Wild raccoons demonstrate flexibility and individuality in innovative problem-solving.

Cognitive skills, such as innovative problem-solving, are hypothesized to aid animals in urban environments. However, the significance of innovation in wild populations, and its expression across individuals and socio-ecological conditions, is poorly understood. To identify how and when innovation arises in urban-dwelling species, we used advanced technologies and new testing and analytical methods to evaluate innovative problem-solving abilities of wild raccoons (Procyon lotor). We deployed multi-compartment puzzle boxes with either one or multiple solution types and identified raccoons using radio frequency identification. Raccoons solved these novel extractive foraging tasks, and their success was influenced by age and exploratory diversity. Successful raccoons always discovered multiple different solution types, highlighting flexible problem-solving. Using a unique, comparative sequence analysis approach, we found that variation in raccoon solving techniques was greater between individuals than within individuals, and this self-similarity intensified during times of competition. Finally, the inclusion of an easier solution in the multi-solution trials enabled previously unsuccessful raccoons to bootstrap their learning and successfully open multiple difficult solutions. Our study suggests that innovative problem-solving is probably influenced by many factors and has provided novel field and analytical methods, as well as new insights on the socio-ecological dynamics of urban populations.

Innovative problem-solving in a small, wild canid.

Innovation - the ability to solve problems in a novel way - is not only associated with cognitive abilities and relative brain size, but also by noncognitive traits, such as personality and motivation. We used a novel foraging task with three access options to determine how neophobia, exploration, and persistence influence innovation in 12 habituated bat-eared foxes (Otocyon megalotis) in the Kalahari Desert. Bat-eared foxes offer a unique system to understand cognition as they have the smallest relative brain size of measured canids and a specialized, termite-based diet, yet have displayed foraging innovations. Interestingly, most of our individuals solved the task at least once and six individuals solved the task in every trial. Neophobia did not influence success on the first trial, but both exploration and persistence influenced success across all trials. Those individuals that solved the puzzle over multiple trials became faster over time, suggesting that they learned how to open the box more efficiently. We found some variation in the method to open the puzzle box with six individuals solving the puzzle using two methods and one individual using all three methods. This is the first study to show innovation in a novel foraging task in wild bat-eared foxes.

Manipulating actions: A selective two-option device for cognitive experiments in wild animals.

Advances in biologging technologies have significantly improved our ability to track individual animals' behaviour in their natural environment. Beyond observations, automation of data collection has revolutionized cognitive experiments in the wild. For example, radio-frequency identification (RFID) antennae embedded in 'puzzle box' devices have allowed for large-scale cognitive experiments where individuals tagged with passive integrated transponder (PIT) tags interact with puzzle boxes to gain a food reward, with devices logging both the identity and solving action of visitors. Here, we extended the scope of wild cognitive experiments by developing a fully automated selective two-option foraging device to specifically control which actions lead to a food reward and which remain unrewarded. Selective devices were based on a sliding-door foraging puzzle, and built using commercially available low-cost electronics. We tested it on two free-ranging PIT-tagged subpopulations of great tits Parus major as a proof of concept. We conducted a diffusion experiment where birds learned from trained demonstrators to get a food reward by sliding the door either to the left or right. We then restricted access of knowledgeable birds to their less preferred side and calculated the latency until birds produced solutions as a measure of behavioural flexibility. A total of 22 of 23 knowledgeable birds produced at least one solution on their less preferred side after being restricted, with higher-frequency solvers being faster at doing so. In addition, 18 of the 23 birds reached their solving rate from prior to the restriction on their less preferred side, with birds with stronger prior side preference taking longer to do so. We therefore introduce and successfully test a new selective two-option puzzle box, providing detailed instructions and freely available software that allows reproducibility. It extends the functionality of existing systems by allowing fine-scale manipulations of individuals' actions and opens a large range of possibilities to study cognitive processes in wild animal populations.

Selection of Laboratory Mice for the Cognitive Task Successful Solution and for the Inability to Solve It.

Using the selected mouse strain EX as the founding population (selection for extrapolation ability) three selection generations of mice were obtained, which were selected for successful solution of object permanence test (plus-sub-strain) and for lack of such solution (minus-sub-strain). The successful solution required not only the ability to operate the object permanence rule (by J. Piajet), but the performance of complicated action (executive function) which was significantly higher in plus-substrain, and this is the unique example of successful selection for cognitive trait.

The development of a cognitive rehabilitation task for mice.

Obesity, neurodegenerative diseases, and injury can all lead to cognitive deficits, which can be improved clinically with the implementation of cognitive rehabilitation. Due to a lack of effective cognitive rehabilitation tools in mice, we re-designed a cognitive task utilized to detect problem-solving deficits, to develop a cognitive rehabilitation paradigm for mice. In this study, we developed a modified the Puzzle Box task by exposing B6 mice to a variety of obstacles and assessing the escape latencies. We then combined obstacles in order to create a "complex obstacle" for the problem-solving task. We determined that our task was reproducible in different cohorts of mice. Furthermore, with repetition the mice display an improvement in the performance, evident by a shorter escape latency and the ability to maintain this improvement in performance, indicative of long-term memory. Given that this approach is new, we validated whether this task could successfully detect deficits in a mouse model of cognitive impairment, the high-fat diet mouse. We demonstrate that high-fat diet mice have longer escape latencies when exposed to the complex obstacle compared to standard diet control mice. Taken together, these data suggest that the Puzzle Box is a valid task for cognitive rehabilitation in mice.

Selection of Mice for Object Permanence Cognitive Task Solution.

The selection of mice for high ("plus") and low ("minus") scores in the puzzle-box test was performed over five generations. This test evaluates the success (or failure) in finding the underpass, leading to the dark part of the box, when it is blocked. This means that the mouse is either able or unable to operate the "object permanence rule" (one of the index's cognitive abilities). For the "+" strain, animals were bred who solved the test when the underpass test blocked with a plug; the "-" strain comprised those who were unable to solve this task. In mice of the "+" strain, the proportion of animals that was able to solve "plug" stages of the test was higher than in the "-" strain and in the non-selected genetically heterogeneous population. The "+" mice ate significantly more new food in the hyponeophagia test. Animals of both strains demonstrated the ability to "manipulate" the plug blocking the underpass, touching the plug with their paws and muzzle, although the majority of "-" mice were unable to open the underpass effectively. Thus, mice of both selected strains demonstrated that they were able to understand that the underpass does exist, but only "+"-strain animals (at least the majority of them) were able to realize the solution. The selection for plug-stage solution success affected the mouse's ability to open the hidden underpass.

Scavenging vs hunting affects behavioral traits of an opportunistic carnivore.

Background: Human-induced changes to ecosystems transform the availability of resources to predators, including altering prey populations and increasing access to anthropogenic foods. Opportunistic predators are likely to respond to altered food resources by changing the proportion of food they hunt versus scavenge. These shifts in foraging behavior will affect species interactions through multiple pathways, including by changing other aspects of predator behavior such as boldness, innovation, and social structure. Methods: To understand how foraging behavior impacts predator behavior, we conducted a controlled experiment to simulate hunting by introducing a prey model to captive coyotes (Canis latrans) and compared their behavior to coyotes that continued to scavenge over one year. We used focal observations to construct behavioral budgets, and conducted novel object, puzzle box, and conspecific tests to evaluate boldness, innovation, and response to conspecifics. Results: We documented increased time spent resting by hunting coyotes paired with decreased time spent active. Hunting coyotes increased boldness and persistence but there were no changes in innovation. Our results illustrate how foraging behavior can impact other aspects of behavior, with potential ecological consequences to predator ecology, predator-prey dynamics, and human-wildlife conflict; however, the captive nature of our study limits specific conclusions related to wild predators. We conclude that human-induced behavioral changes could have cascading ecological implications that are not fully understood.

Abnormal sensory perception masks behavioral performance of Grin1 knockdown mice.

The development and function of sensory systems require intact glutamatergic neurotransmission. Changes in touch sensation and vision are common symptoms in autism spectrum disorders, where altered glutamatergic neurotransmission is strongly implicated. Further, cortical visual impairment is a frequent symptom of GRIN disorder, a rare genetic neurodevelopmental disorder caused by pathogenic variants of GRIN genes that encode NMDA receptors. We asked if Grin1 knockdown mice (Grin1KD), as a model of GRIN disorder, had visual impairments resulting from NMDA receptor deficiency. We discovered that Grin1KD mice had deficient visual depth perception in the visual cliff test. Since Grin1KD mice are known to display robust changes in measures of learning, memory, and emotionality, we asked whether deficits in these higher-level processes could be partly explained by their visual impairment. By changing the experimental conditions to improve visual signals, we observed significant improvements in the performance of Grin1KD mice in tests that measure spatial memory, executive function, and anxiety. We went further and found destabilization of the outer segment of retina together with the deficient number and size of Meissner corpuscles (mechanical sensor) in the hind paw of Grin1KD mice. Overall, our findings suggest that abnormal sensory perception can mask the expression of emotional, motivational and cognitive behavior of Grin1KD mice. This study demonstrates new methods to adapt routine behavioral paradigms to reveal the contribution of vision and other sensory modalities in cognitive performance.

Trisomy of Human Chromosome 21 Orthologs Mapping to Mouse Chromosome 10 Cause Age and Sex-Specific Learning Differences: Relevance to Down Syndrome.

Down syndrome (DS), trisomy of human chromosome 21 (Hsa21), is the most common genetic cause of intellectual disability. The Dp10(1)Yey (Dp10) is a mouse model of DS that is trisomic for orthologs of 25% of the Hsa21 protein-coding genes, the entirety of the Hsa21 syntenic region on mouse chromosome 10. Trisomic genes include several involved in brain development and function, two that modify and regulate the activities of sex hormones, and two that produce sex-specific phenotypes as null mutants. These last four are the only Hsa21 genes with known sexually dimorphic properties. Relatively little is known about the potential contributions to the DS phenotype of segmental trisomy of Mmu10 orthologs. Here, we have tested separate cohorts of female and male Dp10 mice, at 3 and 9 months of age, in an open field elevated zero maze, rotarod, and balance beam, plus the learning and memory tasks, spontaneous alternation, puzzle box, double-H maze, context fear conditioning, and acoustic startle/prepulse inhibition, that depend upon the function of the prefrontal cortex, striatum, hippocampus, and cerebellum. We show that there are age and sex-specific differences in strengths and weaknesses, suggesting that genes within the telomere proximal region of Hsa21 influence the DS phenotype.

Linking Human Perceptions and Spotted Hyena Behavior in Urban Areas of Ethiopia.

Humans have shaped carnivore behavior since at least the Middle Paleolithic period, about 42,000 years ago. In more recent times, spotted hyenas (Crocuta crocuta) in Ethiopia have adapted to living in urban areas, while humans have adapted to living with hyenas. Yet, relationships between coexisting humans and carnivores are rarely addressed beyond mitigating conflicts. We provided a case study for how to broadly think about coexistence and how to study it when measuring if humans and carnivores affect one another. We collected data in four Ethiopian cities: Mekelle, Harar, Addis Ababa, and Arba Minch. We held focus groups and key informant interviews that incorporated feedback from 163 people, representing a wide array of religious, economic, and educational backgrounds. We also determined how many hyenas resided in these cities, hyena behavioral responses to humans using a flight initiation test, and problem-solving abilities via puzzle box trials. We found that in three of the cities, hyenas and humans coexist at high densities and frequently encounter each other. While all participants recognized the importance of hyenas as scavengers to maintain a clean environment, there was pronounced variation in cultural perspectives across cities. For example, while the people of Harar revere hyenas in spiritual terms, in Arba Minch hyenas were regarded as nuisance animals. Hyenas were universally respected as a formidable predator across cities but reports of attacks on livestock and humans were few. Flight initiation tests revealed hyenas fled at significantly closer distances in Harar and Addis Ababa than in Mekelle. Hyenas succeeded at solving a puzzle box in Harar but not in Mekelle. These variable behavior in hyenas correlated to different human perceptions. Our case study results suggest that the hyena-human dynamic is highly variable across these locations. We conclude by exploring the implications of these findings for how humans and hyenas can shape one another's behavior. Developing studies to link human perceptions and animal behavior could advance wildlife conservation, especially in urban areas.