exposure to human interactions and experimental procedures. Our observations suggest that, although neither domesticated nor selectively bred, red junglefowl that are socialized with humans can potentially develop behavior used to describe contact seeking. Together with evidence from cognitive and behavioral studies, our results suggest that social experiences, not only domestication, can affect human-animal interactions. We propose how interactions between behavior, cognition and handling could be studied further in controlled settings to validate the preliminary findings of our study and uncover the underlying mechanisms.

Conspecific odor cues induce different vocal responses in serrate-legged small treefrogs, but only in the absence of acoustic signals

Background Signal detection is crucial to survival and successful reproduction, and animals often modify behavioral decisions based on information they obtained from the social context. Undeniably, the decision-making in male-male competition and female choice of anurans (frogs and toads) depends heavily on acoustic signals. However, increasing empirical evidence suggests that additional or alternative types of cue (e.g., visual, chemical, and vibratory) can be used to detect, discriminate and locate conspecifics in many anuran species. Nevertheless, few studies have investigated whether conspecific odor cues affect male’s calling behavior. In this study, we conducted an experiment to investigate whether and how different chemical cues (male odors, female odors, and stress odors) from conspecifics affect male’s calling strategies in serrate-legged small treefrogs (Kurixalus odontotarsus), and whether the combined chemical and acoustic stimuli have additive effects on calling behavior or not. Results We found that compared with female odors, male K. odontotarsus reduced calling investment in response to male odors or stress odors, in the absence of rival’s advertisement calls. When odor stimuli and advertisement calls were presented simultaneously, however, there were no differences in the vocal response of focal males among odor groups. Conclusions These results provide evidence that male treefrogs switch calling investment according to different odor cues from conspecifics, and further demonstrate that calling behavior can be affected by chemical cues in anuran species. Our study highlights the potential role of airborne chemical cues in sex identification and contributes to increase our understanding of anuran communication.

Enhanced negative emotional processing limits behavioral flexibility in a mouse model of autism spectrum disorder

Impaired behavioral flexibility might underlie some of the symptoms associated with autism spectrum disorder (ASD). We investigated whether and how behavioral flexibility is impaired in a mouse model of ASD by testing Shank2-knockout (Shank2-KO) mice in reversal learning. Shank2-KO mice were trained in probabilistic classical conditioning with two odor cues paired with water and air puff. Upon the reversal of cue-outcome contingency, Shank2-KO mice were significantly slower than wild-type mice in reversing their anticipatory licking responses. Shank2-KO mice also showed stronger anticipatory eye closure responses than wild-type mice to the air puff, raising a possibility that the impairment might be because of enhanced negative emotional processing. Indeed, Shank2-KO mice showed intact reversal learning when the strong air puff was replaced with a mild air puff. Shank2-KO mice also showed intact reversal learning between two odor cues predicting rewards with different probabilities. These results indicate that enhanced negative emotional processing suppresses reversal learning despite of intact capability to learn cue-outcome contingency changes in Shank2-KO mice in our behavioral settings. Our findings suggest that behavioral flexibility may be seriously limited by abnormal emotional processing in ASD.

Spatial, but not temporal, aspects of orientation are controlled by the fine scale distribution of chemical cues in turbulent odor plumes

Orientation within turbulent odor plumes occurs across a vast range of spatial and temporal scales. From salmon homing across featureless oceans to microbes forming reproductive spores, the extraction of spatial and temporal information from chemical cues is a common sensory phenomenon. Yet, given the difficulty of quantifying chemical cues at the spatial and temporal scales used by organisms, discovering what aspects of chemical cues controls orientation behavior has remain elusive. In this study, we place electrochemical sensors on the carapace of orienting crayfish and measure, with fast temporal rates and small spatial scales, the concentration fluctuations arriving at the olfactory appendages during orientation. The results of these studies show that the spatial aspects of orientation (turning and heading angles) are controlled by the temporal aspects of odor cues.

Olfactory tracking strategies in a neotropical fruit bat

ABSTRACTMany studies have characterized olfactory-tracking behaviors in animals, and it has been proposed that search strategies may be generalizable across a wide range of species. Olfaction is important for fruit- and nectar-feeding bats, but it is uncertain whether existing olfactory search models can predict the strategies of flying mammals that emit echolocation pulses through their nose. Quantitative assessments of how well echolocating bats track and localize odor sources are lacking, so we developed a behavioral assay to characterize the olfactory detection and tracking behavior of crawling northern yellow-shouldered bats (Sturnira parvidens), a common neotropical frugivore. Trained bats were presented with a choice between control and banana-odor-infused solutions in a series of experiments that confirmed that bats are able to locate a reward based on odor cues alone and examined the effect of odor concentration on olfactory search behaviors. Decision distance (the distance from which bats made their change in direction before directly approaching the target) was distinctly bimodal, with an observed peak that coincided with an inflection point in the odor concentration gradient. We observed two main search patterns that are consistent with both serial sampling and learned route-following strategies. These results support the hypothesis that bats can combine klinotaxis with spatial awareness of experimental conditions to locate odor sources, similar to terrestrial mammals. Contrary to existing models, bats did not display prominent head-scanning behaviors during their final approach, which may be due to constraints of nasal-emitted biosonar for orientation.

Not avian but mammalian scavengers efficiently consume carcasses under heavy snowfall conditions: a case from northern Japan

Interest in trophic interactions and ecosystem functions derived from carcass consumption by scavengers has been increasing. Here, we conducted the first evaluation of scavenging processes in an ecosystem with heavy snow, located in northern Japan, which is characterized by the limitations of visual and odor cues to detect carcasses. In this study, we verified the behavioral traits and assemblage compositions of avian and mammalian scavengers, which consumed six different carcass types buried in snow. We measured the visits of scavengers using camera traps between 2010 and 2020. The total scavenger richness observed was relatively low (only 12 species) compared to warmer biomes. We observed seven avian scavenger species, but their visit frequencies were extremely low compared with those of nocturnal mammalian scavengers, such as raccoon dogs (Nyctereutes procyonoides) and martens (Martes melampus), which were able to detect carcasses more rapidly and frequently. Our findings imply that large snow piles significantly prevent avian scavengers from detecting carcasses. In contrast, the snow piles could protect carcasses from the freezing air and ensure the occurrence of a basal level of microbial decomposition, possibly leading to carcass decomposition. This probably results in carcasses still providing odor cues for mammalian scavengers with heightened sense of smell. Moreover, considering the high carcass consumption rate (91.3% of full-body carcass; n = 23) and short carcass detection times (approximately 90 h) observed, it is possible that scavenging in heavy snowfall conditions has become systematically integrated into the foraging tactics of many mammalian scavengers.