Pigeons retain partial memories of homing paths years after learning them individually, collectively or culturally.

Memory of past experience is central to many animal decisions, but how long specific memories can influence behaviour is poorly understood. Few studies have reported memories retrieved after several years in non-human animals, especially for spatial tasks, and whether the social context during learning could affect long-term memory retention. We investigated homing pigeons' spatial memory by GPS-recording their homing paths from a site 9 km from their loft. We compared solo flights of naive pigeons with those of pigeons that had last homed from this site 3-4 years earlier, having learnt a homing route either alone (individual learning), together with a naive partner (collective learning) or within cultural transmission chains (cultural learning). We used as a control a second release site unfamiliar to all pigeons. Pigeons from all learning treatments outperformed naive birds at the familiar (but not the unfamiliar) site, but the idiosyncratic routes they formerly used several years before were now partially forgotten. Our results show that non-human animals can use their memory to solve a spatial task years after they last performed it, irrespective of the social context during learning. They also suggest that without reinforcement, landmarks and culturally acquired 'route traditions' are gradually forgotten.

Division of labour promotes the spread of information in colony emigrations by the ant Temnothorax rugatulus.

The fitness of group-living animals often depends on how well members share information needed for collective decision-making. Theoretical studies have shown that collective choices can emerge in a homogeneous group of individuals following identical rules, but real animals show much evidence for heterogeneity in the degree and nature of their contribution to group decisions. In social insects, for example, the transmission and processing of information is influenced by a well-organized division of labour. Studies that accurately quantify how this behavioural heterogeneity affects the spread of information among group members are still lacking. In this paper, we look at nest choices during colony emigrations of the ant Temnothorax rugatulus and quantify the degree of behavioural heterogeneity of workers. Using clustering methods and network analysis, we identify and characterize four behavioural castes of workers-primary, secondary, passive and wandering-covering distinct roles in the spread of information during an emigration. This detailed characterization of the contribution of each worker can improve models of collective decision-making in this species and promises a deeper understanding of behavioural variation at the colony level.

Route learning during tandem running in the rock ant Temnothorax albipennis.

Many animals use information from conspecifics to change their behavior in adaptive ways. When a rock ant, Temnothorax albipennis, finds food, she returns to her colony and uses a method called tandem running to lead nestmates, one at a time, from the nest to the food. In this way, naive ants can learn the location of a food source. Less clear is whether they also learn navigational cues that guide them from nest to food, although this is often assumed. We tested this idea by tracing the routes of individually marked ants as they followed tandem runs to a feeder, returned to the nest, and later traveled independently back to the food. Our results show, for the first time, that tandem run followers learn specific routes from their leaders. Independent journeys back to the food source were significantly more similar to the routes on which the ants had been led, compared with the routes taken by other tandem runs. In contrast, the homeward journey did not resemble the tandem run route. These results are consistent with followers memorizing visual cues during the tandem run that are useful for recapitulating the outward journey, but not as effective when facing in the opposite direction on the homeward journey. We further showed that foraging routes improved through individual experience over multiple trips but not through the social transfer of route information via tandem running. We discuss our findings in relation to social learning and integration of individual and social information in ants.

Rational time investment during collective decision making in Temnothorax ants.

The study of rational choice in humans and other animals typically focuses on decision outcomes, but rationality also applies to decision latencies, especially when time is scarce and valuable. For example, the smaller the difference in quality between two options, the faster a rational actor should decide between them. This is because the consequences of choosing the inferior option are less severe if the options are similar. Experiments have shown, however, that humans irrationally spend more time choosing between similar options. In this study, we assessed the rationality of time investment during nest-site choice by the rock ant, Temnothorax albipennis. Previous studies have shown that collective decision-making allows ant colonies to avoid certain irrational errors. Here we show that the same is true for time investment. Individual ants, like humans, irrationally took more time to complete an emigration when choosing between two similar nests than when choosing between two less similar nests. Whole colonies, by contrast, rationally made faster decisions when the options were more similar. We discuss the underlying mechanisms of decision-making in individuals and colonies and how they lead to irrational and rational time investment, respectively.

The Psychology of Superorganisms: Collective Decision Making by Insect Societies.

Under the superorganism concept, insect societies are so tightly integrated that they possess features analogous to those of single organisms, including collective cognition. If so, colony function might fruitfully be studied using methods developed to understand individual animals. Here, we review research that uses psychological approaches to understand decision making by colonies. The application of neural models to collective choice shows fundamental similarities between how brains and colonies balance speed/accuracy trade-offs in decision making. Experimental analyses have explored collective rationality, cognitive capacity, and perceptual discrimination at both individual and colony levels. A major theme is the emergence of improved colony-level function from interactions among relatively less capable individuals. However, colonies also encounter performance costs due to their reliance on positive feedback, which generates consensus but can also amplify errors. Collective learning is a nascent field for the further application of psychological methods to colonies. The research strategy reviewed here shows how the superorganism concept can serve as more than an illustrative analogy.

Head-mounted sensors reveal visual attention of free-flying homing pigeons.

Gaze behavior offers valuable insights into attention and cognition. However, technological limitations have prevented the examination of animals' gaze behavior in natural, information-rich contexts; for example, during navigation through complex environments. Therefore, we developed a lightweight custom-made logger equipped with an inertial measurement unit (IMU) and GPS to simultaneously track the head movements and flight trajectories of free-flying homing pigeons. Pigeons have a limited range of eye movement, and their eye moves in coordination with their head in a saccadic manner (similar to primate eye saccades). This allows head movement to act as a proxy for visual scanning behavior. Our IMU sensor recorded the 3D movement of the birds' heads in high resolution, allowing us to reliably detect distinct saccade signals. The birds moved their head far more than necessary for maneuvering flight, suggesting that they actively scanned the environment. This movement was predominantly horizontal (yaw) and sideways (roll), allowing them to scan the environment with their lateral visual field. They decreased their head movement when they flew solo over prominent landmarks (major roads and a railway line) and also when they flew in pairs (especially when flying side by side, with the partner maintained in their lateral visual field). Thus, a decrease in head movement indicates a change in birds' focus of attention. We conclude that pigeons use their head gaze in a task-related manner and that tracking flying birds' head movement is a promising method for examining their visual attention during natural tasks.

A Simple Behavioral Model Predicts the Emergence of Complex Animal Hierarchies.

Social dominance hierarchies are widespread, but little is known about the mechanisms that produce nonlinear structures. In addition to despotic hierarchies, where a single individual dominates, shared hierarchies exist, where multiple individuals occupy a single rank. In vertebrates, these complex dominance relationships are thought to develop from interactions that require higher cognition, but similar cases of shared dominance have been found in social insects. Combining empirical observations with a modeling approach, we show that all three hierarchy structures-linear, despotic, and shared-can emerge from different combinations of simple interactions present in social insects. Our model shows that a linear hierarchy emerges when a typical winner-loser interaction (dominance biting) is present. A despotic hierarchy emerges when a policing interaction is added that results in the complete loss of dominance status for an attacked individual (physical policing). Finally, a shared hierarchy emerges with the addition of a winner-winner interaction that results in a positive outcome for both interactors (antennal dueling). Antennal dueling is an enigmatic ant behavior that has previously lacked a functional explanation. These results show how complex social traits can emerge from simple behaviors without requiring advanced cognition.

Ant colonies outperform individuals when a sensory discrimination task is difficult but not when it is easy.

"Collective intelligence" and "wisdom of crowds" refer to situations in which groups achieve more accurate perception and better decisions than solitary agents. Whether groups outperform individuals should depend on the kind of task and its difficulty, but the nature of this relationship remains unknown. Here we show that colonies of Temnothorax ants outperform individuals for a difficult perception task but that individuals do better than groups when the task is easy. Subjects were required to choose the better of two nest sites as the quality difference was varied. For small differences, colonies were more likely than isolated ants to choose the better site, but this relationship was reversed for large differences. We explain these results using a mathematical model, which shows that positive feedback between group members effectively integrates information and sharpens the discrimination of fine differences. When the task is easier the same positive feedback can lock the colony into a suboptimal choice. These results suggest the conditions under which crowds do or do not become wise.

A context-dependent alarm signal in the ant Temnothorax rugatulus.

Because collective cognition emerges from local signaling among group members, deciphering communication systems is crucial to understanding the underlying mechanisms. Alarm signals are widespread in the social insects and can elicit a variety of behavioral responses to danger, but the functional plasticity of these signals has not been well studied. Here we report an alarm pheromone in the ant Temnothorax rugatulus that elicits two different behaviors depending on context. When an ant was tethered inside an unfamiliar nest site and unable to move freely, she released a pheromone from her mandibular gland that signaled other ants to reject this nest as a potential new home, presumably to avoid potential danger. When the same pheromone was presented near the ants' home nest, they were instead attracted to it, presumably to respond to a threat to the colony. We used coupled gas chromatography/mass spectrometry to identify candidate compounds from the mandibular gland and tested each one in a nest choice bioassay. We found that 2,5-dimethylpyrazine was sufficient to induce rejection of a marked new nest and also to attract ants when released at the home nest. This is the first detailed investigation of chemical communication in the leptothoracine ants. We discuss the possibility that this pheromone's deterrent function can improve an emigrating colony's nest site selection performance.

Paint marking using CO2 anaesthetization does not affect exploratory and recruitment behaviours in the rock ant, Temnothorax rugatulus.

The study of animal behaviour sometimes requires unique identification of individuals, especially in the study of social behaviours involving the interactions of multiple individuals. To this end, researchers have developed many different methods of marking individuals. For small animals like insects, paint marks are often applied to their bodies by anaesthetizing them using low temperature or carbon dioxide. Despite this procedure being ubiquitous when studying social insects, the effect of paint and anaesthetics on their behaviour has not been well investigated, especially their effect on performance during a collective task. In our study, we investigate how paint marks and anaesthetics affect the movement and recruitment behaviours of the ant Temnothorax rugatulus in a house hunting context. We painted two thirds of colony members, half of them using CO2 and the other half using low temperature as methods of anaesthetization, and left the one third unpainted as a control group. We then measured their exploratory behaviour prior to house hunting and their recruitment behaviours during house hunting. We found that neither paint marks nor anaesthetics reduce activity levels of these behaviours. However, low-temperature anaesthetized ants performed a higher number of recruitment behaviours than control ants. Because CO2 anaesthetized ants performed all tasks at the same level as control ants, our data suggest that this is a good technique for paint marking ants, especially T. rugatulus. This is the first study empirically testing negative effects of paint marking on individual and collective outcomes in social insects. Our study represents an important step towards routine validation of individual identification methods used in the study of animal behaviour.

Factors Affecting Outcomes of Poor-Grade Subarachnoid Hemorrhage.

OBJECTIVE: Poor-grade subarachnoid hemorrhage (SAH) accounts for 20% of all SAH and is associated with poor outcomes. The first step in improving outcomes is to analyze the factors that contribute to poor outcomes. METHODS: This was a multicenter, retrospective, observational, cohort study. Data fields included demographic, clinical, radiological, and outcome data for all spontaneous patients with SAH treated at 4 hospitals in Aomori Prefecture in Japan. Patients with modified Rankin Scale score 0-2 at discharge were defined as the good outcome group, and those with modified Rankin Scale score 3-6 were defined as the poor outcome group, and comparisons were made between the 2 groups. RESULTS: There were 329 eligible patients with poor-grade SAH, 41 with good outcome group, and 288 with poor outcome group. On multivariate analysis of the outcome, conservative treatment (P < 0.001), Fisher group 4 (P < 0.007), age ≥65 years (P = 0.011), and Hunt and Kosnik grade V on admission (P = 0.021) were significant factors contributing to a poor outcome. CONCLUSIONS: Nonelderly patients who are not in grade V and Fisher group 4 should undergo aneurysm treatment as soon as possible because they are more likely to have a good outcome, whereas elderly patients in grade V and Fisher group 4 are unlikely to benefit from aneurysm treatment at present. The development of a treatment for early brain injury may be important to improve the outcomes of patients with poor-grade SAH.

Ants learn to rely on more informative attributes during decision-making.

Evolutionary theory predicts that animals act to maximize their fitness when choosing among a set of options, such as what to eat or where to live. Making the best choice is challenging when options vary in multiple attributes, and animals have evolved a variety of heuristics to simplify the task. Many of these involve ranking or weighting attributes according to their importance. Because the importance of attributes can vary across time and place, animals might benefit by adjusting weights accordingly. Here, we show that colonies of the ant Temnothorax rugatulus use their experience during nest site selection to increase weights on more informative nest attributes. These ants choose their rock crevice nests on the basis of multiple features. After exposure to an environment where only one attribute differentiated options, colonies increased their reliance on this attribute relative to a second attribute. Although many species show experience-based changes in selectivity based on a single feature, this is the first evidence in animals for adaptive changes in the weighting of multiple attributes. These results show that animal collectives, like individuals, change decision-making strategies according to experience. We discuss how these colony-level changes might emerge from individual behaviour.

Is collective nest site selection in ants influenced by the anchoring effect?

Evolutionary theory predicts that animals make decisions that maximize fitness. If so, they are expected to adhere to principles of rational choice, which a decision-maker must follow to reliably maximize net benefit. For example, evaluation of an option should not be influenced by the quality of other unchosen options. However, humans and other animals are known to evaluate a mediocre option more favorably after encountering poor options than after encountering no options, a phenomenon known as the 'anchoring effect'. Rationality is also expected in the consensus decisions of animal societies, but the anchoring effect has not previously been tested in that context. Here we show that colonies of the rock ant, Temnothorax rugatulus, demonstrate the anchoring effect during nest site selection - colonies moved more readily from a mediocre nest to a good nest when exposed to poor nests than when exposed to mediocre nests. This effect depended on both current conditions and past experience; movement probability was affected only when colonies were exposed to surrounding nests before and during the emigration. The effect was small, reaching statistical significance in only one of two experimental replicates. We discuss possible mechanisms and ultimate explanations for why colonies show this seemingly suboptimal behavior.

Mechanisms of collective learning: how can animal groups improve collective performance when repeating a task?

Learning is ubiquitous in animals: individuals can use their experience to fine-tune behaviour and thus to better adapt to the environment during their lifetime. Observations have accumulated that, at the collective level, groups can also use their experience to improve collective performance. Yet, despite apparent simplicity, the links between individual learning capacities and a collective's performance can be extremely complex. Here we propose a centralized and broadly applicable framework to begin classifying this complexity. Focusing principally on groups with stable composition, we first identify three distinct ways through which groups can improve their collective performance when repeating a task: each member learning to better solve the task on its own, members learning about each other to better respond to one another and members learning to improve their complementarity. We show through selected empirical examples, simulations and theoretical treatments that these three categories identify distinct mechanisms with distinct consequences and predictions. These mechanisms extend well beyond current social learning and collective decision-making theories in explaining collective learning. Finally, our approach, definitions and categories help generate new empirical and theoretical research avenues, including charting the expected distribution of collective learning capacities across taxa and its links to social stability and evolution. This article is part of a discussion meeting issue 'Collective behaviour through time'.

Verification of a Three-day Hospitalization Protocol for Chronic Subdural Hematoma Surgery.

Chronic subdural hematoma (CSH) is predominantly a disease of the elderly. Aging societies in advanced countries are seeing the number of CSH cases increasing. We applied a three-day hospitalization protocol for CSH surgery to reduce healthcare costs and more efficiently manage hospital beds. We investigated the clinical factors that influenced prolonged hospitalization. From January 2015 to December 2020, we performed irrigation, evacuation, and drainage of CSH cases in 221 consecutive patients. The χ2 test and logistic regression analysis were conducted to detect clinical factors influencing prolonged hospitalization. A p-value below 0.05 was considered statistically significant. Applying a three-day hospitalization protocol showed no adverse outcomes. Fifty-two (24%) of 221 patients experienced prolonged hospitalization. The χ2 test showed that female gender, atrial fibrillation, alcohol abuse, preoperative consciousness level, verbal function disturbance, and perioperative activities of daily living were significantly related to prolonged hospitalization. Female gender, atrial fibrillation, and alcohol abuse were significant factors in the logistic regression analysis. A three-day hospitalization protocol for CSH is suitable for patient care; however, particular attention needs to be focused on the female gender, atrial fibrillation, and alcohol abuse, all three of which prolong hospitalization.

Spontaneous remission of skull Langerhans cell histiocytosis that had developed by repeated head injury: illustrative case.

BACKGROUND: Langerhans cell histiocytosis (LCH) was previously characterized as the proliferation of Langerhans-type histiocytes with a wide range of clinical presentations that arise mostly in children. The typical presentation is a gradually enlarging, painless skull mass. Rapid clinical deterioration is rare. OBSERVATIONS: A 3-year-old boy who had incurred a right frontal impact head injury demonstrated no apparent neurological deficits. He subsequently bruised the same region multiple times. The right frontal swelling gradually increased over the course of 6 days after the initial injury. Skull radiography showed no bony lesion. The same site enlarged markedly 12 days after the initial injury. Magnetic resonance imaging revealed a frontal bony tumorous lesion associated with multiple subcutaneous cystic mass lesions. The patient underwent open biopsy of the skull lesion and evacuation of the subcutaneous lesions. Histopathological examination confirmed the diagnosis of LCH. Immunohistochemical evaluation revealed positivity for CD1a and langerin and no immunopositivity for BRAF V600E. The skull lesion spontaneously disappeared 30 days after the biopsy without recurrence. LESSONS: Physicians should be aware of this rare clinical manifestation of LCH that developed by a repeat head injury.

Empirical test of the many-wrongs hypothesis reveals weighted averaging of individual routes in pigeon flocks.

The 'many-wrongs hypothesis' predicts that groups improve their decision-making performance by aggregating members' diverse opinions. Although this has been considered one of the major benefits of collective movement and migration, whether and how multiple inputs are in fact aggregated for superior directional accuracy has not been empirically verified in non-human animals. Here we showed that larger homing pigeon flocks had significantly more efficient (i.e. shorter) homing routes than smaller flocks, consistent with previous findings and with the predictions of the many-wrongs hypothesis. However, detailed analysis showed that flock routes were not simply averages of individual routes, but instead that pigeons that more faithfully recapitulated their routes during individual flights had a proportionally greater influence on their flocks' routes. We discuss the implications of our results for possible mechanisms of collective learning as well as for the definition of leadership in animals solving navigational tasks collectively.

Chronic Subdural Hematoma, Caused by Disseminated Intravascular Coagulation and/or Anticoagulation Therapy, after COVID-19.

Chronic subdural hematoma (CSDH) typically develops in the supratentorial region in elderly patients. We treated a case of unilateral supratentorial and bilateral infratentorial CSDH, whereby the patient had a coronavirus disease 2019 (COVID-19) infection combined with disseminated intravascular coagulation 2 months earlier. The patient had not experienced any head trauma before the onset of the CSDH. The postoperative course was uneventful, and the patient experienced no neurological deficit. We propose that we should be aware not only of acute ischemic or hemorrhagic diseases after COVID-19 infection but also of chronic subdural hematoma caused by coagulopathy after a COVID-19 infection.

Oxidative Stress Mediates Vascular Tortuosity.

Vascular tortuosity is associated with various disorders and is being increasingly detected through advances in imaging techniques. The underlying mechanisms for vascular tortuosity, however, remain unclear. Here, we tested the hypothesis that oxidative stress mediates the generation of tortuous vessels. We used the bilateral common carotid artery (CCA) ligation model to induce vascular tortuosity. Both young and adult rats showed basilar artery tortuous morphological changes one month after bilateral CCA ligation. These tortuous changes were permanent but more pronounced in the adult rats. Microarray and real-time PCR analysis revealed that these tortuous changes were accompanied by the induction of oxidative stress-related genes. Moreover, the indicated model in rabbits showed that tortuous morphological changes to the basilar artery were suppressed by antioxidant treatment. These results are highly suggestive of the significance of oxidative stress in the development of vascular tortuosity. Although further studies will be needed to elucidate the possible mechanisms by which oxidative stress enhances vascular tortuosity, our study also points toward possible prophylaxis and treatment for vascular tortuosity.

Naïve individuals promote collective exploration in homing pigeons.

Group-living animals that rely on stable foraging or migratory routes can develop behavioural traditions to pass route information down to inexperienced individuals. Striking a balance between exploitation of social information and exploration for better alternatives is essential to prevent the spread of maladaptive traditions. We investigated this balance during cumulative route development in the homing pigeon Columba livia. We quantified information transfer within pairs of birds in a transmission-chain experiment and determined how birds with different levels of experience contributed to the exploration-exploitation trade-off. Newly introduced naïve individuals were initially more likely to initiate exploration than experienced birds, but the pair soon settled into a pattern of alternating leadership with both birds contributing equally. Experimental pairs showed an oscillating pattern of exploration over generations that might facilitate the discovery of more efficient routes. Our results introduce a new perspective on the roles of leadership and information pooling in the context of collective learning.