Larval antlions show a cognitive ability/hunting efficiency trade-off connected with the level of behavioural asymmetry

Recently, antlion larvae with greater behavioural asymmetry were shown to have improved learning abilities. However, a major evolutionary question that remained unanswered was why this asymmetry does not increase in all individuals during development. Here, we show that a trade-off exists between learning ability of larvae and their hunting efficiency. Larvae with greater asymmetry learn better than those with less, but the latter are better able to sense vibrational signals used to detect prey and can capture prey more quickly. Both traits, learning ability and hunting efficiency, present obvious fitness advantages; the trade-off between them may explain why behavioural asymmetry, which presumably stems from brain lateralization, is relatively rare in natural antlion populations.     

Associative memory or algorithmic search: a comparative study on learning strategies of bats and shrews

Two common strategies for successful foraging are learning to associate specific sensory cues with patches of prey ("associative learning") and using set decision-making rules to systematically scan for prey ("algorithmic search"). We investigated whether an animal's life history affects which of these two foraging strategies it is likely to use. Natterer's bats (Myotis nattereri) have slow life-history traits and we predicted they would be more likely to use associative learning. Common shrews (Sorex araneus) have fast life-history traits and we predicted that they would rely more heavily on routine-based search. Apart from their marked differences in life-history traits, these two mammals are similar in body size, brain weight, habitat, and diet. We assessed foraging strategy, associative learning ability, and retention time with a four-arm maze; one arm contained a food reward and was marked with four sensory stimuli. Bats and shrews differed significantly in their foraging strategies. Most bats learned to associate the sensory stimuli with the reward and remembered this association over time. Most shrews searched the maze using consistent decision-making rules, but did not learn or remember the association. We discuss these results in terms of life-history traits and other key differences between these species. Our results suggest a link between an animal's life-history strategy and its use of associative learning.     

Elasmobranch cognitive ability: using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark

Top predators inhabiting a dynamic environment, such as coastal waters, should theoretically possess sufficient cognitive ability to allow successful foraging despite unpredictable sensory stimuli. The cognition-related hunting abilities of marine mammals have been widely demonstrated. Having been historically underestimated, teleost cognitive abilities have also now been significantly demonstrated. Conversely, the abilities of elasmobranchs have received little attention, despite many species possessing relatively large brains comparable to some mammals. The need to determine what, if any, cognitive ability these globally distributed, apex predators are endowed with has been highlighted recently by questions arising from environmental assessments, specifically whether they are able to learn to distinguish between anthropogenic electric fields and prey bioelectric fields. We therefore used electroreceptive foraging behaviour in a model species, Scyliorhinus canicula (small-spotted catshark), to determine cognitive ability by analysing whether elasmobranchs are able to learn to improve foraging efficiency and remember learned behavioural adaptations. Positive reinforcement, operant conditioning was used to study catshark foraging behaviour towards artificial, prey-type electric fields (Efields). Catsharks rewarded with food for responding to Efields throughout experimental weeks were compared with catsharks that were not rewarded for responding in order to assess behavioural adaptation via learning ability. Experiments were repeated after a 3-week interval with previously rewarded catsharks this time receiving no reward and vice versa to assess memory ability. Positive reinforcement markedly and rapidly altered catshark foraging behaviour. Rewarded catsharks exhibited significantly more interest in the electrical stimulus than unrewarded catsharks. Furthermore, they improved their foraging efficiency over time by learning to locate and bite the electrodes to gain food more quickly. In contrast, unrewarded catsharks showed some habituation, whereby their responses to the electrodes abated and eventually entirely ceased, though they generally showed no changes in most foraging parameters. Behavioural adaptations were not retained after the interval suggesting learned behaviour was not memorised beyond the interval. Sequences of individual catshark search paths clearly illustrated learning and habituation behavioural adaptation. This study demonstrated learning and habituation occurring after few foraging events and a memory window of between 12 h and 3 weeks. These cognitive abilities are discussed in relation to diet, habitat, ecology and anthropogenic Efield sources.     

Rapid spatial learning in a velvet ant (<Emphasis Type="Italic">Dasymutilla coccineohirta</Emphasis>)

Spatial learning has been examined in a variety of animals to determine what cues are used to navigate through a complex environment. A common feature of previously studied vertebrates and invertebrates is their need to return to a previously visited site for mating, nesting, foraging or predator avoidance. Velvet ants (Hymenoptera: Mutillidae) are cursorial parasitoids with flightless females that must walk through complex terrain to find ground dwelling host larvae burrows. Velvet ants are not central-place foragers (they do not return to an established nest site) so much of the previous work on spatial learning does not directly apply in this context. It was assumed that females primarily use chemosensory cues for navigation and burrow location instead of visual learning. This study, however, demonstrates that velvet ant females are able to use visual landmarks to find an inconspicuous exit in an aversion-motivation spatial learning task. A significant number of velvet ants learned to locate the exit after seven training trials and went to the previous location of the exit even after the maze had been rotated, showing that landmarks external to the maze were used to learn the escape location.     

Friend or foe? The role of latent inhibition in predator and non-predator labelling by coral reef fishes

In communities of high biodiversity, the ability to distinguish predators from non-predators is crucial for prey success. Learning often plays a vital role in the ability to distinguish species that are threatening from those that are not. Many prey animals learn to recognise predators based on a single conditioning event whereby they are exposed to the unknown predator at the same time as alarm cues released from injured conspecifics. The remarkable efficiency of such learning means that recognition mistakes may occur if prey inadvertently learn that a species is a predator when it is not. Latent inhibition is a means by which prey that are pre-exposed to an unknown species in the absence of negative reinforcement can learn that the unknown animal is likely not a threat. Learning through latent inhibition should be conservative because mistakenly identifying predators as non-predators can have fatal consequences. In this study, we demonstrated that a common coral reef fish, lemon damselfish, Pomacentrus moluccensis can learn to recognise a predator as non-threatening through latent inhibition. Furthermore, we showed that we could override the latent inhibition effect by conditioning the prey to recognise the predator numerous times. Our results highlight the ability of prey fish to continually update the information regarding the threat posed by other fishes in their vicinity.     

Evidence of teaching in atlantic spotted dolphins (Stenella frontalis) by mother dolphins foraging in the presence of their calves

Teaching is a powerful form of social learning, but there is little systematic evidence that it occurs in species other than humans. Using long-term video archives the foraging behaviors by mother Atlantic spotted dolphins (Stenella frontalis) were observed when their calves were present and when their calves were not present, including in the presence of non-calf conspecifics. The nine mothers we observed chased prey significantly longer and made significantly more referential body-orienting movements in the direction of the prey during foraging events when their calves were present than when their calves were not present, regardless of whether they were foraging alone or with another non-calf dolphin. Although further research into the potential consequences for the naïve calves is still warranted, these data based on the maternal foraging behavior are suggestive of teaching as a social-learning mechanism in nonhuman animals.     

Anuran tadpoles learn to recognize injury cues from members of the same prey guild

Recognition of predation risk from cues released from injured heterospecific could be beneficial when prey belongs to the same prey guild. Here, we performed three experiments. Experiment 1 showed that P. thaul tadpoles reduced their activity levels when exposed to conspecific injury cues, but not when exposed to amphipod injury cues. Experiment 2 tested whether P. thaul tadpoles can learn to recognize predation risk from chemical cues released from injured heterospecifics from the same prey guild (amphipod, Hyalella patagonica). A group of tadpoles were conditioned by exposing them to a specific concentration of amphipod injury cues paired with conspecific injury cues. Two days later, we evaluated changes in the activity of tadpoles when they were exposed to amphipod cues. As a control of learning, we used an unpaired group. Additionally, we used more control groups to fully investigate the learning mechanism. Our results showed that tadpoles can learn to recognize predation risk from injured amphipods and that the mechanism underlying the observed learned response could be associative. Experiment 3 replicated Experiment 2 and also showed that a low concentration of amphipod cues did not sustain that learning.     

When cues collide: use of stress and statistical cues to word boundaries by 7- to 9-month-old infants

Prior research suggests that stress cues are particularly important for English-hearing infants' detection of word boundaries. It is unclear, though, how infants learn to attend to stress as a cue to word segmentation. This series of experiments was designed to explore infants' attention to conflicting cues at different ages. Experiment 1 replicated previous findings: When stress and statistical cues indicated different word boundaries, 9-month-old infants used syllable stress as a cue to segmentation while ignoring statistical cues. However, in Experiment 2, 7-month-old infants attended more to statistical cues than to stress cues. These results raise the possibility that infants use their statistical learning abilities to locate words in speech and use those words to discover the regular pattern of stress cues in English. Infants at different ages may deploy different segmentation strategies as a function of their current linguistic experience.     

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.     

How do people solve the "weather prediction" task?: individual variability in strategies for probabilistic category learning

Probabilistic category learning is often assumed to be an incrementally learned cognitive skill, dependent on nondeclarative memory systems. One paradigm in particular, the weather prediction task, has been used in over half a dozen neuropsychological and neuroimaging studies to date. Because of the growing interest in using this task and others like it as behavioral tools for studying the cognitive neuroscience of cognitive skill learning, it becomes especially important to understand how subjects solve this kind of task and whether all subjects learn it in the same way. We present here new experimental and theoretical analyses of the weather prediction task that indicate that there are at least three different strategies that describe how subjects learn this task. (1) An optimal multi-cue strategy, in which they respond to each pattern on the basis of associations of all four cues with each outcome; (2) a one-cue strategy, in which they respond on the basis of presence or absence of a single cue, disregarding all other cues; or (3) a singleton strategy, in which they learn only about the four patterns that have only one cue present and all others absent. This variability in how subjects approach this task may have important implications for interpreting how different brain regions are involved in probabilistic category learning.     

Social learning and acquired recognition of a predator by a marine fish

Predation is known to influence the distribution of behavioural traits among prey individuals, populations and communities over both evolutionary and ecological time scales. Prey have evolved mechanisms of rapidly learning the identity of predators. Chemical cues are often used by prey to assess predation risk especially in aquatic systems where visual cues are unreliable. Social learning is a method of threat assessment common among a variety of freshwater fish taxa, which incorporates chemosensory information. Learning predator identities through social learning is beneficial to na?ve individuals as it eliminates the need for direct interaction with a potential threat. Although social learning is widespread throughout the animal kingdom, no research on the use of this mechanism exists for marine species. In this study, we examined the role of social learning in predator recognition for a tropical damselfish, Acanthochromis polyacanthus. This species was found to not only possess and respond to conspecific chemical alarm cues, but na?ve individuals were able to learn a predators' identity from experienced individuals, the process of social learning. Fish that learned to associate risk with the olfactory cue of a predator responded with the same intensity as conspecifics that were exposed to a chemical alarm cue from a conspecific skin extract.     

Learning, memorizing and apparent forgetting of chemical cues from new predators by Iberian green frog tadpoles

Many antipredator adaptations are induced by the prey’s ability to recognize chemical cues from predators. However, predator recognition often requires learning by prey individuals. Iberian green frog tadpoles (Pelophylax perezi) have the ability to learn new potential predators. Here, we tested the memory capabilities of Iberian green frog tadpoles. We conditioned tadpoles with chemicals cues from a non-predatory fish in conjunction with conspecific alarm cues, and examined whether tadpoles retained their conditioned response (reduction of activity level). We found that conditioned tadpoles reduced their activity levels in subsequent exposures to the non-predatory fish cues alone. Tadpoles were able to remember this association and reduced movement rate at least for 9 days after. The ability to learn and memorize potential predators may be especially important for the survivorship of prey species that are likely to find a high variety of predators. However, after those 9 days, there was a lack of response to the non-predatory fish cues alone in the absence of reinforcement. This could be explained if tadpoles behave according to the threat-sensitive predator avoidance hypothesis, and the perceived risk to the learning cue diminished over time, or it could be due to an apparent forgetting process to avoid non-adaptative responses to chemical cues of non-dangerous species that were randomly paired with alarm cues. Thus, this study demonstrates that green frog tadpoles in the absence of reinforcement remember the chemical cues of a learned predator only for a limited time that may be adaptative in a threat-sensitive context.     

Learning and foraging efficiency in German cockroaches, Blattella germanica (L.) (Insecta: Dictyoptera)

We analysed, under laboratory test conditions, how German cockroach larvae oriented their outgoing foraging trip from their shelter. Our results stressed the importance of external factors, like availability and spatial distribution of food sources, in the choice of a foraging strategy within their home range. When food sources were randomly distributed, larvae adopted a random food search strategy. When food distribution was spatially predictable and reliable, cockroaches were able to relate the presence of food with a landmark during a 3-day training period and to develop an oriented search strategy. Cockroaches were able to associate learned spatial information about their home range to the presence of food resources and then to improve their foraging efficiency. However, conflict experiments revealed that detection of food odour overrode learned landmark cues. Received: 16 October 1999 / Accepted after revision: 18 July 2000     

The sectored foraging field: a novel design to quantify spatial strategies, learning, memory, and emotion

Although Norway rats are naturally gregarious, males typically live alone at some point during adulthood. Different social ecologies often require different learning strategies and also modulate response to stressors and gonadal development. To measure effects of the social environment on the interaction between cognition and emotion during aging, we focused on a natural learning context and devised the sectored foraging field, a progressively difficult spatial navigation task. Here, we describe how this apparatus and protocol permits multiple learning strategies in a minimally stressful environment, enabling finely graded analyses of cognition and emotionality. Male Sprague-Dawley rats living alone throughout adulthood adopted a sex-typic discernible spatial strategy. In contrast, males housed in group contexts utilized an algorithmic kinesthetic strategy, repeating the same motor action until they found food. Removal of food and distal, but not local cues, elicited anxious alertness, particularly in group-housed males. Cognitive performance of group-housed rats subsequent to food and cue removal was significantly impaired, yet enhanced in isolates.     

Transfer of metacognitive skills and hint seeking in monkeys

Metacognition is knowledge that can be expressed as confidence judgments about what one knows (monitoring) and by strategies for learning what one does not know (control). Although there is a substantial literature on cognitive processes in animals, little is known about their metacognitive abilities. Here we show that rhesus macaques, trained previously to make retrospective confidence judgments about their performance on perceptual tasks, transferred that ability immediately to a new perceptual task and to a working memory task. We also show that monkeys can learn to request "hints" when they are given problems that they would otherwise have to solve by trial and error. This study demonstrates, for the first time, that nonhuman primates share with humans the ability to monitor and transfer their metacognitive ability both within and between different cognitive tasks, and to seek new knowledge on a need-to-know basis.     

Strategies in probabilistic categorization: results from a new way of analyzing performance

The "Weather Prediction" task is a widely used task for investigating probabilistic category learning, in which various cues are probabilistically (but not perfectly) predictive of class membership. This means that a given combination of cues sometimes belongs to one class and sometimes to another. Prior studies showed that subjects can improve their performance with training, and that there is considerable individual variation in the strategies subjects use to approach this task. Here, we discuss a recently introduced analysis of probabilistic categorization, which attempts to identify the strategy followed by a participant. Monte Carlo simulations show that the analysis can, indeed, reliably identify such a strategy if it is used, and can identify switches from one strategy to another. Analysis of data from normal young adults shows that the fitted strategy can predict subsequent responses. Moreover, learning is shown to be highly nonlinear in probabilistic categorization. Analysis of performance of patients with dense memory impairments due to hippocampal damage shows that although these patients can change strategies, they are as likely to fall back to an inferior strategy as to move to more optimal ones.     

Self-controlled visual discrimination learning of group-housed dwarf goats (Capra hircus): behavioral strategies and effects of relocation on learning and memory

In most studies on animal learning, individual animals are tested separately in a specific learning environment and with a limited number of trials per day. An alternative approach is to test animals in a familiar environment in their social group. In this study, the authors--applying a fully automated learning device--investigated voluntary, self-controlled visual shape discrimination learning of group-housed dwarf goats (Capra hircus). The majority of the tested goats showed successful shape discrimination, which indicates the adaptive value of an effective learning strategy. However, in each group, a few individual goats developed behavioral strategies different from shape discrimination to get reward. Relocation impairs memory retrieval (probably by attention shifting) only temporarily for previously learnt shapes. The results demonstrate the usefulness of a self-controlled learning paradigm to assess learning abilities of social species in their normal social settings. This may be especially relevant for captive animals to improve their welfare.     

WHY A BRAIN CAPABLE OF LANGUAGE EVOLVED ONLY ONCE: PREFRONTAL CORTEX AND SYMBOL LEARNING

Abstract. Language and information processes are critical issues in scientific controversies regarding the qualities that epitomize humanness. Whereas some theorists claim human mental uniqueness with regard to language, others point to successes in teaching language skills to other animals. However, although these animals may learn names for things, they show little ability to utilize a complex framework of symbolic reference. In such a framework, words or other symbols refer not only to objects and concepts but also to sequential and hierarchical relationships with other symbols. This process is essential to human mental operations, including language, mathematics, and music. In humans, these operations may have coevolved with the prefrontal area of the cerebral cortex, which is proportionately much larger in humans than in other animals and more intricately linked with other areas of the brain. Analysis of the structure and function of the prefrontal area suggests that it is centrally involved in the operation of higher-order associative relationships involving the subordination of one set of associations to another. This alternate learning strategy apparently appeared at the cost of certain sensory, motor, or limbic abilities. The payoff was symbolic thinking. Humans thus are unique among species, not just for their highly developed language ability but for their odd style of thinking and learning.     

Short-term gains, long-term pains: How cues about state aid learning in dynamic environments

Successful investors seeking returns, animals foraging for food, and pilots controlling aircraft all must take into account how their current decisions will impact their future standing. One challenge facing decision makers is that options that appear attractive in the short-term may not turn out best in the long run. In this paper, we explore human learning in a dynamic decision making task which places short- and long-term rewards in conflict. Our goal in these studies was to evaluate how people’s mental representation of a task affects their ability to discover an optimal decision strategy. We find that perceptual cues that readily align with the underlying state of the task environment help people overcome the impulsive appeal of short-term rewards. Our experimental manipulations, predictions, and analyses are motivated by current work in reinforcement learning which details how learners value delayed outcomes in sequential tasks and the importance that “state” identification plays in effective learning.     

Conditional visuo-motor learning and dimension reduction

Conditional visuo-motor learning consists in learning by trial and error to associate visual cues with correct motor responses, that have no direct link. Converging evidence supports the role of a large brain network in this type of learning, including the prefrontal and the premotor cortex, the basal ganglia (BG) and the hippocampus. In this paper we focus on the role of a major structure of the BG, the striatum. We first present behavioral results and electrophysiological data recorded from this structure in monkeys engaged in learning new visuo-motor associations. Visual stimuli were presented on a video screen and the animals had to learn, by trial and error, to select the correct movement of a joystick, in order to receive a liquid reward. Behavioral results revealed that the monkeys used a sequential strategy, whereby they learned the associations one by one although they were presented randomly. Human subjects, tested on the same task, also used a sequential strategy. Neuronal recordings in monkeys revealed learning-related modulations of neural activity in the striatum. We then present a mathematical model inspired by viability theory developed to implement the use of strategies during learning. This model complements existing models of the BG based on reinforcement learning (RL), which do not take into account the use of strategies to reduce the dimension of the learning space.