Nature and human well-being: The olfactory pathway.

The world is undergoing massive atmospheric and ecological change, driving unprecedented challenges to human well-being. Olfaction is a key sensory system through which these impacts occur. The sense of smell influences quality of and satisfaction with life, emotion, emotion regulation, cognitive function, social interactions, dietary choices, stress, and depressive symptoms. Exposures via the olfactory pathway can also lead to (anti-)inflammatory outcomes. Increased understanding is needed regarding the ways in which odorants generated by nature (i.e., natural olfactory environments) affect human well-being. With perspectives from a range of health, social, and natural sciences, we provide an overview of this unique sensory system, four consensus statements regarding olfaction and the environment, and a conceptual framework that integrates the olfactory pathway into an understanding of the effects of natural environments on human well-being. We then discuss how this framework can contribute to better accounting of the impacts of policy and land-use decision-making on natural olfactory environments and, in turn, on planetary health.

The PROUST hypothesis: the embodiment of olfactory cognition.

The extension of cognition beyond the brain to the body and beyond the body to the environment is an area of debate in philosophy and the cognitive sciences. Yet, these debates largely overlook olfaction, a sensory modality used by most animals. Here, I use the philosopher's framework to explore the implications of embodiment for olfactory cognition. The philosopher's 4E framework comprises embodied cognition, emerging from a nervous system characterized by its interactions with its body. The necessity of action for perception adds enacted cognition. Cognition is further embedded in the sensory inputs of the individual and is extended beyond the individual to information stored in its physical and social environments. Further, embodiment must fulfill the criterion of mutual manipulability, where an agent's cognitive state is involved in continual, reciprocal influences with its environment. Cognition cannot be understood divorced from evolutionary history, however, and I propose adding evolved, as a fifth term to the 4E framework. We must, therefore, begin at the beginning, with chemosensation, a sensory modality that underlies purposive behavior, from bacteria to humans. The PROUST hypothesis (perceiving and reconstructing odor utility in space and time) describers how olfaction, this ancient scaffold and common denominator of animal cognition, fulfills the criteria of embodied cognition. Olfactory cognition, with its near universal taxonomic distribution as well as the near absence of conscious representation in humans, may offer us the best sensorimotor system for the study of embodiment.

How the evolution of air breathing shaped hippocampal function.

To make maps from airborne odours requires dynamic respiratory patterns. I propose that this constraint explains the modulation of memory by nasal respiration in mammals, including murine rodents (e.g. laboratory mouse, laboratory rat) and humans. My prior theories of limbic system evolution offer a framework to understand why this occurs. The answer begins with the evolution of nasal respiration in Devonian lobe-finned fishes. This evolutionary innovation led to adaptive radiations in chemosensory systems, including the emergence of the vomeronasal system and a specialization of the main olfactory system for spatial orientation. As mammals continued to radiate into environments hostile to spatial olfaction (air, water), there was a loss of hippocampal structure and function in lineages that evolved sensory modalities adapted to these new environments. Hence the independent evolution of echolocation in bats and toothed whales was accompanied by a loss of hippocampal structure (whales) and an absence of hippocampal theta oscillations during navigation (bats). In conclusion, models of hippocampal function that are divorced from considerations of ecology and evolution fall short of explaining hippocampal diversity across mammals and even hippocampal function in humans. This article is part of the theme issue 'Systems neuroscience through the lens of evolutionary theory'.

Acrobatic squirrels learn to leap and land on tree branches without falling.

Arboreal animals often leap through complex canopies to travel and avoid predators. Their success at making split-second, potentially life-threatening decisions of biomechanical capability depends on their skillful use of acrobatic maneuvers and learning from past efforts. Here, we found that free-ranging fox squirrels (Sciurus niger) leaping across unfamiliar, simulated branches decided where to launch by balancing a trade-off between gap distance and branch-bending compliance. Squirrels quickly learned to modify impulse generation upon repeated leaps from unfamiliar, compliant beams. A repertoire of agile landing maneuvers enabled targeted leaping without falling. Unanticipated adaptive landing and leaping "parkour" behavior revealed an innovative solution for particularly challenging leaps. Squirrels deciding and learning how to launch and land demonstrates the synergistic roles of biomechanics and cognition in robust gap-crossing strategies.

How Ambient Environment Influences Olfactory Orientation in Search and Rescue Dogs.

Under natural conditions, an animal orienting to an air-borne odor plume must contend with the shifting influence of meteorological variables, such as air temperature, humidity, and wind speed, on the location and the detectability of the plume. Despite their importance, the natural statistics of such variables are difficult to reproduce in the laboratory and hence few studies have investigated strategies of olfactory orientation by mobile animals under different meteorological conditions. Using trained search and rescue dogs, we quantified the olfactory orientation behaviors of dogs searching for a trail (aged 1-3 h) of a hidden human subject in a natural landscape, under a range of meteorological conditions. Dogs were highly successful in locating the human target hidden 800 m from the start location (93% success). Humidity and air temperature had a significant effect on search strategy: as air conditions became cooler and more humid, dogs searched significantly closer to the experimental trail. Dogs also modified their speed and head position according to their search location distance from the experimental trail. When close to the trail, dogs searched with their head up and ran quickly but when their search took them farther from the trail, they were more likely to search with their nose to the ground, moving more slowly. This study of a mammalian species responding to localized shifts in ambient conditions lays the foundation for future studies of olfactory orientation, and the development of a highly tractable mammalian species for such research.

The navigational nose: a new hypothesis for the function of the human external pyramid.

One of the outstanding questions in evolution is why Homo erectus became the first primate species to evolve the external pyramid, i.e. an external nose. The accepted hypothesis for this trait has been its role in respiration, to warm and humidify air as it is inspired. However, new studies testing the key assumptions of the conditioning hypothesis, such as the importance of turbulence to enhance heat and moisture exchange, have called this hypothesis into question. The human nose has two functions, however, respiration and olfaction. It is thus also possible that the external nose evolved in response to selection for olfaction. The genus Homo had many adaptations for long-distance locomotion, which allowed Homo erectus to greatly expand its species range, from Africa to Asia. Long-distance navigation in birds and other species is often accomplished by orientation to environmental odors. Such olfactory navigation, in turn, is enhanced by stereo olfaction, made possible by the separation of the olfactory sensors. By these principles, the human external nose could have evolved to separate olfactory inputs to enhance stereo olfaction. This could also explain why nose shape later became so variable: as humans became more sedentary in the Neolithic, a decreasing need for long-distance movements could have been replaced by selection for other olfactory functions, such as detecting disease, that would have been critical to survival in newly dense human settlements.

Caching for where and what: evidence for a mnemonic strategy in a scatter-hoarder.

Scatter-hoarding animals face the task of maximizing retrieval of their scattered food caches while minimizing loss to pilferers. This demand should select for mnemonics, such as chunking, i.e. a hierarchical cognitive representation that is known to improve recall. Spatial chunking, where caches with the same type of content are related to each other in physical location and memory, would be one such mechanism. Here we tested the hypothesis that scatter-hoarding eastern fox squirrels (Sciurus niger) are organizing their caches in spatial patterns consistent with a chunking strategy. We presented 45 individual wild fox squirrels with a series of 16 nuts of four different species, either in runs of four of the same species or 16 nuts offered in a pseudorandom order. Squirrels either collected each nut from a different location or collected all nuts from a single location; we then mapped their subsequent cache distributions using GPS. The chunking hypothesis predicted that squirrels would spatially organize caches by nut species, regardless of presentation order. Our results instead demonstrated that squirrels spatially chunked their caches by nut species but only when caching food that was foraged from a single location. This first demonstration of spatial chunking in a scatter hoarder underscores the cognitive demand of scatter hoarding.

Inaccessibility of reinforcement increases persistence and signaling behavior in the fox squirrel (Sciurus niger).

Under natural conditions, wild animals encounter situations where previously rewarded actions do not lead to reinforcement. In the laboratory, a surprising omission of reinforcement induces behavioral and emotional responses described as frustration. Frustration can lead to aggressive behaviors and to the persistence of noneffective responses, but it may also lead to new behavioral responses to a problem, a potential adaptation. We assessed the responses to inaccessible reinforcement in free-ranging fox squirrels (Sciurus niger). We trained squirrels to open a box to obtain food reinforcement, a piece of walnut. After 9 training trials, squirrels were tested in 1 of 4 conditions: a control condition with the expected reward, an alternative reinforcement (a piece of dried corn), an empty box, or a locked box. We measured the presence of signals suggesting arousal (e.g., tail flags and tail twitches) and found that squirrels performed fewer of these behaviors in the control condition and increased certain behaviors (tail flags, biting box) in the locked box condition, compared to other experimental conditions. When faced with nonreinforcement, that is, frustration, squirrels increased the number of interactions with the apparatus and spent more time interacting with the apparatus. This study of frustration responses in a free-ranging animal extends the conclusions of captive studies to the field and demonstrates that fox squirrels show short-term negatively valenced responses to the inaccessibility, omission, and change of reinforcement. (PsycINFO Database Record

Olfactory Orientation and Navigation in Humans.

Although predicted by theory, there is no direct evidence that an animal can define an arbitrary location in space as a coordinate location on an odor grid. Here we show that humans can do so. Using a spatial match-to-sample procedure, humans were led to a random location within a room diffused with two odors. After brief sampling and spatial disorientation, they had to return to this location. Over three conditions, participants had access to different sensory stimuli: olfactory only, visual only, and a final control condition with no olfactory, visual, or auditory stimuli. Humans located the target with higher accuracy in the olfaction-only condition than in the control condition and showed higher accuracy than chance. Thus a mechanism long proposed for the homing pigeon, the ability to define a location on a map constructed from chemical stimuli, may also be a navigational mechanism used by humans.

Navigation outside of the box: what the lab can learn from the field and what the field can learn from the lab.

Space is continuous. But the communities of researchers that study the cognitive map in non-humans are strangely divided, with debate over its existence found among behaviorists but not neuroscientists. To reconcile this and other debates within the field of navigation, we return to the concept of the parallel map theory, derived from data on hippocampal function in laboratory rodents. Here the cognitive map is redefined as the integrated map, which is a construction of dual mechanisms, one based on directional cues (bearing map) and the other on positional cues (sketch map). We propose that the dual navigational mechanisms of pigeons, the navigational map and the familiar area map, could be homologous to these mammalian parallel maps; this has implications for both research paradigms. Moreover, this has implications for the lab. To create a bearing map (and hence integrated map) from extended cues requires self-movement over a large enough space to sample and model these cues at a high resolution. Thus a navigator must be able to move freely to map extended cues; only then should the weighted hierarchy of available navigation mechanisms shift in favor of the integrated map. Because of the paucity of extended cues in the lab, the flexible solutions allowed by the integrated map should be rare, despite abundant neurophysiological evidence for the existence of the machinery needed to encode and map extended cues through voluntary movement. Not only do animals need to map extended cues but they must also have sufficient information processing capacity. This may require a specific ontogeny, in which the navigator's nervous system is exposed to naturally complex spatial contingencies, a circumstance that occurs rarely, if ever, in the lab. For example, free-ranging, flying animals must process more extended cues than walking animals and for this reason alone, the integrated map strategy may be found more reliably in some species. By taking concepts from ethology and the parallel map theory, we propose a path to directly integrating the three great experimental paradigms of navigation: the honeybee, the homing pigeon and the laboratory rodent, towards the goal of a robust, unified theory of animal navigation.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Fox squirrels match food assessment and cache effort to value and scarcity.

Scatter hoarders must allocate time to assess items for caching, and to carry and bury each cache. Such decisions should be driven by economic variables, such as the value of the individual food items, the scarcity of these items, competition for food items and risk of pilferage by conspecifics. The fox squirrel, an obligate scatter-hoarder, assesses cacheable food items using two overt movements, head flicks and paw manipulations. These behaviors allow an examination of squirrel decision processes when storing food for winter survival. We measured wild squirrels' time allocations and frequencies of assessment and investment behaviors during periods of food scarcity (summer) and abundance (fall), giving the squirrels a series of 15 items (alternating five hazelnuts and five peanuts). Assessment and investment per cache increased when resource value was higher (hazelnuts) or resources were scarcer (summer), but decreased as scarcity declined (end of sessions). This is the first study to show that assessment behaviors change in response to factors that indicate daily and seasonal resource abundance, and that these factors may interact in complex ways to affect food storing decisions. Food-storing tree squirrels may be a useful and important model species to understand the complex economic decisions made under natural conditions.

My owner, right or wrong: the effect of familiarity on the domestic dog's behavior in a food-choice task.

Dogs are strongly influenced by human behavior, and they readily form bonds with specific humans. Yet these lines of inquiry are not often combined. The goal of this study was to investigate whether such bonds would play a role in how dogs behave in response to human signals. Using various types of signals, we compared dogs' use of information from a familiar human (their owner) versus an unfamiliar human when choosing between two food containers. In some conditions, the owner indicated a container that gave food and a stranger indicated a container that did not; in other conditions, this was reversed. Dogs more often chose the container indicated by or nearest to their owner, even when this container never yielded a food reward. In two conditions, dogs chose at chance: a control condition in which both pointers were strangers and a condition in which the owner and stranger sat reading books and provided no social signal. This is the first study to directly compare owners to strangers in a single food-choice situation. Our results suggest that dogs make decisions by attending preferentially to social signals from humans with whom they have become familiar.

Sex differences in memory for landmark arrays in C57BL/J6 mice.

The most robust sex differences in cognition across polygynous mammalian species are the sex-specific patterns of the use of spatial cues during encoding and orientation. In laboratory rats, wild rodents, and humans, females orient preferentially to the features and arrangement of local landmarks, while males preferentially attend to distant landmarks. Yet this sex-specific pattern is often absent or reversed in the laboratory mouse, a species representing a major laboratory model of neural mechanisms. We explored sex differences in the C57BL/J6 strain of laboratory mouse by employing tasks that were motivated by the natural patterns of exploration. We predicted that such tasks would unmask the predicted default polygynous patterns of cue use by females and males. We used two standard tasks, a novel object recognition task and a five-stage serial object dishabituation task. On the first task, the results showed a female advantage in detecting the novel object, as predicted by prior results from other polygynous species. In the second task, we found, also as predicted, a male advantage in performance when the polarization of the array was distorted and a female advantage in performance when the local array was re-arranged. The pattern of sex-specific advantages in performance in C57BL/J6 mouse is thus concordant with that found in other polygynous mammals.

The emergence of flexible spatial strategies in young children.

The development of spatial navigation in children depends not only on remembering which landmarks lead to a goal location but also on developing strategies to deal with changes in the environment or imperfections in memory. Using cue combination methods, the authors examined 3- and 4-year-old children's memory for different types of spatial cues and the spatial strategies that they use when those cues are in conflict. Children were taught to search for a toy in 1 of 4 possible hiding locations. Children were then tested on transformations of the array of locations. The transformations dissociated the different types of cues by putting them in conflict with one another. The authors were especially interested in the use of a majority strategy, by which children choose to search in the location indicated by the greatest number of cue types rather than relying on a preferred cue type. Children's memory for spatial cues and their strategies varied both by age and by experimental setup. In Experiment 1, both 3- and 4-year-old children preferred to use the distinct landmarks coincident with the hiding locations over any other types of cues and showed no use of a majority strategy. However, in Experiment 2, when the coincident landmarks were moved adjacent to the hiding locations, both 3- and 4-year-old children preferred to search in the position of the hiding location relative to the array. Furthermore, 4-year-old children in Experiment 2 showed better memory for individual types of cues and the emergence of a majority strategy.

Deficits in cognition and synaptic plasticity in a mouse model of Down syndrome ameliorated by GABAB receptor antagonists.

Cognitive impairment in Down syndrome (DS) is characterized by deficient learning and memory. Mouse genetic models of DS exhibit impaired cognition in hippocampally mediated behavioral tasks and reduced synaptic plasticity of hippocampal pathways. Enhanced efficiency of GABAergic neurotransmission was implicated in those changes. We have recently shown that signaling through postsynaptic GABA(B) receptors is significantly increased in the dentate gyrus of Ts65Dn mice, a genetic model of DS. Here we examined a role for GABA(B) receptors in cognitive deficits in DS by defining the effect of selective GABA(B) receptor antagonists on behavior and synaptic plasticity of adult Ts65Dn mice. Treatment with the GABA(B) receptor antagonist CGP55845 restored memory of Ts65Dn mice in the novel place recognition, novel object recognition, and contextual fear conditioning tasks, but did not affect locomotion and performance in T-maze. The treatment increased hippocampal levels of brain-derived neurotrophic factor, equally in 2N and Ts65Dn mice. In hippocampal slices, treatment with the GABA(B) receptor antagonists CGP55845 or CGP52432 enhanced long-term potentiation (LTP) in the Ts65Dn DG. The enhancement of LTP was accompanied by an increase in the NMDA receptor-mediated component of the tetanus-evoked responses. These findings are evidence for a contribution of GABA(B) receptors to changes in hippocampal-based cognition in the Ts65Dn mouse. The ability to rescue cognitive performance through treatment with selective GABA(B) receptor antagonists motivates studies to further explore the therapeutic potential of these compounds in people with DS.

From chemotaxis to the cognitive map: the function of olfaction.

A paradox of vertebrate brain evolution is the unexplained variability in the size of the olfactory bulb (OB), in contrast to other brain regions, which scale predictably with brain size. Such variability appears to be the result of selection for olfactory function, yet there is no obvious concordance that would predict the causal relationship between OB size and behavior. This discordance may derive from assuming the primary function of olfaction is odorant discrimination and acuity. If instead the primary function of olfaction is navigation, i.e., predicting odorant distributions in time and space, variability in absolute OB size could be ascribed and explained by variability in navigational demand. This olfactory spatial hypothesis offers a single functional explanation to account for patterns of olfactory system scaling in vertebrates, the primacy of olfaction in spatial navigation, even in visual specialists, and proposes an evolutionary scenario to account for the convergence in olfactory structure and function across protostomes and deuterostomes. In addition, the unique percepts of olfaction may organize odorant information in a parallel map structure. This could have served as a scaffold for the evolution of the parallel map structure of the mammalian hippocampus, and possibly the arthropod mushroom body, and offers an explanation for similar flexible spatial navigation strategies in arthropods and vertebrates.

Sex differences in object recognition are modulated by object similarity.

How females and males differ in performance in object recognition tasks appears to vary among mammalian species, with female superiority found in the laboratory rat and humans but not in the laboratory mouse. Here we assessed sex differences in object recognition in C57BL/J6 mice by varying the similarity between objects to be learned. Females outperformed males in object recognition when the novel object was similar to a previously learned object.

Digit ratio predicts sense of direction in women.

The relative length of the second-to-fourth digits (2D:4D) has been linked with prenatal androgen in humans. The 2D:4D is sexually dimorphic, with lower values in males than females, and appears to correlate with diverse measures of behavior. However, the relationship between digit ratio and cognition, and spatial cognition in particular, has produced mixed results. In the present study, we hypothesized that spatial tasks separating cue conditions that either favored female or male strategies would examine this structure-function correlation with greater precision. Previous work suggests that males are better in the use of directional cues than females. In the present study, participants learned a target location in a virtual landscape environment, in conditions that contained either all directional (i.e., distant or compass bearing) cues, or all positional (i.e., local, small objects) cues. After a short delay, participants navigated back to the target location from a novel starting location. Males had higher accuracy in initial search direction than females in environments with all directional cues. Lower digit ratio was correlated with higher accuracy of initial search direction in females in environments with all directional cues. Mental rotation scores did not correlate with digit ratio in either males or females. These results demonstrate for the first time that a sex difference in the use of directional cues, i.e., the sense of direction, is associated with more male-like digit ratio.

How does cognition evolve? Phylogenetic comparative psychology.

Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.