Stronger neural dynamics capture changes in infants' visual working memory capacity over development

Visual working memory (VWM) capacity has been studied extensively in adults, and methodological advances have enabled researchers to probe capacity limits in infancy using a preferential looking paradigm. Evidence suggests that capacity increases rapidly between 6 and 10 months of age. To understand how the VWM system develops, we must understand the relationship between the looking behavior used to study VWM and underlying cognitive processes. We present a dynamic neural field model that captures both real-time and developmental processes underlying performance. Three simulation experiments show how looking is linked to VWM processes during infancy and how developmental changes in performance could arise through increasing neural connectivity. These results provide insight into the sources of capacity limits and VWM development more generally.     

Infant Attention Grows Up: The Emergence of a Developmental Cognitive Neuroscience Perspective

Visual attention has long been regarded as a tool for studying the development of basic cognitive skills in infancy and early childhood. However, over the past decade, the development of attention in early life has emerged as an important topic of research in its own right. This essay describes recent changes in the methods used to study attention in infancy, and in the nature of inferences about the early development of attention, as both research and theory in the area have become progressively integrated with models of attention from cognitive science and neuroscience.     

The teleological stance: Past,present, and future

We review the support for, and criticisms of, the teleological stance theory, often described as a foundation for goal‐directed action understanding early in life. A major point of contention in the literature has been how teleological processes and assumptions of rationality are represented and understood in infancy, and this debate has been largely centered on three paradigms. Visual habituation studies assess infant's abilities to retrospectively assess teleological processes; the presence of such processes is supported by the literature. Rational imitation is a phenomenon that has been questioned both theoretically and empirically, and there is currently little support for this concept in the literature. The involvement of teleological processes in action prediction is unclear. To date, the ontology of teleological processes remains unspecified. To remedy this, we present a new action‐based theory of teleological processes (here referred to as the embodied account of teleological processes), based on the development of goal‐directed reaching with its origin during the fetal period and continuous development over the first few months of life.     

Neuroimaging the sleeping brain: Insight on memory functioning in infants and toddlers

Episodic memory, or the ability to remember past events with specific detail, is central to the human experience and is related to learning and adaptive functioning in a variety of domains. In typically developing children, episodic memory emerges during infancy and improves during early childhood and beyond. Developmental processes within the hippocampus are hypothesized to be primarily responsible for both the early emergence and persistence of episodic memory in late infancy and early childhood. However, these hypotheses are based on non-human models. In-vivo investigations in early human development of hippocampal processes have been significantly limited by methodological challenges in acquiring neuroimaging data, particularly task-related functional neuroimaging data, from infants and toddlers. Recent studies in adults have shown neural activity in the brain regions supporting episodic memory during slow-wave sleep using functional magnetic resonance imaging (fMRI), and fMRI has been increasingly utilized in infancy and early childhood to address other research questions. We review initial evidence and present preliminary data showing the promise of this approach for examining hippocampal contribution to how infants and toddlers remember individual events, and their association with information about the context in which the event occurred. Overall, our review, integrated with the presentation of some preliminary data provides insight on leveraging sleep to gain new perspectives on early memory functioning.     

Competitive short-term and long-term memory processes in spatial habituation

Exposure to a spatial location leads to habituation of exploration such that, in a novelty preference test, rodents subsequently prefer exploring a novel location to the familiar location. According to Wagner's (1981) theory of memory, short-term and long-term habituation are caused by separate and sometimes opponent processes. In the present study, this dual-process account of memory was tested. Mice received a series of exposure training trials to a location before receiving a novelty preference test. The novelty preference was greater when tested after a short, rather than a long, interval. In contrast, the novelty preference was weaker when exposure training trials were separated by a short, rather than a long interval. Furthermore, it was found that long-term habituation was determined by the independent effects of the amount of exposure training and the number of exposure training trials when factors such as the intertrial interval and the cumulative intertrial interval were controlled. A final experiment demonstrated that a long-term reduction of exploration could be caused by a negative priming effect due to associations formed during exploration. These results provide evidence against a single-process account of habituation and suggest that spatial habituation is determined by both short-term, recency-based memory and long-term, incrementally strengthened memory.     

Autonomy in Action: Linking the Act of Looking to Memory Formation in Infancy via Dynamic Neural Fields

Looking is a fundamental exploratory behavior by which infants acquire knowledge about the world. In theories of infant habituation, however, looking as an exploratory behavior has been deemphasized relative to the reliable nature with which looking indexes active cognitive processing. We present a new theory that connects looking to the dynamics of memory formation and formally implement this theory in a Dynamic Neural Field model that learns autonomously as it actively looks and looks away from a stimulus. We situate this model in a habituation task and illustrate the mechanisms by which looking, encoding, working memory formation, and long‐term memory formation give rise to habituation across multiple stimulus and task contexts. We also illustrate how the act of looking and the temporal dynamics of learning affect each other. Finally, we test a new hypothesis about the sources of developmental differences in looking.     

Common processes may contribute to extinction and habituation

Psychologists routinely attribute the characteristics of conditioned behavior to complicated cognitive processes. For example, many of the characteristics of behavior undergoing extinction have been attributed to retrieval from memory. The authors argue that these characteristics may result from the simpler process of habituation. In particular, conditioned responding may decrease during extinction partially because habituation occurs to the stimuli that control responding when those stimuli are presented repeatedly or for a prolonged time (e.g., the experimental context, the conditioned stimulus in classical conditioning). This idea is parsimonious, has face validity, and evokes only processes that are well established by other evidence. In addition, behavior undergoing extinction shows 12 of the fundamental properties of behavior undergoing habituation. However, this model probably cannot provide a complete theory of extinction. It provides no obvious explanation for some of the other characteristics of extinguished behavior.     

Behavioral and genetic characterization of habituation using Caenorhabditis elegans

This review surveys the literature that investigates the behavioral characterization and cellular and molecular mechanisms of habituation using the model organism Caenorhabditis elegans. In 1990, C. elegans was first observed to show habituation to a non-localized mechanical tap. The parameters that govern this behavioral plasticity in C. elegans were subsequently characterized, which lead to the important hypothesis that habituation is mediated by multiple mechanisms. Many tools are available to C. elegans researchers that allow for relatively easy genetic manipulation. This has lead to a number of recent genetic studies that have begun to identify key genes and molecules that play a role in the mechanisms of habituation. Some of these genes include a vesicular glutamate transporter, a glutamate receptor subunit, a dopamine receptor and downstream intracellular signaling molecules, such as G proteins and kinases. Some of these genes only affect certain parameters of habituation, but not others supporting the hypothesis that multiple mechanisms mediate habituation. The field of research has also led to the dissection of different phases of memory (short-term vs. long-term memory for habituation), which are triggered by different training paradigms. The differences in mechanism between these various forms of memory are also beginning to be revealed.     

Evidence for habituation of the irrelevant-sound effect on serial recall

Working memory theories make opposing predictions as to whether the disruptive effect of task-irrelevant sound on serial recall should be attenuated after repeated exposure to the auditory distractors. Although evidence of habituation has emerged after a passive listening phase, previous attempts to observe habituation to to-be ignored distractors on a trial-by-trial basis have proven to be fruitless. With the present study, we suggest that habituation to auditory distractors occurs, but has often been overlooked because past attempts to measure habituation in the irrelevant-sound paradigm were not sensitive enough. In a series of four experiments, the disruptive effects of to-be-ignored speech and music relative to a quiet control condition were markedly reduced after eight repetitions, regardless of whether trials were presented in blocks (Exp. 1) or in a random order (Exp. 2). The auditory distractor’s playback direction (forward, backward) had no effect (Exp. 3). The same results were obtained when the auditory distractors were only presented in a retention interval after the presentation of the to-be-remembered items (Exp. 4). This pattern is only consistent with theoretical accounts that allow for attentional processes to interfere with the maintenance of information in working memory.     

Nonassociative learning processes determine expression and extinction of conditioned fear in mice

Freezing to a tone following auditory fear conditioning is commonly considered as a measure of the strength of the tone-shock association. The decrease in freezing on repeated nonreinforced tone presentation following conditioning, in turn, is attributed to the formation of an inhibitory association between tone and shock that leads to a suppression of the expression of fear. This study challenges these concepts for auditory fear conditioning in mice. We show that acquisition of conditioned fear by a few tone-shock pairings is accompanied by a nonassociative sensitization process. As a consequence, the freezing response of conditioned mice seems to be determined by both associative and nonassociative memory components. Our data suggest that the intensity of freezing as a function of footshock intensity is primarily determined by the nonassociative component, whereas the associative component is more or less categorical. We next demonstrate that the decrease in freezing on repeated nonreinforced tone presentation following conditioning shows fundamental properties of habituation. Thus, it might be regarded as a habituation-like process, which abolishes the influence of sensitization on the freezing response to the tone without affecting the expression of the associative memory component. Taken together, this study merges the dual-process theory of habituation with the concept of classical fear conditioning and demonstrates that sensitization and habituation as two nonassociative learning processes may critically determine the expression of conditioned fear in mice.     

Recall in Infancy: A Neurodevelopmental Account

ABSTRACT— Relations between developments in neural structures and changes in memory in infancy are a relatively recent focus of research. Greater knowledge about brain development, as well as methodological advances such as combined use of behavioral and electrophysiological techniques, have led to the generation and testing of specific hypotheses regarding sources of age-related change. Theory and data converge to suggest that the early-stage processes of encoding and consolidation are a significant source of age-related variability in memory early in life. Additional research is needed to determine how these processes change and interact with myriad other determinants of recall.     

Analyses of habituation in Caenorhabditis elegans

Although the nonassociative form of learning, habituation, is often described as the simplest form of learning, remarkably little is known about the cellular processes underlying its behavioral expression. Here, we review research on habituation in the nematode Caenorhabditis elegans that addresses habituation at behavioral, neural circuit, and genetic levels. This work highlights the need to understand the dynamics of a behavior before attempting to determine its underlying mechanism. In many cases knowing the characteristics of a behavior can direct or guide a search for underlying cellular mechanisms. We have highlighted the importance of interstimulus interval (ISI) in both short- and long-term habituation and suggested that different cellular mechanisms might underlie habituation at different ISIs. Like other organisms, C. elegans shows both accumulation of habituation with repeated training blocks and long-term retention of spaced or distributed training, but not for massed training. Exposure to heat shock during the interblock intervals eliminates the long-term memory for habituation but not the accumulation of short-term habituation over blocks of training. Analyses using laser ablation of identified neurons, and of identified mutants have shown that there are multiple sites of plasticity for the response and that glutamate plays a role in long-term retention of habituation training.     

Perception of individuality in bat vocal communication: discrimination between, or recognition of, interaction partners?

Different cognitive processes underlying voice identity perception in humans may have precursors in mammals. A perception of vocal signatures may govern individualised interactions in bats, which comprise species living in complex social structures and are nocturnal, fast-moving mammals. This paper investigates to what extent bats recognise, and discriminate between, individual voices and discusses acoustic features relevant for accomplishing these tasks. In spontaneous presentation and habituation–dishabituation experiments, we investigated how Megaderma lyra perceives and evaluates stimuli consisting of contact call series with individual-specific signatures from either social partners or unknown individuals. Spontaneous presentations of contact call stimuli from social partners or unknown individuals elicited strong, but comparable reactions. In the habituation–dishabituation experiments, bats dishabituated significantly to any new stimulus. However, reactions were less pronounced to a novel stimulus from the bat used for habituation than to stimuli from other bats, irrespective of familiarity, which provides evidence for identity discrimination. A model separately assessing the dissimilarity of stimuli in syllable frequencies, syllable durations and inter-call intervals relative to learned memory templates accounted for the behaviour of the bats. With respect to identity recognition, the spontaneous presentation experiments were not conclusive. However, the habituation–dishabituation experiments suggested that the bats recognised voices of social partners as the reaction to a re-habituation stimulus differed after a dishabituation stimulus from a social partner and an unknown bat.     

Genetic differences in response to novelty and spatial memory using a two-trial recognition task in mice

A two-trial memory task, based on a free-choice exploration paradigm in a Y-maze, was previously developed to study recognition processes in Sprague-Dawley rats. Because this paradigm avoids the use of electric shock or deprivation that may have nonspecific effects and does not require learning of a rule, it may be particularly useful for studying memory in mice. Four inbred strains (Balb/cByJ, DBA/2J, C57BL/6J, and SJL/J), an F1 hybrid (C57BL/6 x SJL/J), and one outbred strain (CD1) were used to validate this task in mice and to characterize a strain distribution in response to novelty and working memory. Exploration was measured with a short (2 min) intertrial interval (ITI) between acquisition and retrieval, while memory was examined with longer intervals (30 min, 1 h, and 2 h). A study of the time course of the response to novelty revealed varying degrees of preference and/or habituation to novelty among the different strains, with CD1 exhibiting a very high response to novelty and others showing lower (C57 x SJL hybrids) to complete absence (SJL) of exploration of novelty. Memory span, assessed with increasing ITIs, varied widely among strains from 30 min (C57 x SJL hybrids) to at least 2 h (C57 and BALB). Such demonstrated sensitivity to a wide range of behavioral phenotypes supports the use of this spatial memory task as an effective tool for the study of genetic influences on the response to novelty and recognition processes in mice.     

Infant information processing and family history of specific language impairment: converging evidence for RAP deficits from two paradigms

An infant's ability to process auditory signals presented in rapid succession (i.e. rapid auditory processing abilities [RAP]) has been shown to predict differences in language outcomes in toddlers and preschool children. Early deficits in RAP abilities may serve as a behavioral marker for language-based learning disabilities. The purpose of this study is to determine if performance on infant information processing measures designed to tap RAP and global processing skills differ as a function of family history of specific language impairment (SLI) and/or the particular demand characteristics of the paradigm used. Seventeen 6- to 9-month-old infants from families with a history of specific language impairment (FH+) and 29 control infants (FH-) participated in this study. Infants' performance on two different RAP paradigms (head-turn procedure [HT] and auditory-visual habituation/recognition memory [AVH/RM]) and on a global processing task (visual habituation/recognition memory [VH/RM]) was assessed at 6 and 9 months. Toddler language and cognitive skills were evaluated at 12 and 16 months. A number of significant group differences were seen: FH+ infants showed significantly poorer discrimination of fast rate stimuli on both RAP tasks, took longer to habituate on both habituation/recognition memory measures, and had lower novelty preference scores on the visual habituation/recognition memory task. Infants' performance on the two RAP measures provided independent but converging contributions to outcome. Thus, different mechanisms appear to underlie performance on operantly conditioned tasks as compared to habituation/recognition memory paradigms. Further, infant RAP processing abilities predicted to 12- and 16-month language scores above and beyond family history of SLI. The results of this study provide additional support for the validity of infant RAP abilities as a behavioral marker for later language outcome. Finally, this is the first study to use a battery of infant tasks to demonstrate multi-modal processing deficits in infants at risk for SLI.     

Relationship between food habituation and reinforcing efficacy of food

Reinforcing value and habituation are two processes that have been used to study eating behaviors, but no research has examined their relationship, how they relate to energy intake, and whether they respond in a similar manner to food deprivation. Twenty-two female subjects were randomized to food deprived or non-deprived conditions, and assessed for food reinforcement, habituation to food and ad libitum eating. Results showed food reinforcement and habituation are correlated (r = 0.62, p = 0.002) and both independently predict energy intake. Hierarchical regression showed that the rate of habituation accounted for 30 percent of the variance in eating (p = 0.008), and adding food reinforcement increased the amount of variance accounted for up to 57.5 percent (p < 0.05). This suggests that both processes may influence energy intake in a meal.     

Memory in 3‐month‐old infants benefits from a short nap

A broad range of studies demonstrate that sleep has a facilitating role in memory consolidation (see Rasch & Born, 2013 ). Whether sleep‐dependent memory consolidation is also apparent in infants in their first few months of life has not been investigated. We demonstrate that 3‐month‐old infants only remember a cartoon face approximately 1.5–2 hours after its first presentation when a period of sleep followed learning. Furthermore, habituation time, that is, the time to become bored with a stimulus shown repetitively, correlated negatively with the density of infant sleep spindles, implying that processing speed is linked to specific electroencephalographic components of sleep. Our findings show that without a short period of sleep infants have problems remembering a newly seen face, that sleep enhances memory consolidation from a very early age, highlighting the importance of napping in infancy, and that infant sleep spindles may be associated with some aspects of cognitive ability.     

Examining individual differences in infants’ habituation patterns using objective quantitative techniques

The assessment of individual differences in infant habituation patterns is important for answering basic questions about continuity in cognitive development. Nevertheless, there are flaws with existing methods for determining relevant parameters of the cognitive processes associated with habituation. In this paper, a more rigorous, model-based alternative approach is illustrated. The approach demonstrates how the habituation data of individual infants may be fit by specific functions, how habituation may be distinguished from random responding, and how the parameter estimates of individual infants’ habituation functions might be analyzed for meaningful subgroups or clusters. The model-based approach provides novel insights about individual subgroups when applied to a real habituation data set and thereby demonstrates the feasibility and utility of the techniques advocated.     

Reconceptualizing inhibition of return as

Inhibition of return (IOR) is an effect on spatial attention whereby reaction times to a target presented at a location where a stimulus had recently been presented are increased, as opposed to when a target is presented at a new location. Despite early reports that habituation is not responsible for the IOR effect, the human cognitive literature provides indirect evidence in favor of the possibility. In addition, recent neurophysiological studies provide direct support for the idea that habituation is at least a contributing source for the IOR effect. The present article describes how habituation may account for the IOR effect and explores some of the predictions that this hypothesis suggests.     

A new group-training procedure for habituation demonstrates that presynaptic glutamate release contributes to long-term memory in Caenorhabditis elegans

In the experiments reported here we have developed a new group-training protocol for assessing long-term memory for habituation in Caenorhabditis elegans. We have replicated all of the major findings of the original single-worm protocol using the new protocol: (1) distributed training produced long-term retention of training, massed training did not; (2) distributed training at long interstimulus intervals (ISIs) produced long-term retention, short ISIs did not; and (3) long-term memory for distributed training is protein synthesis-dependent as it could be blocked by heat shock during the inter-block interval. In addition, we have shown that long-term memory for habituation is graded, depending on the number of blocks of stimuli in training. The inter-block interval must be >40 min for long-term retention of training to occur. Finally, we have tested long-term memory for habituation training in a strain of worms with a mutation in a vesicular glutamate transporter in the sensory neurons that transduce tap (eat-4). The results from these eat-4 worms indicate that glutamate release from the sensory neurons has an important role in the formation of long-term memory for habituation.