Assessing learning and memory in pigs

In recent years, there has been a surge of interest in (mini) pigs (Sus scrofa) as species for cognitive research. A major reason for this is their physiological and anatomical similarity with humans. For example, pigs possess a well-developed, large brain. Assessment of the learning and memory functions of pigs is not only relevant to human research but also to animal welfare, given the nature of current farming practices and the demands they make on animal health and behavior. In this article, we review studies of pig cognition, focusing on the underlying processes and mechanisms, with a view to identifying. Our goal is to aid the selection of appropriate cognitive tasks for research into pig cognition. To this end, we formulated several basic criteria for pig cognition tests and then applied these criteria and knowledge about pig-specific sensorimotor abilities and behavior to evaluate the merits, drawbacks, and limitations of the different types of tests used to date. While behavioral studies using (mini) pigs have shown that this species can perform learning and memory tasks, and much has been learned about pig cognition, results have not been replicated or proven replicable because of the lack of validated, translational behavioral paradigms that are specially suited to tap specific aspects of pig cognition. We identified several promising types of tasks for use in studies of pig cognition, such as versatile spatial free-choice type tasks that allow the simultaneous measurement of several behavioral domains. The use of appropriate tasks will facilitate the collection of reliable and valid data on pig cognition.     

Implicit learning as an ability

The ability to automatically and implicitly detect complex and noisy regularities in the environment is a fundamental aspect of human cognition. Despite considerable interest in implicit processes, few researchers have conceptualized implicit learning as an ability with meaningful individual differences. Instead, various researchers (e.g., Reber, 1993; Stanovich, 2009) have suggested that individual differences in implicit learning are minimal relative to individual differences in explicit learning. In the current study of English 16–17 year old students, we investigated the association of individual differences in implicit learning with a variety of cognitive and personality variables. Consistent with prior research and theorizing, implicit learning, as measured by a probabilistic sequence learning task, was more weakly related to psychometric intelligence than was explicit associative learning, and was unrelated to working memory. Structural equation modeling revealed that implicit learning was independently related to two components of psychometric intelligence: verbal analogical reasoning and processing speed. Implicit learning was also independently related to academic performance on two foreign language exams (French, German). Further, implicit learning was significantly associated with aspects of self-reported personality, including intuition, Openness to Experience, and impulsivity. We discuss the implications of implicit learning as an ability for dual-process theories of cognition, intelligence, personality, skill learning, complex cognition, and language acquisition.     

Eliciting false memories on implicit and explicit memory tests after incidental learning

Abstract: In a false memory experiment, lists of semantic associates (e.g., newspaper, letter, book, etc.) were presented to three groups of participants to induce false memories for critical nonpresented (CN) words (e.g., read) in an incidental learning task. The control group simply estimated the frequency rate in everyday Japanese discourse of each word on a list. The imagery instruction group received an additional instruction to imagine a thematically related converging word from the target words on a list. Participants in the imagery plus writing group received the same instructions as those in the imagery instruction group, but were also required to write down the word they imagined for each list. The results from the implicit and explicit memory tests given after the incidental learning episode showed that the level of priming for CN words was equivalent to that for actually presented target words for all three groups on the implicit test, whereas explicit memory results showed that participants explicitly recognized more target words than CN words. The implications for implicit associative response and fuzzy‐trace theories of false memory, as well as implicit priming, are discussed.     

Effects of Arousal on Everyday Memory

The notion of an unidimensional continuum of arousal is difficult to sustain, as is the universality of predictions from the Yerkes-Dodson law. A brief his- torical account of how these difficulties have arisen is provided, as well as sketches of some theoretical alternatives that have appeared in the past 10 years. It is argued that this more recent theorizing can supply explanatory constructs to bring order to the data on the relation of increases in arousal to memory performance. The argument is illustrated by an analysis of a number of studies involving everyday memory performance, studies involving encod- ing of eyewitness memories or retrieval of complex motor sequences.     

Future directions for implicit learning: Toward a clarification of issues associated with knowledge representation and consciousness

Areas of agreement and disagreement regarding knowledge representation and consciousness within implicit learning research are reviewed. It is argued that further progress in the field requires more precise definitions of abstract and episodic knowledge, and of conscious and unconscious forms of cognition. In particular, we argue that implicit learning research should be informed by more general theories of memory and performance, and that concepts such as consciousness are unlikely to act as explanatory constructs within this approach.     

Retrieval during learning facilitates subsequent memory encoding

In multiple-list learning, retrieval during learning has been suggested to improve recall of the single lists by enhancing list discrimination and, at test, reducing interference. Using electrophysiological, oscillatory measures of brain activity, we examined to what extent retrieval during learning facilitates list encoding. Subjects studied 5 lists of items in anticipation of a final cumulative recall test and did either a retrieval or a no-retrieval task between study of the lists. Retrieval was from episodic memory (recall of the previous list), semantic memory (generation of exemplars from an unrelated category), or short-term memory (2-back task). Behaviorally, all 3 forms of retrieval enhanced recall of both previously and subsequently studied lists. Physiologically, the results showed an increase of alpha power (8-14 Hz) from List 1 to List 5 encoding when no retrieval activities were interpolated but no such increase when any of the 3 retrieval activities occurred. Brain-behavior correlations showed that alpha-power dynamics from List 1 to List 5 encoding predicted subsequent recall performance. The results suggest that, without intermittent retrieval, encoding becomes ineffective across lists. In contrast, with intermittent retrieval, there is a reset of the encoding process for each single list that makes encoding of later lists as effective as encoding of early lists.     

Testing complex animal cognition: Concept learning,proactive interference,and list memory

This article describes an approach for assessing and comparing complex cognition in rhesus monkeys and pigeons by training them in a sequence of synergistic tasks, each yielding a whole function for enhanced comparisons. These species were trained in similar same/different tasks with expanding training sets (8, 16, 32, 64, 128 … 1024 pictures) followed by novel‐stimulus transfer eventually resulting in full abstract‐concept learning. Concept‐learning functions revealed better rhesus transfer throughout and full concept learning at the 128 set, versus pigeons at the 256 set. They were then tested in delayed same/different tasks for proactive interference by inserting occasional tests within trial‐unique sessions where the test stimulus matched a previous sample stimulus (1, 2, 4, 8, 16 trials prior). Proactive‐interference functions revealed time‐based interference for pigeons (1, 10 s delays), but event‐based interference for rhesus (no effect of 1, 10, 20 s delays). They were then tested in list‐memory tasks by expanding the sample to four samples in trial‐unique sessions (minimizing proactive interference). The four‐item, list‐memory functions revealed strong recency memory at short delays, gradually changing to strong primacy memory at long delays over 30 s for rhesus, and 10 s for pigeons. Other species comparisons and future directions are discussed.     

Route selection by rats and humans in a navigational traveling salesman problem

Spatial cognition is typically examined in non-human animals from the perspective of learning and memory. For this reason, spatial tasks are often constrained by the time necessary for training or the capacity of the animal’s short-term memory. A spatial task with limited learning and memory demands could allow for more efficient study of some aspects of spatial cognition. The traveling salesman problem (TSP), used to study human visuospatial problem solving, is a simple task with modifiable learning and memory requirements. In the current study, humans and rats were characterized in a navigational version of the TSP. Subjects visited each of 10 baited targets in any sequence from a set starting location. Unlike similar experiments, the roles of learning and memory were purposely minimized; all targets were perceptually available, no distracters were used, and each configuration was tested only once. The task yielded a variety of behavioral measures, including target revisits and omissions, route length, and frequency of transitions between each pair of targets. Both humans and rats consistently chose routes that were more efficient than chance, but less efficient than optimal, and generally less efficient than routes produced by the nearest-neighbor strategy. We conclude that the TSP is a useful and flexible task for the study of spatial cognition in human and non-human animals.     

催产素对学习和记忆的调节效应：来自动物与人类的研究证据

作为一种神经肽, 催产素对于个体社会认知和情绪加工有着非常重要的调节作用, 其中就包括对在人们工作和生活中扮演着关键角色的学习和记忆活动的影响。采用不同模态技术的动物和人类研究一致表明了外源性催产素对于学习和记忆具有重要的调节作用, 这一作用可能是外源性催产素通过与多巴胺奖赏通路、边缘系统等学习和记忆关键脑网络中广泛分布的催产素受体相结合, 进而调整其功能状态实现的; 但与此同时, 催产素对学习和记忆的促进或抑制作用会因实验范式、刺激材料、给药时间、位置和剂量等因素的不同而存在差异。未来需要协同动物和人类研究的各自优势, 采用规范化的实验任务设置和给药程序克服当前该领域的研究局限, 并积极发掘催产素在干预相关精神疾病患者学习和记忆加工缺陷中的应用潜力。     

Mental time travel,memory and the social learning strategies tournament

The social learning strategies tournament was an open computer-based tournament investigating the best way to learn in a changing environment. Here we present an analysis of the impact of memory on the ability of strategies entered into the social learning strategies tournament (Rendell, Boyd, et al., 2010) to modify their own behavior to suit a changing environment. The tournament showed that a strategy's ability to remember the past and to predict the future were both key to its success. The possibility that a strategy needs to engage in an approximation of ‘mental time travel’ to succeed in the tournament strongly implies that investment in randomly timed social learning is not enough to guarantee success. A strategy must use social learning strategically with reference to both predicted future environmental states and past environmental states. We examine the two most successful strategies (DiscountMachine and Intergeneration) in terms of their use of memory and discuss the impact of their complex memory use on their ability to time learning moves strategically and track environmental change. The tournament suggests that the human capacity for mental time travel may have improved the efficiency of social learning and allowed humans to invest in more sophisticated social learning than is seen elsewhere in the animal kingdom.     

Treating animals as ends

Conclusion Starting with a moral theory famous for being antagonistic toward animal rights, I have argued that we do have direct duties toward some animals, specifically those animals most closely related to human beings, whose behavior is reasonably interpreted as the result of conscious choice. Like animal rights views, the Kantian view escapes the intuitive counter-examples leveled at simple versions of utilitarianism. It rules out causing pain to the protected animals and also rules out killing them painlessly. But the Kantian view does not rule out painless experimentation at the cost of ruling out even harmless observation of animals. Nor is it restricted to a doctrine of negative obligations. The Kantian view forbids actions we intuitively think are wrong, allows those we think are permissible, and enjoins those we think are praiseworthy.     

The neurobiology of learning and memory

The study of memory is a great challenge, perhaps the greatest in biological sciences. Memory involves changes in a tiny fraction of an extremely large pool of elements, a conclusion that makes the task of finding those changes using current technologies formidable. What can be done about this roadblock to neurological investigations of learning? One response that has become particularly productive in recent years is to study learning or learning-like phenomena in relatively simple "model" systems. The idea is to extract basic principles from these models in which molecular and anatomical details can be studied and then to use these in analyzing learning in higher regions of the brain. In this article we discuss current progress and emerging concepts derived from the simple system approach using animal models.     

Long-term associative learning predicts verbal short-term memory performance

Studies using tests such as digit span and nonword repetition have implicated short-term memory across a range of developmental domains. Such tests ostensibly assess specialized processes for the short-term manipulation and maintenance of information that are often argued to enable long-term learning. However, there is considerable evidence for an influence of long-term linguistic learning on performance in short-term memory tasks that brings into question the role of a specialized short-term memory system separate from long-term knowledge. Using natural language corpora, we show experimentally and computationally that performance on three widely used measures of short-term memory (digit span, nonword repetition, and sentence recall) can be predicted from simple associative learning operating on the linguistic environment to which a typical child may have been exposed. The findings support the broad view that short-term verbal memory performance reflects the application of long-term language knowledge to the experimental setting.     

Neurogenesis and the spacing effect: learning over time enhances memory and the survival of new neurons

Information that is spaced over time is better remembered than the same amount of information massed together. This phenomenon, known as the spacing effect, was explored with respect to its effect on learning and neurogenesis in the adult dentate gyrus of the hippocampal formation. Because the cells are generated over time and because learning enhances their survival, we hypothesized that training with spaced trials would rescue more new neurons from death than the same number of massed trials. In the first experiment, animals trained with spaced trials in the Morris water maze outperformed animals trained with massed trials, but there was not a direct effect of trial spacing on cell survival. Rather, animals that learned well retained more cells than animals that did not learn or learned poorly. Moreover, performance during acquisition correlated with the number of cells remaining in the dentate gyrus after training. In the second experiment, the time between blocks of trials was increased. Consequently, animals trained with spaced trials performed as well as those trained with massed, but remembered the location better two weeks later. The strength of that memory correlated with the number of new cells remaining in the hippocampus. Together, these data indicate that learning, and not mere exposure to training, enhances the survival of cells that are generated 1 wk before training. They also indicate that learning over an extended period of time induces a more persistent memory, which then relates to the number of cells that reside in the hippocampus.     

Category learning and multiple memory systems

Categorization is a vitally important skill that people use every day. Early theories of category learning assumed a single learning system, but recent evidence suggests that human category learning may depend on many of the major memory systems that have been hypothesized by memory researchers. As different memory systems flourish under different conditions, an understanding of how categorization uses available memory systems will improve our understanding of a basic human skill, lead to better insights into the cognitive changes that result from a variety of neurological disorders, and suggest improvements in training procedures for complex categorization tasks.     

Multivariate relationships between measures of learning style and memory

Three self-report instruments assessing “learning style” were administered to 106 undergraduate students: the Inventory of Learning Processes, the Study Behavior Questionnaire, and the Learning Style Inventory. Performance measures on word list and prose learning tasks were also obtained using both immediate and delayed retention tests. Canonical correlation analysis of the pairs of learning style instruments indicated that there was a small to moderate amount of overlapped variance. Inspection of the canonical variates revealed that what overlap existed was generally due to a common factor related to the depth of processing conception of memory. No significant canonical correlations were obtained between any of the learning style instruments and word list retention measures. However, the Inventory of Learning Processes and the Learning Style Inventory each obtained one significant canonical correlation with the set of prose retention measures. There was little overlap between sets of retention measures derived separately from prose and word list tasks. The findings have implications concerning (a) the validity and equivalency of available self-report instruments assessing learning style, (b) the role of the learning task in studying individual differences in learning and memory processes, and (c) the assessment of “depth of processing” at the level of individual differences.     

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.     

The effects of non-contingent extrinsic and intrinsic rewards on memory consolidation

Emotional and arousing treatments given shortly after learning enhance delayed memory retrieval in animal and human studies. Positive affect and reward induced prior to a variety of cognitive tasks enhance performance, but their ability to affect memory consolidation has not been investigated before. Therefore, we investigated the effects of a small, non-contingent, intrinsic or extrinsic reward on delayed memory retrieval. Participants (n=108) studied and recalled a list of 30 affectively neutral, imageable nouns. Experimental groups were then given either an intrinsic reward (e.g., praise) or an extrinsic reward (e.g., US 1 dollar). After a one-week delay, participants' retrieval performance for the word list was significantly better in the extrinsic reward groups, whether the reward was expected or not, than in controls. Those who received the intrinsic reward performed somewhat better than controls, but the difference was not significant. Thus, at least some forms of arousal and reward, even when semantically unrelated to the learned material, can effectively modulate memory consolidation. These types of treatments might be useful for the development of new memory intervention strategies.     

Hippocampal and neocortical contributions to memory: advances in the complementary learning systems framework

The complementary learning systems framework provides a simple set of principles, derived from converging biological, psychological and computational constraints, for understanding the differential contributions of the neocortex and hippocampus to learning and memory. The central principles are that the neocortex has a low learning rate and uses overlapping distributed representations to extract the general statistical structure of the environment, whereas the hippocampus learns rapidly using separated representations to encode the details of specific events while minimizing interference. In recent years, we have instantiated these principles in working computational models, and have used these models to address human and animal learning and memory findings, across a wide range of domains and paradigms. Here, we review a few representative applications of our models, focusing on two domains: recognition memory and animal learning in the fear-conditioning paradigm. In both domains, the models have generated novel predictions that have been tested and confirmed.