Honeybee methodology, cognition, and theory: recording local directional decisions in interpatch foraging and interpreting their theoretical relevance

Investigations made into the cognitive decision making of honeybees (Apis mellifera) traveling from one flower patch to another flower patch (interpatch foraging) are few. To facilitate such research, we present methods to artificially emulate interpatch foraging and quantify the immediate decision making of honeybees (within 50 cm) choosing to fly an interpatch path. These “Interpatch Methods” are validated, applied, and shown to produce novel information for the field of honeybee spatial cognition. Generally, we demonstrate that a single foraging cohort of honeybees is shown to be capable of making decisions based upon different sets of learned cues, in the exact same context. Specifically, both terminal beacon orientation cues and compass navigation cues can guide the cognitive decision making of interpatch foraging honeybees; our bees chose both cues equally. Finally, the theoretical importance of decision making for interpatch paths is compared with the other foraging paths (outward and homing) with respect to the information available to recruited foragers and scout foragers. We conclude that the ability to analyze interpatch foraging is critical for a more complete understanding of honeybee foraging cognition and that our methods are capable of providing that understanding.     

Copying without rewards: socially influenced foraging decisions among brown capuchin monkeys

An individual’s foraging activity can be influenced by the choices made by nearby conspecifics. The interest shown in the location and characteristics of a feeding patch may depend on the feeding success of a conspecific there, a process that needs to be distinguished from choices guided by rewards to the observer itself. We investigated how rewards for both self and others influence the foraging choices of captive capuchin monkeys (Cebus apella). Thirteen adult capuchins observed familiar female conspecific models explore one of three opaque boxes under three conditions. In the first, there were no rewards available to either monkey; in the second, rewards were available to the model only; and in the third, both monkeys could retrieve a reward. Under all conditions, subjects more often explored the same box as the model than was expected by chance. Thus, without ever receiving a reward themselves or without seeing another receive rewards, subjects’ searches were directed at the box explored by another monkey. The tendency to match the model’s choice increased if the subject was rewarded. We compared these results to control conditions in which the model was either absent, or present but not allowed to demonstrate. Subjects’ located the reward less often in control conditions, than in the experimental conditions. We conclude that extrinsic rewards, while helpful, are not required for partners to influence the foraging choices of capuchins, and that the unrewarded copying of foraging choices demonstrated here may provide the basis for additional social influences on learning. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007)     

Political ideology as motivated social cognition: Behavioral and neuroscientific evidence

Ideology is a potent motivational force; human beings are capable of committing atrocities (as well as acts of generosity and courage) and sacrificing even their own lives for the sake of abstract belief systems. In this article, we summarize the major tenets of a model of political ideology as motivated social cognition (Jost et al. in Psychol Bull 129:339–375, 2003a, Psychol Bull 129:389–393, 2003b, Person Soc Psychol Bull 33:989–1007, 2007), focusing on epistemic, existential, and relational motives and their implications for left-right (or liberal-conservative) political orientation. We review behavioral evidence indicating that chronically and temporarily activated needs to reduce uncertainty, ambiguity, threat, and disgust are positively associated with conservatism (or negatively associated with liberalism). Studies from neuroscience and genetics suggest that right- (vs. left-) wing orientation is associated with greater neural sensitivity to threat and larger amygdala volume, as well as less sensitivity to response conflict and smaller anterior cingulate volume. These findings and others provide converging evidence for Jost and colleagues’ model of ideology as motivated social cognition and, more broadly, reflect the utility of an integrative political neuroscience approach to understanding the basic cognitive, neural, and motivational processes that give rise to ideological activity.     

Evidence against integration of spatial maps in humans: generality across real and virtual environments

A real-world open-field search task was implemented with humans as an analogue of Blaisdell and Cook’s (Anim Cogn 8:7–16, 2005) pigeon foraging task and Sturz, Bodily, and Katz’s (Anim Cogn 9:207–217, 2006) human virtual foraging task to 1) determine whether humans were capable of integrating independently learned spatial maps and 2) make explicit comparisons of mechanisms used by humans to navigate real and virtual environments. Participants searched for a hidden goal located in one of 16 bins arranged in a 4 × 4 grid. In Phase 1, the goal was hidden between two landmarks (blue T and red L). In Phase 2, the goal was hidden to the left and in front of a single landmark (blue T). Following training, goal-absent trials were conducted in which the red L from Phase 1 was presented alone. Bin choices during goal-absent trials assessed participants’ strategies: association (from Phase 1), generalization (from Phase 2), or integration (combination of Phase 1 and 2). Results were inconsistent with those obtained with pigeons but were consistent with those obtained with humans in a virtual environment. Specifically, during testing, participants did not integrate independently learned spatial maps but used a generalization strategy followed by a shift in search behavior away from the test landmark. These results were confirmed by a control condition in which a novel landmark was presented during testing. Results are consistent with the bulk of recent findings suggesting the use of alternative navigational strategies to cognitive mapping. Results also add to a growing body of literature suggesting that virtual environment approaches to the study of spatial learning and memory have external validity and that spatial mechanisms used by human participants in navigating virtual environments are similar to those used in navigating real-world environments.     

Universal Grammar as a Theory of Notation

What is common to all languages is notation, so Universal Grammar can be understood as a system of notational types. Given that infants acquire language, it can be assumed to arise from some a priori mental structure. Viewing language as having the two layers of calculus and protocol, we can set aside the communicative habits of speakers. Accordingly, an analysis of notation results in the three types of Identifier, Modifier and Connective. Modifiers are further interpreted as Quantifiers and Qualifiers. The resulting four notational types constitute the categories of Universal Grammar. Its ontology is argued to consist in the underlying cognitive schema of Essence, Quantity, Quality and Relation. The four categories of Universal Grammar are structured as polysemous fields and are each constituted as a radial network centred on some root concept which, however, need not be lexicalized. The branches spread out along troponymic vectors and together map out all possible lexemes. The notational typology of Universal Grammar is applied in a linguistic analysis of the ‘parts of speech’ using the English language. The analysis constitutes a ‘proof of concept’ in (1) showing how the schema of Universal Grammar is capable of classifying the so-called ‘parts of speech’, (2) presenting a coherent analysis of the verb, and (3) showing how the underlying cognitive schema allows for a sub-classification of the auxiliaries.     

Artificial grammer learning by infants: an auto‐associator perspective

This paper reviews a recent article suggesting that infants use a system of algebraic rules to learn an artificial grammar (Marcus, Vijayan, Bandi Rao & Vishton, Rule learning by seven‐month‐old infants. Science, 183(1999), 77–80). In three reported experiments, infants exhibited increased responding to auditory strings that violated the pattern of elements they were habituated to. We argue that a perceptual interpretation is more parsimonious, as well as more consistent with a broad array of habituation data, and we report successful neural network simulations that implement this lower‐level interpretation. In the discussion, we discuss how our model relates to other habituation research, and how it compares to other neural network models of habituation in general, and models of the Marcus et al. (1999) task specifically.     

A cGMP-dependent protein kinase gene, foraging, modifies habituation-like response decrement of the giant fiber escape circuit in Drosophila

The Drosophila giant fiber jump-and-flight escape response is a model for genetic analysis of both the physiology and the plasticity of a sensorimotor behavioral pathway. We previously established the electrically induced giant fiber response in intact tethered flies as a model for habituation, a form of nonassociative learning. Here, we show that the rate of stimulus-dependent response decrement of this neural pathway in a habituation protocol is correlated with PKG (cGMP-Dependent Protein Kinase) activity and foraging behavior. We assayed response decrement for natural and mutant rover and sitter alleles of the foraging (for) gene that encodes a Drosophila PKG. Rover larvae and adults, which have higher PKG activities, travel significantly farther while foraging than sitters with lower PKG activities. Response decrement was most rapid in genotypes previously shown to have low PKG activities and sitter-like foraging behavior. We also found differences in spontaneous recovery (the reversal of response decrement during a rest from stimulation) and a dishabituation-like phenomenon (the reversal of response decrement evoked by a novel stimulus). This electrophysiological study in an intact animal preparation provides one of the first direct demonstrations that PKG can affect plasticity in a simple learning paradigm. It increases our understanding of the complex interplay of factors that can modulate the sensitivity of the giant fiber escape response, and it defines a new adult-stage phenotype of the foraging locus. Finally, these results show that behaviorally relevant neural plasticity in an identified circuit can be influenced by a single-locus genetic polymorphism existing in a natural population of Drosophila.     

Common marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>) do not utilize social information in three simultaneous social foraging tasks

Social foraging is suggested to increase foraging efficiency, as individuals might benefit from public information acquired by monitoring the foraging activities of other group members. We conducted a series experiments with captive common marmosets (Callithrix jacchus) to investigate to what extent marmosets utilize social information about food location when foraging simultaneously with conspecifics. Subjects were confronted with dominant and subordinate demonstrators in three experiments which differed in the amount of information about food location available to the demonstrators. In all three experiments, the focal subjects’ performance in the social condition was not enhanced in comparison to a non-social control condition. Because we could rule out kleptoparasitism and aggressive displacements as explanations, we argue that the subjects’ tendency for scramble competition by avoiding others and dispersing over the foraging area seems to inhibit or mask the acquisition of social information about the location of rewarded patches.     

Expertise acquisition as sustained learning in humans and other animals: commonalities across species

Expertise acquisition may be a universal attribute of animals. In this study data on foraging efficiency, or expertise, was compared for four species: honeybees (Apis mellifera), oystercatchers (Haematopus ostralegus), chimpanzees (Pan troglodytes), and humans (Homo sapiens). Polynomial regression models were constructed to investigate the relationship between age and foraging efficiency. There was a similar expertise–acquisition function between age and foraging efficiency across species, best described by a quadratic equation. The peak of performance was reached, in all cases, before the average age of death but well after reaching physical maturity and the percentage of lifespan devoted to the skill was more than 10% of the species-typical lifespan.     

Mother–Calf vocal communication in Atlantic walrus: a first field experimental study

In all colonial pinnipeds studied, mother–young vocal recognition exists and allows rapid and reliable meetings in spite of the confusing environment of the breeding colony. The efficiency of this recognition process guarantees pup survival, especially in species where females alternate foraging sea trips and lactation periods on land. The Atlantic Walrus (Odobenus rosmarus rosmarus) is a highly gregarious pinniped with females attending their calves for an extended period of time (2–3 years). Although we expect mother–calf vocal recognition to occur in this species due to the high density of individuals packed in herds, it has never been experimentally demonstrated. Here, we assessed the individual stereotypy of both mother and calf barks recorded in the wild by measuring frequency and temporal acoustic parameters. Both discriminant function and artificial neural network analyses resulted in high correct classification rates, underlying a well-defined individual stereotypy in parameters related to frequency modulation and frequency values. Playback experiments showed that mothers were more responsive to the barks of their own calf than to those of unrelated young. Finally, propagation experiments revealed that barks propagate at greater distances over water surface than over ice, acoustic features such as frequency modulation and frequency spectrum being highly resistant to degradation during propagation. Thus, acoustic analysis and propagation experiments suggest that these frequency parameters might be the key acoustic features involved in the individual identification process. This experimental study clearly demonstrates that Atlantic walrus has developed a highly reliable mother–calf vocal communication allowing such strong social bond.     

Integrating information about location and value of resources by white-faced saki monkeys (<Emphasis Type="Italic">Pithecia pithecia</Emphasis>)

Most studies of spatial memory in primates focus on species that inhabit large home ranges and have dispersed, patchy resources. Researchers assume that primates use memory to minimize distances traveled between resources. We investigated the use of spatial memory in a group of six white-faced sakis (Pithecia pithecia) on 12.8-ha Round Island, Guri Lake, Venezuela during a period of fruit abundance. The sakis’ movements were analyzed with logistic regressions, a predictive computer model and a computer model that simulates movements. We considered all the resources available to the sakis and compared observed distances to predicted distances from a computer model for foragers who know nothing about the location of resources. Surprisingly, the observed distances were four times greater than the predicted distances, suggesting that the sakis passed by a majority of the available fruit trees without feeding. The odds of visiting a food tree, however, were significantly increased if the tree had been visited in the previous 3 days and had more than 100 fruit. The sakis’ preferred resources were highly productive fruit trees, Capparis trees, and trees with water holes. They traveled efficiently to these sites. The sakis choice of feeding sites indicate that they combined knowledge acquired by repeatedly traveling through their home range with ‘what’ and ‘where’ information gained from individual visits to resources. Although the sakis’ foraging choices increased the distance they traveled overall, choosing more valued sites allowed the group to minimize intragroup feeding competition, maintain intergroup dominance over important resources, and monitor the state of resources throughout their home range. The sakis’ foraging decisions appear to have used spatial memory, elements of episodic-like memory and social and nutritional considerations. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).     

Learning representations of wordforms with recurrent networks: comment on sibley, kello, plaut, & elman (2008)

Sibley et al. (2008) report a recurrent neural network model designed to learn wordform representations suitable for written and spoken word identification. The authors claim that their sequence encoder network overcomes a key limitation associated with models that code letters by position (e.g., CAT might be coded as C‐in‐position‐1, A‐in‐position‐2, T‐in‐position‐3). The problem with coding letters by position (slot‐coding) is that it is difficult to generalize knowledge across positions; for example, the overlap between CAT and TOMCAT is lost. Although we agree this is a critical problem with many slot‐coding schemes, we question whether the sequence encoder model addresses this limitation, and we highlight another deficiency of the model. We conclude that alternative theories are more promising.     

Alexander Bain's Mind and Body (1872): An underappreciated contribution to early neuropsychology

Alexander Bain (1818–1903) is well known for his two influential textbooks, The senses and the intellect (1855) and The emotions and the will (1859). In comparison, Bain's Mind and body: The theories of their relation (1872) has been of limited interest to historians, and it is here where he presents one of the first neural network models. This paper addresses the historical foundations of Bain's neural network model and explores some of his primary influences. Additionally, this study addresses some of the reasons Bain's Mind and Body did not receive the historical notice his earlier works garnered.     

Do sheep (<Emphasis Type="Italic">Ovis aries</Emphasis>) categorize plant species according to botanical family?

The ability of grazing herbivores to assign food types to categories by relying on certain relevant criteria could considerably reduce cognitive demand and increase their foraging efficiency when selecting among many different plant items. Grasses and legumes differ functionally in vegetation communities as well as in nutritive value. We aimed to determine whether sheep can generalize an aversion they learnt for a grass or a legume species to another species of the same functional type and consequently whether botanical family is a potential level of categorization. Over four successive weeks, 12 lambs were conditioned against either a freshly cut grass (tall fescue—Festuca arundinacea, N = 6) or legume species (sainfoin—Onobrychis viciifolia, N = 6) using a negative post-ingestive stimulus (lithium chloride) on day 1. Preference of all lambs between another grass (cocksfoot—Dactylis glomerata) and another legume (alfalfa—Medicago sativa) was assessed on day 3 by measuring their relative consumptions. Preference for alfalfa progressively became lower for lambs that were conditioned against sainfoin than against tall fescue, indicating that lambs generalized the aversion between species along some perceptual gradient and classed the considered grasses and legumes in distinct categories. Beyond this original result, the question now is to identify which specific plant characteristics or functional traits the animals rely on in order to form categories.     

Visual discrimination,sequential learning and memory retrieval in the Australian desert ant <Emphasis Type="Italic">Melophorus bagoti</Emphasis>

Bees, wasps and ants—so-called central-place foragers—need potent homing strategies to return to their nest. Path integration and view-based landmark guidance are the key strategies for the ants’ navigation. For instance, they memorise different views in a sequence (sequential memory) but also have a step counter that informs them about the covered distance during each foraging trip (odometer). The sequential memory and the odometer information can act as contextual cues during travel for retrieving the appropriate stored view. When and which cue is used at different stages and lengths of the foraging trips is still unknown. In this study, we examined how the Australian desert ant Melophorus bagoti uses sequential memory and odometric information to retrieve visual memories. Using a set-up made out of channels and two-choice boxes (Y-mazes), we demonstrate first that M. bagoti foragers are able to learn and discriminate a variety of visual stimuli in a sequence of views along the inbound trip back to the nest. We then forced the homing ants to encounter a fixed sequence of two visual patterns during their inbound trips. By manipulating the position and distance of the visual stimuli and decision boxes, we could set the two contextual cues (sequential memory and odometer) into conflict. After the short 4-m outbound distance, a preference for odometric information as a contextual cue was found, but after the long 8-m outbound distance, ants relied primarily on their sequential memory retrieval. Odometer precision deteriorates with increasing travel distance, and accordingly, our findings imply that desert ants may be relying on the most reliable contextual cue for retrieving visual memories.     

Cues to food location that domestic dogs (Canis familiaris) of different ages do and do not use

The results of three experiments are reported. In the main study, a human experimenter presented domestic dogs (Canis familiaris) with a variety of social cues intended to indicate the location of hidden food. The novel findings of this study were: (1) dogs were able to use successfully several totally novel cues in which they watched a human place a marker in front of the target location; (2) dogs were unable to use the marker by itself with no behavioral cues (suggesting that some form of human behavior directed to the target location was a necessary part of the cue); and (3) there were no significant developments in dogs’ skills in these tasks across the age range 4 months to 4 years (arguing against the necessity of extensive learning experiences with humans). In a follow-up study, dogs did not follow human gaze into “empty space” outside of the simulated foraging context. Finally, in a small pilot study, two arctic wolves (Canis lupus) were unable to use human cues to locate hidden food. These results suggest the possibility that domestic dogs have evolved an adaptive specialization for using human-produced directional cues in a goal-directed (especially foraging) context. Exactly how they understand these cues is still an open question. Received: 28 April 2000 / Accepted after revision: 2 September 2000     

Experimental evidence for route integration and strategic planning in wild capuchin monkeys

Both in captivity and the wild, primates are found to travel mostly to the nearest available resource, but they may skip over the closest resource and travel to more distant resources, which are often found to be more productive. This study examines the tradeoff between distance and reward in the foraging choices of one group of wild capuchin monkeys (Cebus apella nigritus) using feeding platforms in large-scale foraging experiments conducted over four years. Three feeding sites were arrayed in an oblique triangle, such that once the monkey group had chosen one site to feed, they had a choice between two remaining sites, a close one with less food and the other up to 2.3 times as far away but with more food. Sites were provisioned once per day. The capuchins generally chose the closer feeding site, even when the more distant site offered up to 12 times as much food. The distances to, rewards of, or various profitability measures applied to each alternative site individually did not explain the group’s choices in ways consistent with foraging theory or principles of operant psychology. The group’s site choices were predicted only by comparing efficiency measures of entire foraging pathways: (1) direct travel to the more rewarding distant site, versus (2) the longer ‘detour’ through the closer site on the way to the more distant one. The group chose the detour more often when the reward was larger and the added detour distance shorter. They appeared to be more sensitive to the absolute increase in detour distance than to the relative increase compared to the straight route. The qualitative and quantitative results agree with a simple rule: do not use the detour unless the energy gain from extra food outweighs the energy cost of extra travel. These results suggest that members of this group integrate information on spatial location, reward, and perhaps potential food competition in their choice of multi-site foraging routes, with important implications for social foraging. This contribution is part of the special issue “ A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007b).     

Linking patterns of infant eye movements to a neural network model of the ventral stream using representational similarity analysis

Little is known about the development of higher-level areas of visual cortex during infancy, and even less is known about how the development of visually guided behavior is related to the different levels of the cortical processing hierarchy. As a first step toward filling these gaps, we used representational similarity analysis (RSA) to assess links between gaze patterns and a neural network model that captures key properties of the ventral visual processing stream. We recorded the eye movements of 4- to 12-month-old infants (N = 54) as they viewed photographs of scenes. For each infant, we calculated the similarity of the gaze patterns for each pair of photographs. We also analyzed the images using a convolutional neural network model in which the successive layers correspond approximately to the sequence of areas along the ventral stream. For each layer of the network, we calculated the similarity of the activation patterns for each pair of photographs, which was then compared with the infant gaze data. We found that the network layers corresponding to lower-level areas of visual cortex accounted for gaze patterns better in younger infants than in older infants, whereas the network layers corresponding to higher-level areas of visual cortex accounted for gaze patterns better in older infants than in younger infants. Thus, between 4 and 12 months, gaze becomes increasingly controlled by more abstract, higher-level representations. These results also demonstrate the feasibility of using RSA to link infant gaze behavior to neural network models. A video abstract of this article can be viewed at https://youtu.be/K5mF2Rw98Is     

Colour cues or spatial cues? Context-dependent preferences in the European greenfinch (<Emphasis Type="Italic">Carduelis chloris</Emphasis>)

Using featural cues such as colour to identify ephemeral food can increase foraging efficiency. Featural cues may change over time however; therefore, animals should use spatial cues to relocate food that occurs in a temporally stable position. We tested this hypothesis by measuring the cue preferences of captive greenfinches Carduelis chloris when relocating food hidden in a foraging tray. In these standardised associative learning trials, greenfinches favoured colour cues when returning to a foraging context that they had encountered before only once (“one-trial test”) but switched to spatial cues when they had encountered that scenario on ten previous occasions (“repeated-trial test”). We suggest that repeated encounters generated a context in which individuals had a prior expectation of temporal stability, and hence context-dependent cue selection. Next, we trained birds to find food in the absence of colour cues but tested them in the presence of visual distracters. Birds were able to learn spatial cues after one encounter, but only when visual distracters were identical in colouration. When a colourful distracter was present in the test phase, cue selection was random. Unlike the first one-trial test, birds were not biased towards this colourful visual distracter. Together, these results suggest that greenfinches are able to learn both cue types, colour cue biases represent learning, not simply distraction, and spatial cues are favoured over colour cues only in temporally stable contexts.     

Not using the obvious: desert ants, Melophorus bagoti, learn local vectors but not beacons in an arena

Many ant species travel large distances to find food, sometimes covering distances that are up to one million times their body length. Even when these foraging trips follow convoluted paths, the ants usually find their way back to their nest with precision (Wehner et al. in J Exp Biol 199:129–140, 1996). Ants have been shown to use both compass cues in the sky (pattern of polarised light) and landmarks on Earth to return to their nest. We present two experiments conducted on a solitary foraging ant: Melophorus bagoti in their natural habitat in the central Australian desert. Ants were trained and tested in situ. We tested foragers’ ability to exit a circular arena which provided an undifferentiated panorama. Artificial visual landmarks were located near a small exit. On tests in which path integration information was not available, foragers did not use artificial landmarks as beacons. Instead, they oriented in the learned exit direction, whether or not it pointed to the nest. We suggest that M. bagoti foragers learned a context-specific local vector when cued by the context of the circular arena. Our findings present the first evidence that M. bagoti foragers learn context-specific compass directions to chart their initial path home.