Protein synthesis-dependent long-term memory induced by one single associative training trial in the parasitic wasp Lariophagus distinguendus

Protein synthesis-dependent long-term memory in Apis mellifera and Drosophila melanogaster is formed after multiple trainings that are spaced in time. The parasitic wasp Lariophagus distinguendus remarkably differs from these species. It significantly responds to the artificial odor furfurylheptanoate (FFH) in olfactometer experiments, when this odor was presented during one single training trial, consisting of one sequence of host recognition behavior on a wheat grain infested by its hosts. Feeding wasps with actinomycin D erases the learned response 24 h after the training, demonstrating that protein synthesis-dependent long-term memory has been formed in L. distinguendus already after one single training.     

What matters in the associative learning of visual cues in foraging parasitoid wasps: colour or brightness?

Visual cues are known to be used by numerous animal taxa to gather information on quality and localisation of resources. Because environmental lighting can interfere with the spectral features of visual cues, the specific characteristics of the colour signals that promote forager decision and learning are still not known in the majority of insects (excepted in bees). We analysed the effect of previous experience on the use of visual information by the wasp Venturia canescens, a parasitoid of pyralidae, in the context of host searching. These parasitoids search for hosts concealed in several fruit species, so visual cues from the host microhabitat could play a key role in host finding. We also investigated the type of visual cues on which wasps based their decision. We tested whether wasps are able to associate an achromatic cue (brightness) or a chromatic one (hue, i.e. dominant wavelength and/or chroma) with the presence of hosts. Our results show that in the context of host foraging, chromatic cues are more reliable than brightness in achieving the associative learning process. Therefore, understanding the behavioural ecology of foraging should make use of the knowledge about the visual information used.     

The effect of presentation rate on implicit sequence learning in aging

Implicit sequence learning is thought to be preserved in aging when the to-be learned associations are first-order; however, when associations are second-order, older adults (OAs) tend to experience deficits as compared to young adults (YAs). Two experiments were conducted using a first (Experiment 1) and second-order (Experiment 2) serial-reaction time task. Stimuli were presented at a constant rate of either 800 milliseconds (fast) or 1200 milliseconds (slow). Results indicate that both age groups learned first-order dependencies equally in both conditions. OAs and YAs also learned second-order dependencies, but the learning of lag-2 information was significantly impacted by the rate of presentation for both groups. OAs showed significant lag-2 learning in slow condition while YAs showed significant lag-2 learning in the fast condition. The sensitivity of implicit sequence learning to the rate of presentation supports the idea that OAs and YAs different processing speeds impact the ability to build complex associations across time and intervening events.     

Conceptual knowledge attenuates viewpoint dependency in visual object recognition

Learning verbal semantic knowledge for objects has been shown to attenuate recognition costs incurred by changes in view from a learned viewpoint. Such findings were attributed to the semantic or meaningful nature of the learned verbal associations. However, recent findings demonstrate surprising benefits to visual perception after learning even noninformative verbal labels for stimuli. Here we test whether learning verbal information for novel objects, independent of its semantic nature, can facilitate a reduction in viewpoint-dependent recognition. To dissociate more general effects of verbal associations from those stemming from the semantic nature of the associations, participants learned to associate semantically meaningful (adjectives) or nonmeaningful (number codes) verbal information with novel objects. Consistent with a role of semantic representations in attenuating the viewpoint-dependent nature of object recognition, the costs incurred by a change in viewpoint were attenuated for stimuli with learned semantic associations relative to those associated with nonmeaningful verbal information. This finding is discussed in terms of its implications for understanding basic mechanisms of object perception as well as the classic viewpoint-dependent nature of object recognition.     

Learning about non-predators and safe places: the forgotten elements of risk assessment

A fundamental prerequisite for prey to avoid being captured is the ability to distinguish dangerous stimuli such as predators and risky habitats from non-dangerous stimuli such as non-predators and safe locations. Most research to date has focused on mechanisms allowing prey to learn to recognize risky stimuli. The paradox of learned predator recognition is that its remarkable efficiency leaves room for potentially costly mistakes if prey inadvertently learn to recognize non-predatory species as dangerous. Here, we pre-exposed embryonic woodfrogs, Rana sylvatica, to the odour of a tiger salamander, Ambystoma tigrinum, without risk reinforcement, and later try to teach the tadpoles to recognize the salamander, a red-bellied newt Cynops pyrrhogaster—a closely related amphibian, or a goldfish, Carassius auratus, as a predator. Tadpoles were then tested for their responses to salamander, newt or fish odour. Pre-exposure to salamander did not affect the ability of tadpoles to learn to recognize goldfish as a predator. However, the embryonic pre-exposure to salamanders inhibited the subsequent learning of salamanders as a potential predator, through a mechanism known as latent inhibition. The embryonic pre-exposure also prevented the learned recognition of novel newts, indicating complete generalization of non-predator recognition. This pattern does not match that of generalization of predator recognition, whereby species learning to recognize a novel predator do respond, but not as strongly, to novel species closely related to the known predator. The current paper discusses the costs of making recognition mistakes within the context of generalization of predators and dangerous habitats versus generalization of non-predators and safe habitats and highlights the asymmetry in which amphibians incorporate information related to safe versus risky cues in their decision-making. Mechanisms such as latent inhibition allow a variety of prey species to collect information about non-threatening stimuli, as early as during their embryonic development, and to use this information later in life to infer the danger level associated with the stimuli.     

How to measure patch encounter rate: decision-making mechanisms in the parasitic wasp <Emphasis Type="Italic">Asobara tabida</Emphasis>

Parasitic wasps are faced with the decision of where and for how long to search for hosts. Their leaving decisions depend on the rate at which new host-containing patches are encountered: parasitoids increase foraging efficiency by leaving earlier when patch encounter rates become higher. The mechanisms by which these often tiny insects can assess patch encounter rates have not been thoroughly investigated so far. The aim of the present study, where females of the braconid wasp Asobara tabida encountered patches after varying time intervals, was to measure the shape of the travel–time response curve and to analyse how information on inter-patch distances is translated into foraging behaviour. I examined several proxies for travel-time duration, like those of physiological nature as egg content, cues of senescence, amount of energy spent, or muscle fatigue, as well as true cognitive mechanisms, like measurement of distance or interval timing. Constraints in the wasp’s ability to detect patch borders accurately after travelling, e.g. habituation to the patch odour or receptor blocking, are also discussed. From the data presented, most of the above-mentioned mechanisms and constraints can be rejected to work for A. tabida. The effects of inter-patch travel time are strongest when they are short, and even though it cannot be excluded that time measures are processed using an internal clock, I suggest that a Bayesian-like mechanism of timing, the biological basis of which might involve the build-up of neurosecretory material, is the most likely candidate influencing leaving decisions in A. tabida.     

Wisdom and Learning from Important and Meaningful Life Experiences

According to the wisdom literature, learning from important and meaningful life experiences can foster wisdom. Leading others is one such experience. This paper explores empirically whether and how learning acquired from leadership experience can foster wisdom, which is defined as a real-life process encompassing three core components: cognitive integration, embodiment in actions, and positive effects for oneself and others. This paper consists of two studies. Study 1 investigated the learning acquired from leadership experience and its relationship with wisdom. Eight leaders in higher education in Taiwan participated in five interviews spanning 2 years which explored the lessons learned from their leadership experience. Analysis of the interviews found that leaders acquired rich and multidimensional learning from their leadership experience and that components of wisdom were involved in their learning and their application of the lessons learned. Study 2 examined whether the results of Study 1 could be generalized to a wider population of higher education leaders. An inventory of learning and wisdom compiled from Study 1 was administered to 94 Taiwanese higher education leaders twice within 8 months. Multivariate statistical analysis showed that leaders’ responses to items of both acquired learning and components of wisdom increased in 8 months and that these increases were strongly correlated. Results suggest that learning from important and meaningful life experiences can foster wisdom.     

Learning by observation in rhesus monkeys

Habit memory provides us with a vast repertoire of learned rules, including stimulus-reward associations, that ensures fast and adapted decision making in daily life. Because we share this ability with monkeys, lesion and recording studies in rhesus macaques have played a key role in understanding the neural bases of individual trial-and-error habit learning. Humans, however, can learn new rules at a lower cost via observation of conspecifics. The neural properties underlying this more ecological form of habit learning remain unexplored, and it is unclear whether the rhesus macaque can be a useful model in this endeavor. We addressed this issue by testing four monkeys from the same social group in their usual semi-natural habitat using a well-established marker of habit memory, concurrent discrimination learning. Each monkey learned 24 lists of 10 object-reward associations each. For one list out of two, monkeys could observe the testing session of another member of the group prior to being tested with the same list themselves. Learning was faster for these lists than for those learned solely by trial-and-error. Errors to criterion (9/10 correct responses) were reduced by 39%, and faultless performance could be achieved for up to 5 of the 10 pairs. These data demonstrate that rhesus macaques spontaneously observe a conspecific learning new stimulus-reward associations, and substantially benefit from this observation. They ascertain that the neural underpinnings of socially-mediated forms of habit learning can be explored using the powerful tools of monkey research, including neurophysiological recordings.     

Embryonic olfactory learning in frogs.

We examined the effect of embryonic olfactory experiences on behaviour after hatching in two species of anuran amphibians, Rana temporaria and Rana sylvatica. Odorants (orange and citral) injected into the egg were "learned" by the embryo and subsequently preferred by tadpoles after hatching. The observed preferences were specific to the odours experienced prior to hatching, and tadpoles discriminated between the odour experienced as embryos and a novel odour. The acquired preference was maintained after metamorphosis for those individuals that exhibited a preference as tadpoles. Preferences of tadpoles were also influenced "naturally" by odours present in the water surrounding the developing embryos. The experimentally induced olfactory preferences did not appear to influence the exhibition of sibling recognition abilities. The study represents the first demonstration of "embryonic" learning in amphibians, and the functions and importance of early olfactory learning for amphibians are discussed.     

Category label and response location shifts in category learning

The category shift literature suggests that rule-based classification, an important form of explicit learning, is mediated by two separate learned associations: a stimulus-to-label association that associates stimuli and category labels, and a label-to-response association that associates category labels and responses. Three experiments investigate whether information–integration classification, an important form of implicit learning, is also mediated by two separate learned associations. Participants were trained on a rule-based or an information–integration categorization task and then the association between stimulus and category label, or between category label and response location was altered. For rule-based categories, and in line with previous research, breaking the association between stimulus and category label caused more interference than breaking the association between category label and response location. However, no differences in recovery rate emerged. For information–integration categories, breaking the association between stimulus and category label caused more interference and led to greater recovery than breaking the association between category label and response location. These results provide evidence that information–integration category learning is mediated by separate stimulus-to-label and label-to-response associations. Implications for the neurobiological basis of these two learned associations are discussed.     

The nose tells it to the eyes: crossmodal associations between olfaction and vision

Crossmodal linkage between the olfactory and visual senses is still largely underexplored. In this study, we investigated crossmodal olfactory-visual associations by testing whether and how visual processing of objects is affected by the presence of olfactory cues. To this end, we explored the influence of prior learned associations between an odour (eg odour of orange) and a visual stimulus naturally associated with that odour (picture of orange) on the movements of the eyes over a complex scene. Participants were asked to freely explore a photograph containing an odour-related visual cue embedded among other objects while being exposed to the corresponding odour (subjects were unaware of the presence of the odour). Eye movements were recorded to analyse the order and distribution of fixations on each object of the scene. Our data show that the odour-related visual cue was explored faster and for a shorter time in the presence of the congruent odour. These findings suggest that odours can affect visual processing by attracting attention to the possible odour source and by facilitating its identification.     

Conflict between egg recognition and egg rejection decisions in common cuckoo (<Emphasis Type="Italic">Cuculus canorus</Emphasis>) hosts

Common cuckoos (Cuculus canorus) are obligate brood parasites, laying eggs into nests of small songbirds. The cuckoo hatchling evicts all eggs and young from a nest, eliminating hosts’ breeding success. Despite the consistently high costs of parasitism by common cuckoos, great reed warbler (Acrocephalus arundinaceus) hosts sometime accept and other times reject parasitic eggs. To explore the cognitive basis of this seemingly maladaptive variation in host responses, we documented differences in egg rejection rates within 1-day periods just before and during the egg-laying cycle across host nests. Hosts rejected cuckoo eggs at 28% of nests during the pre-egg-laying stage, but when cuckoos exchanged the first host egg with the parasite egg, rejections increased to 75%. Even later, when several host eggs remained in a nest after parasitism, rejection rate fell to 37.5%. Experimental parasitism with conspecific eggs on the first and second day of host laying showed a similar directional change in relative rejection rates, dropping from 35 to 0%. Mistakes in egg discrimination (ejection error and ejection cost) were observed mostly in the latter part of the laying cycle, mainly when nests contained 5–6 eggs. These correlational and experimental patterns of egg rejection support a cognitive process of egg discrimination through several shifts in hosts’ optimal acceptance thresholds of foreign eggs. The results are also consistent with the evolution of foreign egg rejection in the context of nest-sanitation (i.e. the removal of foreign objects). Our results suggest that common cuckoo hosts may recognize more eggs than they reject. This implies that the experience of the host with one or more of its own eggs in the clutch is a key factor in rejecting parasite eggs by allowing inspection and learning about their own clutch.     

Selective associations in one-day-old rats: taste-toxicosis and texture-shock aversion learning

One-day-old rats learned aversions to a novel taste paired with lithium-induced distress and to a tactile stimulus paired with brief electric shocks. However, aversions did not develop when taste was paired with shock or when the tactile stimulus was paired with lithium treatment. The aversions occurred only when lithium treatment immediately followed taste exposure and when shock was concurrent with exposure to the tactile stimulus. These findings indicate that selective associations in aversion learning are mediated by innate mechanisms that govern conditioning in the absence of extensive ontogenetic experience. The present research also shows that selective associations are sufficient for the occurrence of long-delay learning.     

Bedding down new words: Sleep promotes the emergence of lexical competition in visual word recognition

Lexical competition processes are widely viewed as the hallmark of visual word recognition, but little is known about the factors that promote their emergence. This study examined for the first time whether sleep may play a role in inducing these effects. A group of 27 participants learned novel written words, such as banara, at 8 am and were tested on their learning at 8 pm the same day (AM group), while 29 participants learned the words at 8 pm and were tested at 8 am the following day (PM group). Both groups were retested after 24 hours. Using a semantic categorization task, we showed that lexical competition effects, as indexed by slowed responses to existing neighbor words such as banana, emerged 12 h later in the PM group who had slept after learning but not in the AM group. After 24 h the competition effects were evident in both groups. These findings have important implications for theories of orthographic learning and broader neurobiological models of memory consolidation.     

Neurons in Human Temporal Cortex Active with Verbal Associative Learning

In neuronal activity recorded from human middle temporal gyrus during learning of associations between word pairs, a population was identified that had greater activity for associations that were learned rapidly during initial encoding compared to those learned slowly or not at all by an individual subject. This population can be separated from other neurons by the combination of inhibition during word reading when no learning is required and excitation during recent memory for words. These neurons are present in both hemispheres, predominately in deeper layers of cortex. During initial encoding, the increased activity appears at presentation of all word pairs but persists for several seconds only for the rapidly learned pairs, likely reflecting rehersal of items being learned. Human associative learning is related to activity of this specific population of “association” neurons, identified here for the first time.     

Pitches that Wire Together Fire Together: Scale Degree Associations Across Time Predict Melodic Expectations

The ongoing generation of expectations is fundamental to listeners’ experience of music, but research into types of statistical information that listeners extract from musical melodies has tended to emphasize transition probabilities and n-grams, with limited consideration given to other types of statistical learning that may be relevant. Temporal associations between scale degrees represent a different type of information present in musical melodies that can be learned from musical corpora using expectation networks, a computationally simple method based on activation and decay. Expectation networks infer the expectation of encountering one scale degree followed in the near (but not necessarily immediate) future by another given scale degree, with previous work suggesting that scale degree associations learned by expectation networks better predict listener ratings of pitch similarity than transition probabilities. The current work outlines how these learned scale degree associations can be combined to predict melodic continuations and tests the resulting predictions on a dataset of listener responses to a musical cloze task previously used to compare two other models of melodic expectation, a variable-order Markov model (IDyOM) and Temperley's music-theoretically motivated model. Under multinomial logistic regression, all three models explain significant unique variance in human melodic expectations, with coefficient estimates highest for expectation networks. These results suggest that generalized scale degree associations informed by both adjacent and nonadjacent relationships between melodic notes influence listeners’ melodic predictions above and beyond n-gram context, highlighting the need to consider a broader range of statistical learning processes that may underlie listeners’ expectations for upcoming musical events.     

The encoding process of nonconfigural information in contextual cuing

Jiang and Wagner (2004) demonstrated that individual target-distractor associations were learned in contextual cuing. We examined whether individual associations can be learned in efficient visual searches that do not involve attentional deployment to individual search items. In Experiment 1, individual associations were not learned during the efficient search tasks. However, in Experiment 2, where additional exposure duration of the search display was provided by presenting placeholders marking future locations of the search items, individual associations were successfully learned in the efficient search tasks and transferred to inefficient search. Moreover, Experiment 3 demonstrated that a concurrent task requiring attention does not affect the learning of the local visual context. These results clearly showed that attentional deployment is not necessary for learning individual locations and clarified how the human visual system extracts and preserves regularity in complex visual environments for efficient visual information processing.     

Parasitoid wasps’ exposure to host-infested plant volatiles affects their olfactory cognition of host-infested plants

Using Cotesia vestalis, a parasitoid wasp of diamondback moth larvae and three crucifer plant species (cabbage, komatsuna, and Japanese radish), we examined the effects of exposure to host-infested plant volatiles from one plant species on a newly emerged wasp’s subsequent olfactory cognition of host-infested plant volatiles from the same or different plant species. The preference of C. vestalis between infested and uninfested plant volatiles was tested in a choice chamber. Volatile-inexperienced wasps significantly preferred infested cabbage and infested radish volatiles, but not infested komatsuna volatiles. After exposure to infested cabbage volatiles, wasps showed a significant preference for infested cabbage volatiles, while the significant preference for infested radish volatiles that had been observed in inexperienced wasps was no longer observed. After exposure to infested komatsuna volatiles, wasps significantly preferred infested komatsuna volatiles, and the pre-exposure significant preferences for infested cabbage volatiles and infested radish volatiles remained. After exposure to infested radish volatiles, the significant preferences for infested cabbage and infested radish volatiles did not change. Furthermore, wasps showed a significant preference for infested komatsuna volatiles. The compound compositions of the volatile blends from the three infested plant species were grouped separately in a principal coordinates analysis. The experience-based cognition of C. vestalis for host-infested plant volatiles of three plant species is discussed.     

Song learning and cognitive ability are not consistently related in a songbird

Learned aspects of song have been hypothesized to signal cognitive ability in songbirds. We tested this hypothesis in hand-reared song sparrows (Melospiza melodia) that were tutored with playback of adult songs during the critical period for song learning. The songs developed by the 19 male subjects were compared to the model songs to produce two measures of song learning: the proportion of notes copied from models and the average spectrogram cross-correlation between copied notes and model notes. Song repertoire size, which reflects song complexity, was also measured. At 1 year of age, subjects were given a battery of five cognitive tests that measured speed of learning in the context of a novel foraging task, color association, color reversal, detour-reaching, and spatial learning. Bivariate correlations between the three song measures and the five cognitive measures revealed no significant associations. As in other studies of avian cognition, different cognitive measures were for the most part not correlated with each other, and this result remained true when 22 hand-reared female song sparrows were added to the analysis. General linear mixed models controlling for effects of neophobia and nest of origin indicated that all three song measures were associated with better performance on color reversal and spatial learning but were associated with worse performance on novel foraging and detour-reaching. Overall, the results do not support the hypothesis that learned aspects of song signal cognitive ability.     

Spatial metaphor in language can promote the development of cross‐modal mappings in children

Pitch is often described metaphorically: for example, Farsi and Turkish speakers use a ‘thickness’ metaphor (low sounds are ‘thick’ and high sounds are ‘thin’), while German and English speakers use a height metaphor (‘low’, ‘high’). This study examines how child and adult speakers of Farsi, Turkish, and German map pitch and thickness using a cross‐modal association task. All groups, except for German children, performed significantly better than chance. German‐speaking adults’ success suggests the pitch‐to‐thickness association can be learned by experience. But the fact that German children were at chance indicates that this learning takes time. Intriguingly, Farsi and Turkish children's performance suggests that learning cross‐modal associations can be boosted through experience with consistent metaphorical mappings in the input language.