Judith Schomaker

Short- and long-lasting consequences of novelty, deviance and surprise on brain and cognition.

When one encounters a novel stimulus this sets off a cascade of brain responses, activating several neuromodulatory systems. As a consequence novelty has a wide range of effects on cognition; improving perception and action, increasing motivation, eliciting exploratory behavior, and promoting learning. Here, we review these benefits and how they may arise in the brain. We propose a framework that organizes noveltys effects on brain and cognition into three groups. First, novelty can transiently enhance perception. This effect is proposed to be mediated by novel stimuli activating the amygdala and enhancing early sensory processing. Second, novel stimuli can increase arousal, leading to short-lived effects on action in the first hundreds of milliseconds after presentation. We argue that these effects are related to deviance, rather than to novelty per se, and link them to activation of the locus-coeruleus norepinephrine system. Third, spatial novelty may trigger the dopaminergic mesolimbic system, promoting dopamine release in the hippocampus, having longer-lasting effects, up to tens of minutes, on motivation, reward processing, and learning and memory.

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.

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.

Novelty processing and memory formation in Parkinson's disease

BACKGROUND Parkinsons disease (PD) is characterized by a degeneration of nigrostriatal dopaminergic cells, resulting in dopamine depletion. This depletion is counteracted through dopamine replacement therapy (DRT). Dopamine has been suggested to affect novelty processing and memory, which suggests that these processes are also implicated in PD and that DRT could affect them. OBJECTIVE To investigate word learning and novelty processing in patients with PD as indexed by the P2 and P3 event-related potential components, and the role of DRT in these processes. METHODS 21 patients with PD and 21 matched healthy controls were included. Patients with PD were tested on and off DRT in two sessions in a counterbalanced design, and healthy controls were tested twice without intervention. Electroencephalogram (EEG) was measured while participants performed a word learning Von Restorff task. RESULTS Healthy controls showed the typical Von Restorff effect, with better memory for words that were presented in novel fonts, than for words presented in standard font. Surprisingly, this effect was reversed in the patients with PD. In line with the behavioral findings, the P3 was larger for novel than for standard font words in healthy controls, but not in patients with PD. For both groups the P2 and P3 event-related components were larger for recalled versus forgotten words. DRT did not affect these processes. CONCLUSIONS Learning of novel information is compromised in patients with PD. Likewise, the P2 and P3 components that predict successful memory encoding are reduced in PD patients. This was true both on and off DRT, suggesting that these findings reflect abnormalities in learning and memory in PD that are not resolved by dopaminergic medication.

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.

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.

Facilitation of responses by task-irrelevant complex deviant stimuli

Novel stimuli reliably attract attention, suggesting that novelty may disrupt performance when it is task-irrelevant. However, under certain circumstances novel stimuli can also elicit a general alerting response having beneficial effects on performance. In a series of experiments we investigated whether different aspects of novelty--stimulus novelty, contextual novelty, surprise, deviance, and relative complexity--lead to distraction or facilitation. We used a version of the visual oddball paradigm in which participants responded to an occasional auditory target. Participants responded faster to this auditory target when it occurred during the presentation of novel visual stimuli than of standard stimuli, especially at SOAs of 0 and 200 ms (Experiment 1). Facilitation was absent for both infrequent simple deviants and frequent complex images (Experiment 2). However, repeated complex deviant images did facilitate responses to the auditory target at the 200 ms SOA (Experiment 3). These findings suggest that task-irrelevant deviant visual stimuli can facilitate responses to an unrelated auditory target in a short 0-200 millisecond time-window after presentation. This only occurs when the deviant stimuli are complex relative to standard stimuli. We link our findings to the novelty P3, which is generated under the same circumstances, and to the adaptive gain theory of the locus coeruleus-norepinephrine system (Aston-Jones and Cohen, 2005), which may explain the timing of the effects.

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

ABSTRACT 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.

Predicting the unknown : Novelty processing depends on expectations

Fulfilled predictions lead to neural suppression akin to repetition suppression, but it is currently unclear if such effects generalize to broader stimulus categories in the absence of exact expectations. In particular, does expecting novelty alter the way novel stimuli are processed? In the present study, the effects of expectations on novelty processing were investigated using event-related potentials, while controlling for the effect of repetition. Sequences of five stimuli were presented in a continuous way, such that the last stimulus of a 5-stimulus sequence was followed by the first stimulus of a new 5-stimulus sequence without interruption. The 5-stimulus sequence was predictable: the first three stimuli were preceded by a cue indicating that the next stimulus was likely to be a standard stimulus, and the last two by a cue indicating that the next stimulus was likely to be novel. On some trials a cue typically predicting a standard was in fact followed by an unexpected novel stimulus. This design allowed to investigate the independent effects of (violated) expectations and repetition on novelty processing. The initial detection of expected novels was enhanced compared to unexpected novels, as indexed by a larger anterior N2. In contrast, the orienting response, as reflected by a novelty P3, was reduced for expected compared to unexpected novels. Although the novel stimuli were never repeated themselves, they could be presented after one another in the sequence. Such a category repetition affected the processing of novelty, as evidenced by an enhanced anterior N2, and a reduced novelty P3 for novels preceded by other novels. Taken together, the current study shows that novelty processing is influenced by expectations.