Conceptual learning by miniature brains

Concepts act as a cornerstone of human cognition. Humans and non-human primates learn conceptual relationships such as ‘same’, ‘different’, ‘larger than’, ‘better than’, among others. In all cases, the relationships have to be encoded by the brain independently of the physical nature of objects linked by the relation. Consequently, concepts are associated with high levels of cognitive sophistication and are not expected in an insect brain. Yet, various works have shown that the miniature brain of honeybees rapidly learns conceptual relationships involving visual stimuli. Concepts such as ‘same’, ‘different’, ‘above/below of’ or ‘left/right are well mastered by bees. We review here evidence about concept learning in honeybees and discuss both its potential adaptive advantage and its possible neural substrates. The results reviewed here challenge the traditional view attributing supremacy to larger brains when it comes to the elaboration of concepts and have wide implications for understanding how brains can form conceptual relations.     

Predator crypsis enhances behaviourally mediated indirect effects on plants by altering bumblebee foraging preferences

Predators of pollinators can influence pollination services and plant fitness via both consumptive (reducing pollinator density) and non-consumptive (altering pollinator behaviour) effects. However, a better knowledge of the mechanisms underlying behaviourally mediated indirect effects of predators is necessary to properly understand their role in community dynamics. We used the tripartite relationship between bumblebees, predatory crab spiders and flowers to ask whether behaviourally mediated effects are localized to flowers harbouring predators, or whether bees extend their avoidance to entire plant species. In a tightly controlled laboratory environment, bumblebees (Bombus terrestris) were exposed to a random mixture of equally rewarding yellow and white artificial flowers, but foraging on yellow flowers was very risky: bees had a 25 per cent chance of receiving a simulated predation attempt by ‘robotic’ crab spiders. As bees learnt to avoid ‘dangerous’ flowers, their foraging preferences changed and they began to visit fewer yellow flowers than expected by chance. Bees avoided spider-free yellow flowers as well as dangerous yellow flowers when spiders were more difficult to detect (the colour of yellow spiders was indistinguishable from that of yellow flowers). Therefore, this interaction between bee learning and predator crypsis could lead flower species harbouring cryptic predators to suffer from reduced reproductive success.     

How Lateral Connections and Spiking Dynamics May Separate Multiple Objects Moving Together

Over successive stages, the ventral visual system of the primate brain develops neurons that respond selectively to particular objects or faces with translation, size and view invariance. The powerful neural representations found in Inferotemporal cortex form a remarkably rapid and robust basis for object recognition which belies the difficulties faced by the system when learning in natural visual environments. A central issue in understanding the process of biological object recognition is how these neurons learn to form separate representations of objects from complex visual scenes composed of multiple objects. We show how a one-layer competitive network comprised of ‘spiking’ neurons is able to learn separate transformation-invariant representations (exemplified by one-dimensional translations) of visual objects that are always seen together moving in lock-step, but separated in space. This is achieved by combining ‘Mexican hat’ functional lateral connectivity with cell firing-rate adaptation to temporally segment input representations of competing stimuli through anti-phase oscillations (perceptual cycles). These spiking dynamics are quickly and reliably generated, enabling selective modification of the feed-forward connections to neurons in the next layer through Spike-Time-Dependent Plasticity (STDP), resulting in separate translation-invariant representations of each stimulus. Variations in key properties of the model are investigated with respect to the network’s ability to develop appropriate input representations and subsequently output representations through STDP. Contrary to earlier rate-coded models of this learning process, this work shows how spiking neural networks may learn about more than one stimulus together without suffering from the ‘superposition catastrophe’. We take these results to suggest that spiking dynamics are key to understanding biological visual object recognition.     

How (and why) the visual control of action differs from visual perception

Vision not only provides us with detailed knowledge of the world beyond our bodies, but it also guides our actions with respect to objects and events in that world. The computations required for vision-for-perception are quite different from those required for vision-for-action. The former uses relational metrics and scene-based frames of reference while the latter uses absolute metrics and effector-based frames of reference. These competing demands on vision have shaped the organization of the visual pathways in the primate brain, particularly within the visual areas of the cerebral cortex. The ventral ‘perceptual’ stream, projecting from early visual areas to inferior temporal cortex, helps to construct the rich and detailed visual representations of the world that allow us to identify objects and events, attach meaning and significance to them and establish their causal relations. By contrast, the dorsal ‘action’ stream, projecting from early visual areas to the posterior parietal cortex, plays a critical role in the real-time control of action, transforming information about the location and disposition of goal objects into the coordinate frames of the effectors being used to perform the action. The idea of two visual systems in a single brain might seem initially counterintuitive. Our visual experience of the world is so compelling that it is hard to believe that some other quite independent visual signal—one that we are unaware of—is guiding our movements. But evidence from a broad range of studies from neuropsychology to neuroimaging has shown that the visual signals that give us our experience of objects and events in the world are not the same ones that control our actions.     

Development of a New Method to Track Multiple Honey Bees with Complex Behaviors on a Flat Laboratory Arena

A computer program that tracks animal behavior, thereby revealing various features and mechanisms of social animals, is a powerful tool in ethological research. Because honeybee colonies are populated by thousands of bees, individuals co-exist in high physical densities and are difficult to track unless specifically tagged, which can affect behavior. In addition, honeybees react to light and recordings must be made under special red-light conditions, which the eyes of bees perceive as darkness. The resulting video images are scarcely distinguishable. We have developed a new algorithm, K-Track, for tracking numerous bees in a flat laboratory arena. Our program implements three main processes: (A) The object (bee''s) region is detected by simple threshold processing on gray scale images, (B) Individuals are identified by size, shape and spatiotemporal positional changes, and (C) Centers of mass of identified individuals are connected through all movie frames to yield individual behavioral trajectories. The tracking performance of our software was evaluated on movies of mobile multi-artificial agents and of 16 bees walking around a circular arena. K-Track accurately traced the trajectories of both artificial agents and bees. In the latter case, K-track outperformed Ctrax, well-known software for tracking multiple animals. To investigate interaction events in detail, we manually identified five interaction categories; ‘crossing’, ‘touching’, ‘passing’, ‘overlapping’ and ‘waiting’, and examined the extent to which the models accurately identified these categories from bee''s interactions. All 7 identified failures occurred near a wall at the outer edge of the arena. Finally, K-Track and Ctrax successfully tracked 77 and 60 of 84 recorded interactive events, respectively. K-Track identified multiple bees on a flat surface and tracked their speed changes and encounters with other bees, with good performance.     

Sperm chemotaxis in marine species is optimal at physiological flow rates according theory of filament surfing

Sperm of marine invertebrates have to find eggs cells in the ocean. Turbulent flows mix sperm and egg cells up to the millimeter scale; below this, active swimming and chemotaxis become important. Previous work addressed either turbulent mixing or chemotaxis in still water. Here, we present a general theory of sperm chemotaxis inside the smallest eddies of turbulent flow, where signaling molecules released by egg cells are spread into thin concentration filaments. Sperm cells ‘surf’ along these filaments towards the egg. External flows make filaments longer, but also thinner. These opposing effects set an optimal flow strength. The optimum predicted by our theory matches flow measurements in shallow coastal waters. Our theory quantitatively agrees with two previous fertilization experiments in Taylor-Couette chambers and provides a mechanistic understanding of these early experiments. ‘Surfing along concentration filaments’ could be a paradigm for navigation in complex environments in the presence of turbulent flow.     

Odour boosts visual object approach in flies

Multisensory integration is synergistic—input from one sensory modality might modulate the behavioural response to another. Work in flies has shown that a small visual object presented in the periphery elicits innate aversive steering responses in flight, likely representing an approaching threat. Object aversion is switched to approach when paired with a plume of food odour. The ‘open-loop’ design of prior work facilitated the observation of changing valence. How does odour influence visual object responses when an animal has naturally active control over its visual experience? In this study, we use closed-loop feedback conditions, in which a fly''s steering effort is coupled to the angular velocity of the visual stimulus, to confirm that flies steer toward or ‘fixate’ a long vertical stripe on the visual midline. They tend either to steer away from or ‘antifixate’ a small object or to disengage active visual control, which manifests as uncontrolled object ‘spinning’ within this experimental paradigm. Adding a plume of apple cider vinegar decreases the probability of both antifixation and spinning, while increasing the probability of frontal fixation for objects of any size, including a normally typically aversive small object.     

Humans but Not Chimpanzees Vary Face-Scanning Patterns Depending on Contexts during Action Observation

Human and nonhuman primates comprehend the actions of other individuals by detecting social cues, including others’ goal-directed motor actions and faces. However, little is known about how this information is integrated with action understanding. Here, we present the ontogenetic and evolutionary foundations of this capacity by comparing face-scanning patterns of chimpanzees and humans as they viewed goal-directed human actions within contexts that differ in whether or not the predicted goal is achieved. Human adults and children attend to the actor’s face during action sequences, and this tendency is particularly pronounced in adults when observing that the predicted goal is not achieved. Chimpanzees rarely attend to the actor’s face during the goal-directed action, regardless of whether the predicted action goal is achieved or not. These results suggest that in humans, but not chimpanzees, attention to actor’s faces conveying referential information toward the target object indicates the process of observers making inferences about the intentionality of an action. Furthermore, this remarkable predisposition to observe others’ actions by integrating the prediction of action goals and the actor’s intention is developmentally acquired.     

Repression and Recuperation of Brood Production in Bombus terrestris Bumble Bees Exposed to a Pulse of the Neonicotinoid Pesticide Imidacloprid

Currently, there is concern about declining bee populations and some blame the residues of neonicotinoid pesticides in the nectar and pollen of treated crops. Bumble bees are important wild pollinators that are widely exposed to dietary neonicotinoids by foraging in agricultural environments. In the laboratory, we tested the effect of a pulsed exposure (14 days ‘on dose’ followed by 14 days ‘off dose’) to a common neonicotinoid, imidacloprid, on the amount of brood (number of eggs and larvae) produced by Bombus terrestris L. bumble bees in small, standardised experimental colonies (a queen and four adult workers). During the initial ‘on dose’ period we observed a dose-dependent repression of brood production in colonies, with productivity decreasing as dosage increased up to 98 µg kg⁻¹ dietary imidacloprid. During the following ‘off dose’ period, colonies showed a dose-dependent recuperation such that total brood production during the 28-day pulsed exposure was not correlated with imidacloprid up to 98 µg kg⁻¹. Our findings raise further concern about the threat to wild bumble bees from neonicotinoids, but they also indicate some resilience to a pulsed exposure, such as that arising from the transient bloom of a treated mass-flowering crop.     

Differential Beta-Band Event-Related Desynchronization during Categorical Action Sequence Planning

A primate study reported the existence of neurons from the dorso-lateral prefrontal cortex which fired prior to executing categorical action sequences. The authors suggested these activities may represent abstract level information. Here, we aimed to find the neurophysiological representation of planning categorical action sequences at the population level in healthy humans. Previous human studies have shown beta-band event-related desynchronization (ERD) during action planning in humans. Some of these studies showed different levels of ERD according to different types of action preparation. Especially, the literature suggests that variations in cognitive factors rather than physical factors (force, direction, etc) modulate the level of beta-ERD. We hypothesized that the level of beta-band power will differ according to planning of different categorical sequences. We measured magnetoencephalography (MEG) from 22 subjects performing 11 four-sequence actions - each consisting of one or two of three simple actions - in 3 categories; ‘Paired (ooxx)’, ‘Alternative (oxox)’ and ‘Repetitive (oooo)’ (‘o’ and ‘x’ each denoting one of three simple actions). Time-frequency representations were calculated for each category during the planning period, and the corresponding beta-power time-courses were compared. We found beta-ERD during the planning period for all subjects, mostly in the contralateral fronto-parietal areas shortly after visual cue onset. Power increase (transient rebound) followed ERD in 20 out of 22 subjects. Amplitudes differed among categories in 20 subjects for both ERD and transient rebound. In 18 out of 20 subjects ‘Repetitive’ category showed the largest ERD and rebound. The current result suggests that beta-ERD in the contralateral frontal/motor/parietal areas during planning is differentiated by the category of action sequences.     

Distributed Patterns of Event-Related Potentials Predict Subsequent Ratings of Abstract Stimulus Attributes

Exposure to pleasant and rewarding visual stimuli can bias people''s choices towards either immediate or delayed gratification. We hypothesised that this phenomenon might be based on carry-over effects from a fast, unconscious assessment of the abstract ‘time reference’ of a stimuli, i.e. how the stimulus relates to one''s personal understanding and connotation of time. Here we investigated whether participants'' post-experiment ratings of task-irrelevant, positive background visual stimuli for the dimensions ‘arousal’ (used as a control condition) and ‘time reference’ were related to differences in single-channel event-related potentials (ERPs) and whether they could be predicted from spatio-temporal patterns of ERPs. Participants performed a demanding foreground choice-reaction task while on each trial one task-irrelevant image (depicting objects, people and scenes) was presented in the background. Conventional ERP analyses as well as multivariate support vector regression (SVR) analyses were conducted to predict participants'' subsequent ratings. We found that only SVR allowed both ‘arousal’ and ‘time reference’ ratings to be predicted during the first 200 ms post-stimulus. This demonstrates an early, automatic semantic stimulus analysis, which might be related to the high relevance of ‘time reference’ to everyday decision-making and preference formation.     

‘Bee Hotels’ as Tools for Native Pollinator Conservation: A Premature Verdict?

Society is increasingly concerned with declining wild bee populations. Although most bees nest in the ground, considerable effort has centered on installing ‘bee hotels’—also known as nest boxes or trap nests—which artificially aggregate nest sites of above ground nesting bees. Campaigns to ‘save the bees’ often promote these devices despite the absence of data indicating they have a positive effect. From a survey of almost 600 bee hotels set up over a period of three years in Toronto, Canada, introduced bees nested at 32.9% of sites and represented 24.6% of more than 27,000 total bees and wasps recorded (47.1% of all bees recorded). Native bees were parasitized more than introduced bees and females of introduced bee species provisioned nests with significantly more female larva each year. Native wasps were significantly more abundant than both native and introduced bees and occupied almost 3/4 of all bee hotels each year; further, introduced wasps were the only group to significantly increase in relative abundance year over year. More research is needed to elucidate the potential pitfalls and benefits of using bee hotels in the conservation and population dynamics of wild native bees.     

Same or different? Abstract relational concept use in juvenile bamboo sharks and Malawi cichlids

Sorting objects and events into categories and concepts is an important cognitive prerequisite that spares an individual the learning of every object or situation encountered in its daily life. Accordingly, specific items are classified in general groups that allow fast responses to novel situations. The present study assessed whether bamboo sharks Chiloscyllium griseum and Malawi cichlids Pseudotropheus zebra can distinguish sets of stimuli (each stimulus consisting of two abstract, geometric objects) that meet two conceptual preconditions, i.e., (1) “sameness” versus “difference” and (2) a certain spatial arrangement of both objects. In two alternative forced choice experiments, individuals were first trained to choose two different, vertically arranged objects from two different but horizontally arranged ones. Pair discriminations were followed by extensive transfer test experiments. Transfer tests using stimuli consisting of (a) black and gray circles and (b) squares with novel geometric patterns provided conflicting information with respect to the learnt rule “choose two different, vertically arranged objects”, thereby investigating (1) the individuals’ ability to transfer previously gained knowledge to novel stimuli and (2) the abstract relational concept(s) or rule(s) applied to categorize these novel objects. Present results suggest that the level of processing and usage of both abstract concepts differed considerably between bamboo sharks and Malawi cichlids. Bamboo sharks seemed to combine both concepts—although not with equal but hierarchical prominence—pointing to advanced cognitive capabilities. Conversely, Malawi cichlids had difficulties in discriminating between symbols and failed to apply the acquired training knowledge on new sets of geometric and, in particular, gray-level transfer stimuli.     

“Vision for Action” in Young Children Aligning Multi-Featured Objects: Development and Comparison with Nonhuman Primates

Effective vision for action and effective management of concurrent spatial relations underlie skillful manipulation of objects, including hand tools, in humans. Children’s performance in object insertion tasks (fitting tasks) provides one index of the striking changes in the development of vision for action in early life. Fitting tasks also tap children’s ability to work with more than one feature of an object concurrently. We examine young children’s performance on fitting tasks in two and three dimensions and compare their performance with the previously reported performance of adult individuals of two species of nonhuman primates on similar tasks. Two, three, and four year-old children routinely aligned a bar-shaped stick and a cross-shaped stick but had difficulty aligning a tomahawk-shaped stick to a matching cut-out. Two year-olds were especially challenged by the tomahawk. Three and four year-olds occasionally held the stick several inches above the surface, comparing the stick to the surface visually, while trying to align it. The findings suggest asynchronous development in the ability to use vision to achieve alignment and to work with two and three spatial features concurrently. Using vision to align objects precisely to other objects and managing more than one spatial relation between an object and a surface are already more elaborated in two year-old humans than in other primates. The human advantage in using hand tools derives in part from this fundamental difference in the relation between vision and action between humans and other primates.     

Genetic and ‘cultural’ similarity in wild chimpanzees

The question of whether animals possess ‘cultures’ or ‘traditions’ continues to generate widespread theoretical and empirical interest. Studies of wild chimpanzees have featured prominently in this discussion, as the dominant approach used to identify culture in wild animals was first applied to them. This procedure, the ‘method of exclusion,’ begins by documenting behavioural differences between groups and then infers the existence of culture by eliminating ecological explanations for their occurrence. The validity of this approach has been questioned because genetic differences between groups have not explicitly been ruled out as a factor contributing to between-group differences in behaviour. Here we investigate this issue directly by analysing genetic and behavioural data from nine groups of wild chimpanzees. We find that the overall levels of genetic and behavioural dissimilarity between groups are highly and statistically significantly correlated. Additional analyses show that only a very small number of behaviours vary between genetically similar groups, and that there is no obvious pattern as to which classes of behaviours (e.g. tool-use versus communicative) have a distribution that matches patterns of between-group genetic dissimilarity. These results indicate that genetic dissimilarity cannot be eliminated as playing a major role in generating group differences in chimpanzee behaviour.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.     

Pointing Behavior in Infants Reflects the Communication Partner’s Attentional and Knowledge States: A Possible Case of Spontaneous Informing

Inferring the epistemic states of others is considered to be an essential requirement for humans to communicate; however, the developmental trajectory of this ability is unclear. The aim of the current study was to determine developmental trends in this ability by using pointing behavior as a dependent measure. Infants aged 13 to 18 months (n = 32, 16 females) participated in the study. The experiment consisted of two phases. In the Shared Experience Phase, both the participant and the experimenter experienced (played with) an object, and the participant experienced a second object while the experimenter was absent. In the Pointing Phase, the participant was seated on his/her mother’s lap, facing the experimenter, and the same two objects from the Shared Experience Phase were presented side-by-side behind the experimenter. The participants’ spontaneous pointing was analyzed from video footage. While the analysis of the Shared Experience Phase suggested that there was no significant difference in the duration of the participants’ visual attention to the two objects, the participants pointed more frequently to the object that could be considered “new” for the experimenter (in Experiment 1). This selective pointing was not observed when the experimenter could be considered unfamiliar with both of the objects (in Experiment 2). These findings suggest that infants in this age group spontaneously point, presumably to inform about an object, reflecting the partner’s attentional and knowledge states.     

How Possibly Do Leisure and Social Activities Impact Mental Health of Middle-Aged Adults in Japan?: An Evidence from a National Longitudinal Survey

Objectives

This study aimed to investigate longitudinal relations between leisure and social activities and mental health status, considering the presence or absence of other persons in the activity as an additional variable, among middle-aged adults in Japan. This study used nationally representative data in Japan with a five-year follow-up period.

Methods

This study focused on 16,642 middle-aged adults, age 50–59 at baseline, from a population-based, six-year panel survey conducted by the Japanese Ministry of Health, Labour and Welfare. To investigate the relations between two leisure activities (‘hobbies or cultural activities’ and ‘exercise or sports’) and four social activities (‘community events’, ‘support for children’, ‘support for elderly individuals’ and ‘other social activities’) at baseline and mental health status at follow-up, multiple logistic regression analysis was used. We also used multiple logistic regression analysis to investigate the association between ways of participating in these activities (‘by oneself’, ‘with others’, or ‘both’ (both ‘by oneself’ and ‘with others’)) at baseline and mental health status at follow-up.

Results

Involvement in both leisure activity categories, but not in social activities, was significantly and positively related to mental health status in both men and women.Furthermore, in men, both ‘hobbies or cultural activities’ and ‘exercise or sports’ were significantly related to mental health status only when conducted ‘with others’. In women, the effects of ‘hobbies or cultural activities’ on mental health status were no differences regardless of the ways of participating, while the result of ‘exercise or sports’ was same as that in men.

Conclusions

Leisure activities appear to benefit mental health status among this age group, whereas specific social activities do not. Moreover, participation in leisure activities would be effective especially if others are present. These findings should be useful for preventing the deterioration of mental health status in middle-aged adults in Japan.     

Disruptive Colouration and Perceptual Grouping

Camouflage is the primary defence of many animals and includes multiple strategies that interfere with figure-ground segmentation and object recognition. While matching background colours and textures is widespread and conceptually straightforward, less well explored are the optical ‘tricks’, collectively called disruptive colouration, that exploit perceptual grouping mechanisms. Adjacent high contrast colours create false edges, but this is not sufficient for an object’s shape to be broken up; some colours must blend with the background. We test the novel hypothesis that this will be particularly effective when the colour patches on the animal appear to belong to, not merely different background colours, but different background objects. We used computer-based experiments where human participants had to find cryptic targets on artificial backgrounds. Creating what appeared to be bi-coloured foreground objects on bi-coloured backgrounds, we generated colour boundaries that had identical local contrast but either lay within or between (illusory) objects. As predicted, error rates for targets matching what appeared to be different background objects were higher than for targets which had otherwise identical local contrast to the background but appeared to belong to single background objects. This provides evidence for disruptive colouration interfering with higher-level feature integration in addition to previously demonstrated low-level effects involving contour detection. In addition, detection was impeded in treatments where targets were on or in close proximity to multiple background colour or tone boundaries. This is consistent with other studies which show a deleterious influence of visual ‘clutter’ or background complexity on search.