To update or to create? The influence of novelty and prior knowledge on memory networks.

Schemas are foundational mental structures shaped by experience. They influence behaviour, guide the encoding of new memories and are shaped by associated information. The adaptability of memory schemas facilitates the integration of new information that aligns with existing knowledge structures. First, we discuss how novel information consistent with an existing schema can be swiftly assimilated when presented. This cognitive updating is facilitated by the interaction between the hippocampus and the prefrontal cortex. Second, when novel information is inconsistent with the schema, it likely engages the hippocampus to encode the information as part of an episodic memory trace. Third, novelty may enhance hippocampal dopamine through either the locus coeruleus or ventral tegmental area pathways, with the pathway involved potentially depending on the type of novelty encountered. We propose a gradient theory of schema and novelty to elucidate the neural processes by which schema updating or novel memory traces are formed. It is likely that experiences vary along a familiarity-novelty continuum, and the degree to which new experiences are increasingly novel will guide whether memory for a new experience either integrates into an existing schema or prompts the creation of a new cognitive framework. This article is part of the theme issue 'Long-term potentiation: 50 years on'.

Developmental and age differences in visuomotor adaptation across the lifespan.

In the present cross-sectional study, we examined age and sex differences in sensorimotor adaptation. We tested 253 individuals at a local science museum (NEMO Science Museum, Amsterdam). Participants spanned a wide age range (8-70 years old; 54% male), allowing us to examine effects of both development and healthy aging within a single study. Participants performed a visuomotor adaptation task in which they had to adapt manual joystick movements to rotated visual feedback. We assessed the rate of adaptation following the introduction of the visual perturbation (both for early and later stages of adaptation), and the rate of de-adaptation following its removal. Results showed reliable adaptation patterns which did not differ by sex. We observed a quadratic relationship between age and both early adaptation and de-adaptation rates, with younger and older adults exhibiting the fasted adaptation rates. Our findings suggest that both younger and older age are associated with poorer strategic, cognitive processes involved in adaptation. We propose that developmental and age differences in cognitive functions and brain properties may underlie these effects on sensorimotor functioning.

The effect of target-related and target-irrelevant novel stimuli on response behaviour.

Novel events catch our attention, which can influence performance of a task. Whether this attentional capture by novelty benefits or impairs performance depends on several factors, such as the relevance of the stimulus, task requirements, and the timing of the event. Additionally, it has been argued that novel stimuli can hold intrinsic reward value, which may directly affect approach motivation, similar to positive valence stimuli. This link between novelty and approach/avoid behaviour has not been investigated directly. Here, we investigated whether stimulus novelty interacts with response behaviour in an approach/avoidance task, and whether these effects depend on the task relevance of novelty and stimulus timing. In experiment 1, participants gave an approach or avoid response dependent on a shape (diamond or square) presented at different stimulus onset asynchronies (SOA) following a novel or familiar scene (target-irrelevant novelty). In experiment 2, participants had to approach or avoid a novel or familiar image depending on the content (indoor/outdoor; target-related novelty). A shape was presented at different SOA. Results of a linear mixed model showed novelty-induced performance costs as demonstrated by longer RT and lower accuracy when novelty was target-relevant, likely due to attentional lingering at novel images. When images were target-irrelevant, approach but not avoid responses were faster for familiar versus novel images at 200 ms SOA only. Thus, novelty had a differentially pronounced detrimental effect on performance. These observations confirm that processing of novel stimuli generally depends on stimulus relevance, and tentatively suggests that differential processing of novel and familiar images is intensified by motivated approach behaviour.

Effects of exploring a novel environment on memory across the lifespan.

Exploration of a novel environment has been shown to promote memory formation in healthy adults. Studies in animals have suggested that such novelty-induced memory boosts are mediated by hippocampal dopamine. The dopaminergic system is known to develop and deteriorate over the lifespan, but so far, the effects of novelty on memory across the lifespan have not yet been investigated. In the current study, we had children, adolescents, younger, and older adults (n = 439) explore novel and previously familiarized virtual environments to pinpoint the effects of spatial novelty on declarative memory in humans across different age groups. After exploration, words were presented while participants performed a deep or shallow encoding task. Incidental memory was quantified in a surprise test. Results showed that participants in the deep encoding condition remembered more words than those in the shallow condition, while novelty did not influence this effect. Interestingly, however, children, adolescents and younger adults benefitted from exploring a novel compared to a familiar environment as evidenced by better word recall, while these effects were absent in older adults. Our findings suggest that the beneficial effects of novelty on memory follow the deterioration of neural pathways involved in novelty-related processes across the lifespan.

A bias toward the unknown: individual and environmental factors influencing exploratory behavior.

With limited resources, exploring new opportunities is crucial for survival. Exploring novel options, however, comes at the cost of uncertainty. Therefore, there is a trade-off between exploiting options with a known beneficial outcome and exploring novel options with a potentially higher gain. Computational models have suggested that novelty may promote exploratory behavior by inducing a so-called novelty bonus through reward-related processes. So far, few studies have provided behavioral evidence for such a novelty bonus. In this study, we aimed to investigate whether spatial novelty can stimulate exploratory behavior (Experiment 1), and whether age, novelty-seeking, and reduced action radius or social interactions due to COVID-19 restrictions influenced the exploration-exploitation trade-off (Experiment 2). In both experiments, we employed a novel paradigm in which participants made binary decisions between food items, while on rare trials, a surprise option was presented. Results from Experiment 1 are in line with a novelty bonus, with spatial novelty promoting exploratory behavior. In Experiment 2, we found that exploratory behavior declined with age, high novelty seekers made more exploratory choices than low novelty seekers, and participants with a smaller action radius made fewer exploratory choices. These findings are consistent with previous findings in animals and predictions from computational models.

Novelty exposure induces stronger sensorimotor representations during a manual adaptation task.

Active exploration of novel spatial environments enhances memory for subsequently presented explicit, declarative information in humans. These effects have been attributed to novelty promoting dopamine release via mesolimbic dopaminergic pathways in the brain. As procedural motor learning has been linked to dopamine as well, we predict that novelty effects extend to this domain. To test this hypothesis, the present study examined whether spatial novelty exploration benefits subsequent sensorimotor adaptation. Participants explored either two different virtual environments (i.e., novelty condition; n = 210) or two identical environments (i.e., familiar condition; n = 253). They then performed a manual adaptation task in which they had to adapt joystick movements to a visual perturbation. We assessed the rate of adaptation following the introduction of this perturbation, and the rate of deadaptation following its removal. While results showed reliable adaptation patterns and similar adaptation rates across both conditions, individuals in the novelty condition showed slower deadaptation. This suggests that exposure to spatial novelty induced stronger sensorimotor representations during adaptation, potentially through novelty-induced dopaminergic effects in mesocortical and/or nigrostriatal pathways. Novelty exposure may be employed to promote motor learning on tasks that require precision movements in altered sensory contexts, for example, in astronauts moving in microgravity or patients with impaired motor processing.

Motivational Objects in Natural Scenes (MONS): A Database of >800 Objects.

In daily life, we are surrounded by objects with pre-existing motivational associations. However, these are rarely controlled for in experiments with natural stimuli. Research on natural stimuli would therefore benefit from stimuli with well-defined motivational properties; in turn, such stimuli also open new paths in research on motivation. Here we introduce a database of Motivational Objects in Natural Scenes (MONS). The database consists of 107 scenes. Each scene contains 2 to 7 objects placed at approximately equal distance from the scene center. Each scene was photographed creating 3 versions, with one object ("critical object") being replaced to vary the overall motivational value of the scene (appetitive, aversive, and neutral), while maintaining high visual similarity between the three versions. Ratings on motivation, valence, arousal and recognizability were obtained using internet-based questionnaires. Since the main objective was to provide stimuli of well-defined motivational value, three motivation scales were used: (1) Desire to own the object; (2) Approach/Avoid; (3) Desire to interact with the object. Three sets of ratings were obtained in independent sets of observers: for all 805 objects presented on a neutral background, for 321 critical objects presented in their scene context, and for the entire scenes. On the basis of the motivational ratings, objects were subdivided into aversive, neutral, and appetitive categories. The MONS database will provide a standardized basis for future studies on motivational value under realistic conditions.

Memory Performance for Everyday Motivational and Neutral Objects Is Dissociable from Attention.

Episodic memory is typically better for items coupled with monetary reward or punishment during encoding. It is yet unclear whether memory is also enhanced for everyday objects with appetitive or aversive values learned through a lifetime of experience, and to what extent episodic memory enhancement for motivational and neutral items is attributable to attention. In a first experiment, we investigated attention to everyday motivational objects using eye-tracking during free-viewing and subsequently tested episodic memory using a remember/know procedure. Attention was directed more to aversive stimuli, as evidenced by longer viewing durations, whereas recollection was higher for both appetitive and aversive objects. In the second experiment, we manipulated the visual contrast of neutral objects through changes of contrast to further dissociate attention and memory encoding. While objects presented with high visual contrast were looked at longer, recollection was best for objects presented in unmodified, medium contrast. Generalized logistic mixed models on recollection performance showed that attention as measured by eye movements did not enhance subsequent memory, while motivational value (Experiment 1) and visual contrast (Experiment 2) had quadratic effects in opposite directions. Our findings suggest that an enhancement of incidental memory encoding for appetitive items can occur without an increase in attention and, vice versa, that enhanced attention towards salient neutral objects is not necessarily associated with memory improvement. Together, our results provide evidence for a double dissociation of attention and memory effects under certain conditions.

Attention in natural scenes: Affective-motivational factors guide gaze independently of visual salience.

In addition to low-level stimulus characteristics and current goals, our previous experience with stimuli can also guide attentional deployment. It remains unclear, however, if such effects act independently or whether they interact in guiding attention. In the current study, we presented natural scenes including every-day objects that differed in affective-motivational impact. In the first free-viewing experiment, we presented visually-matched triads of scenes in which one critical object was replaced that varied mainly in terms of motivational value, but also in terms of valence and arousal, as confirmed by ratings by a large set of observers. Treating motivation as a categorical factor, we found that it affected gaze. A linear-effect model showed that arousal, valence, and motivation predicted fixations above and beyond visual characteristics, like object size, eccentricity, or visual salience. In a second experiment, we experimentally investigated whether the effects of emotion and motivation could be modulated by visual salience. In a medium-salience condition, we presented the same unmodified scenes as in the first experiment. In a high-salience condition, we retained the saturation of the critical object in the scene, and decreased the saturation of the background, and in a low-salience condition, we desaturated the critical object while retaining the original saturation of the background. We found that highly salient objects guided gaze, but still found additional additive effects of arousal, valence and motivation, confirming that higher-level factors can also guide attention, as measured by fixations towards objects in natural scenes.

Happier, faster: Developmental changes in the effects of mood and novelty on responses.

Positive mood ameliorates several cognitive processes: It can enhance cognitive control, increase flexibility, and promote variety seeking in decision making. These effects of positive mood have been suggested to depend on frontostriatal dopamine, which is also associated with the detection of novelty. This suggests that positive mood could also affect novelty detection. In the present study, children and adults saw either a happy or a neutral movie to induce a positive or neutral mood. After that, they were shown novel and familiar images. On some trials a beep was presented over headphones either at the same time as the image or at a 200-ms stimulus onset asynchrony (SOA), and the task of the participant was to detect these auditory targets. Children were slower in responding than adults. Positive mood, however, speeded responses, especially in children, and induced facilitatory effects of novelty. These effects were consistent with increased arousal. Although effects of novelty were more consistent with an attentional response, in children who had watched a happy movie the novel images evoked a more liberal response criterion, suggestive of increased arousal. This suggests that mood and novelty may affect response behaviour stronger in children than in adults.

Exploring a novel environment improves motivation and promotes recall of words.

Active exploration of novel environments is known to increase plasticity in animals, promoting long-term potentiation in the hippocampus and enhancing memory formation. These effects can occur during as well as after exploration. In humans novelty's effects on memory have been investigated with other methods, but never in an active exploration paradigm. We therefore investigated whether active spatial exploration of a novel compared to a previously familiarized virtual environment promotes performance on an unrelated word learning task. Exploration of the novel environment enhanced recall, generally thought to be hippocampus-dependent, but not recognition, believed to rely less on the hippocampus. Recall was better for participants that gave higher presence ratings for their experience in the virtual environment. These ratings were higher for the novel compared to the familiar virtual environment, suggesting that novelty increased attention for the virtual rather than real environment; however, this did not explain the effect of novelty on recall.

Expecting the unexpected: the effects of deviance on novelty processing.

Novelty is often prioritized and detected automatically. It attracts attention-eliciting the orienting response. However, novelty is not a unitary concept, and the extent to which the orienting response is elicited depends on several factors. In the present study we investigated how stimulus novelty, deviance from the context, and complexity of the stimulus context contribute to the anterior N2 and novelty P3 event-related potential components, using the visual novelty oddball paradigm. In the first experiment the novelty P3 was drastically reduced when the stimulus context was complex compared with simple, and in a second experiment when novels were frequent rather than deviant. No such effect was found for the anterior N2, suggesting it is a function of stimulus characteristics, not deviance. In contrast, the novelty P3 depended on deviance and contextual complexity.

Novelty enhances visual perception.

The effects of novelty on low-level visual perception were investigated in two experiments using a two-alternative forced-choice tilt detection task. A target, consisting of a Gabor patch, was preceded by a cue that was either a novel or a familiar fractal image. Participants had to indicate whether the Gabor stimulus was vertically oriented or slightly tilted. In the first experiment tilt angle was manipulated; in the second contrast of the Gabor patch was varied. In the first, we found that sensitivity was enhanced after a novel compared to a familiar cue, and in the second we found sensitivity to be enhanced for novel cues in later experimental blocks when participants became more and more familiarized with the familiar cue. These effects were not caused by a shift in the response criterion. This shows for the first time that novel stimuli affect low-level characteristics of perception. We suggest that novelty can elicit a transient attentional response, thereby enhancing perception.

It is all me: the effect of viewpoint on visual-vestibular recalibration.

Participants performed a visual-vestibular motor recalibration task in virtual reality. The task consisted of keeping the extended arm and hand stable in space during a whole-body rotation induced by a robotic wheelchair. Performance was first quantified in a pre-test in which no visual feedback was available during the rotation. During the subsequent adaptation phase, optical flow resulting from body rotation was provided. This visual feedback was manipulated to create the illusion of a smaller rotational movement than actually occurred, hereby altering the visual-vestibular mapping. The effects of the adaptation phase on hand stabilization performance were measured during a post-test that was identical to the pre-test. Three different groups of subjects were exposed to different perspectives on the visual scene, i.e., first-person, top view, or mirror view. Sensorimotor adaptation occurred for all three viewpoint conditions, performance in the post-test session showing a marked under-compensation relative to the pre-test performance. In other words, all viewpoints gave rise to a remapping between vestibular input and the motor output required to stabilize the arm. Furthermore, the first-person and mirror view adaptation induced a significant decrease in variability of the stabilization performance. Such variability reduction was not observed for the top view adaptation. These results suggest that even if all three viewpoints can evoke substantial adaptation aftereffects, the more naturalistic first-person view and the richer mirror view should be preferred when reducing motor variability constitutes an important issue.