The effect of feedback novelty on neural correlates of feedback processing.

It has been suggested that stimulus novelty itself can be rewarding and recent evidence suggests that novelty processing and reward processing share common neural mechanisms. For feedback processing, this can be beneficial as well as detrimental: If novelty lends a rewarding characteristic to a stimulus, then this should particularly decrease the impact of negative feedback. The present study investigated whether such an effect of feedback novelty on feedback processing is reflected in electrophysiological markers of reinforcement learning (feedback-related negativity, FRN) and feedback processing (feedback-P300) in a simple decision-making task. In this task, participants had to chose between two stimuli in a learning trial followed by a novel or a familiar feedback stimulus. Learning from feedback allowed them to optimize their payoff in a later test trial. As expected, we found that the FRN effect, i.e. the difference between the FRN amplitudes after negative and positive feedback, was reduced for novel compared to familiar feedback stimuli. In addition, the amplitude of the feedback-P300 was decreased by feedback novelty, both for the anterior P3a and the posterior P3b. Together, these results indicate that feedback novelty can affect feedback processing as reflected by feedback-related brain activity.

Auditory Task Irrelevance: A Basis for Inattentional Deafness.

Objective This study investigates the neural basis of inattentional deafness, which could result from task irrelevance in the auditory modality. Background Humans can fail to respond to auditory alarms under high workload situations. This failure, termed inattentional deafness, is often attributed to high workload in the visual modality, which reduces one's capacity for information processing. Besides this, our capacity for processing auditory information could also be selectively diminished if there is no obvious task relevance in the auditory channel. This could be another contributing factor given the rarity of auditory warnings. Method Forty-eight participants performed a visuomotor tracking task while auditory stimuli were presented: a frequent pure tone, an infrequent pure tone, and infrequent environmental sounds. Participants were required either to respond to the presentation of the infrequent pure tone (auditory task-relevant) or not (auditory task-irrelevant). We recorded and compared the event-related potentials (ERPs) that were generated by environmental sounds, which were always task-irrelevant for both groups. These ERPs served as an index for our participants' awareness of the task-irrelevant auditory scene. Results Manipulation of auditory task relevance influenced the brain's response to task-irrelevant environmental sounds. Specifically, the late novelty-P3 to irrelevant environmental sounds, which underlies working memory updating, was found to be selectively enhanced by auditory task relevance independent of visuomotor workload. Conclusion Task irrelevance in the auditory modality selectively reduces our brain's responses to unexpected and irrelevant sounds regardless of visuomotor workload. Application Presenting relevant auditory information more often could mitigate the risk of inattentional deafness.

Components in the P300: Don't forget the Novelty P3!

This study investigated stimulus-response patterns of temporal principal components analysis (PCA)-derived event-related potential (ERP) components in a classical auditory habituation paradigm with long interstimulus intervals. The skin conductance response (SCR) was included as the "gold standard" model of the Orienting Reflex. Thirty participants were presented with a single series of 10 identical 60 dB tones, followed by a change trial at a different frequency. Single-trial, electrooculography-corrected ERPs were submitted to temporal PCA. The main focus was on the components expected in the P300/Late Positive Complex (LPC), and their electromagnetic tomography-derived cortical sources. Nine components were identified between 90 and 470 ms poststimulus (in temporal order): three N1 subcomponents, P2, four LPC components, and a negative Slow Wave (SW). The expected order of P3a, P3b, Novelty P3 (nP3), and positive Slow Wave (+SW) in the LPC was confirmed. SCR demonstrated strong exponential decay and recovery. P3b and nP3 each showed exponential decrement over trials, but only nP3 showed recovery at the change trial. Novelty effects failed to reach significance for the other LPC components, and were not apparent in non-LPC components. Frontal lobe activity in Brodmann areas 6, 8, and 9 was common to P3a, P3b, nP3, and +SW, consistent with the functional integration of these components in the LPC. Individual components had specific sources, although some sources overlapped between components or were reactivated later in the LPC. These data provide a fresh perspective on the components of the LPC and their cortical sources, and offer a processing model for the P300 in a habituation task, potentially generalizable to other paradigms.

Effects of sensation seeking on habituation to novelty: An EEG study.

Sensation seeking is characterized by a strong need for novelty and has been associated with various risk-taking behaviors. Using the extreme between-group design, the current study investigated the electrophysiological mechanisms underlying habituation to novelty processing in sensation seeking. Twenty high sensation seekers (HSS) and 20 low sensation seekers (LSS) performed an auditory oddball task while their EEG was recorded. The results revealed that both the novelty P3 and midfrontal theta power decreased from the first to the second half for LSS but not for HSS. Additionally, this reduced vigilance was predicted by the experience-seeking subcomponent of sensation seeking. Together, our findings are supportive of an abnormal habituation to novel events in the sensation-seeking trait.

Event-related neuronal responses to acoustic novelty in single-sided deaf cochlear implant users: Initial findings.

OBJECTIVE: A cochlear implant (CI) is an auditory prosthesis restoring profound hearing loss. However, CI-transmitted sounds are degraded compared to normal acoustic hearing. We investigated cortical responses related to CI-degraded against acoustic listening. METHODS: Event-related potentials (ERPs) were recorded from eight single-sided deaf CI users who performed a three-stimulus oddball task, separately with their normal hearing ear and CI ear. The oddball tones were occasionally intermitted by novel sounds. ERP responses were compared between electric and acoustic listening for the auditory (N1) and auditory-cognitive (Novelty P3, Target-P3) ERP components. RESULTS: CI-degraded listening was associated with attenuated sensory processing (N1) and with attenuated early cortical responses to acoustic novelty whereas the late cortical responses to acoustic novelty and the target-P3 did not differ between NH and CI ears. CONCLUSION: The present study replicates the CI-attenuation of Novelty-P3 amplitudes in a within-subject comparison. Further, we show that the CI-attenuation of Novelty-P3 amplitudes extends to early cortical responses to acoustic novelty, but not to late novelty responses. SIGNIFICANCE: The dissociation into CI-attenuated P3 early Novelty-P3 amplitudes and CI-unaffected late Novelty-P3 amplitudes represents a cortical fingerprint of CI-degraded listening. It further contributes to general claims of distinct auditory Novelty-P3 sub-components.

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.

Effects of Gender and Apolipoprotein E on Novelty MMN and P3a in Healthy Elderly and Amnestic Mild Cognitive Impairment.

Background: The apolipoprotein E epsilon4 (ApoE ε4) allele and female gender may be important risk factors for the development of Alzheimer's disease and amnestic mild cognitive impairment (aMCI). Novelty mismatch negativity (MMN) represents the pre-attentive index of deviance detection and P3a represents the attention orienting response. Furthermore, MMN and P3a components have been reported to be potential markers in aMCI. Therefore, this study will investigate the effects of gender and ApoE on auditory novelty MMN and P3a and their relationship to neuropsychological performance in aMCI. Methods: Thirty nine aMCI subjects and 44 controls underwent neuropsychological assessment and ApoE genotyping. Novelty MMN and P3a components were investigated during an auditory novelty oddball task. Results: Firstly, novelty MMN latency was significantly shorter in aMCI than in healthy control (HC) group. Secondly, novelty MMN latency was negatively correlated with episodic memory in aMCI, but not in HC. Novelty P3a latency was negatively correlated with information processing speed in all subjects. For gender effect, novelty MMN latency was shorter in aMCI females than in HC females. Moreover, novelty P3a amplitudes were lower in males than in females in both aMCI and HC. For the effect of ApoE status, novelty MMN latency was shorter in aMCI ApoE ε4- than HC ApoE ε4-. Conclusion: aMCI presents altered pre-attentive processing indexed by novelty MMN components. Furthermore, there may be a compensatory mechanism on the impaired processing in aMCI. It further suggests that aMCI female and ApoE ε4- recruited the compensatory mechanism.

Task-Irrelevant Novel Sounds have Antithetical Effects on Visual Target Processing in Young and Old Adults.

In young adults, primary visual task processing can be either enhanced or disrupted by novel auditory stimuli preceding target events, depending on task demands. Little is known about this phenomenon in older individuals, who, in general, are more susceptible to distraction. In the current study, age-related differences in the electrophysiological effects of task-irrelevant auditory stimuli on visual target processing were examined. Under both low and high primary task loads, the categorization/updating process in response to visual targets preceded by auditory novels, as indexed by the target P3 component, was enhanced in young, but diminished in old adults. In both age groups, the alerting/orienting response to novel auditory stimuli, as measured by the P3a, was smaller under high task load, whereas redirecting attention to the visual task after a novel auditory event, as indexed by the reorienting negativity (RON), tended to be augmented under high task load. Old subjects generated a smaller P3a and RON. We conclude that task irrelevant novel auditory stimuli have the opposite effect on the processing of visual targets in young and old adults. This finding may help explain age-related increases in the disruption of primary task activity by irrelevant, but salient auditory events.

Hormonal modulation of novelty processing in women: Enhanced under working memory load with high dehydroepiandrosterone-sulfate-to-dehydroepiandrosterone ratios.

Several studies have suggested that dehydroepiandrosterone (DHEA) and dehydroepiandrosterone-sulfate (DHEAS) may enhance working memory and attention, yet current evidence is still inconclusive. The balance between both forms of the hormone might be crucial regarding the effects that DHEA and DHEAS exert on the central nervous system. To test the hypothesis that higher DHEAS-to-DHEA ratios might enhance working memory and/or involuntary attention, we studied the DHEAS-to-DHEA ratio in relation to involuntary attention and working memory processing by recording the electroencephalogram of 22 young women while performing a working memory load task and a task without working memory load in an audio-visual oddball paradigm. DHEA and DHEAS were measured in saliva before each task. We found that a higher DHEAS-to-DHEA ratio was related to enhanced auditory novelty-P3 amplitudes during performance of the working memory task, indicating an increased processing of the distracter, while on the other hand there was no difference in the processing of the visual target. These results suggest that the balance between DHEAS and DHEA levels modulates involuntary attention during the performance of a task with cognitive load without interfering with the processing of the task-relevant visual stimulus.

Neural correlates of attention bias in posttraumatic stress disorder.

OBJECTIVE: Patients suffering from posttraumatic stress disorder (PTSD) exhibit hyper arousal symptoms and attention problems which were frequently investigated using the P3 event-related potentials (ERPs). Our study aimed at providing more precise knowledge of the functional significance of the P3 alteration seen in PTSD by revealing its spatio-temporal dynamics. METHODS: Fifteen PTSD patients and fifteen healthy trauma-exposed controls participated in a three-tone "oddball" task while their brain activity was recorded by magnetoencephalography (MEG). They were asked to detect rare target tones and ignore standard tones and infrequent threatening distractors. An adaptive spatial-filter method (SAM beamformer) was applied for source estimation. RESULTS: Compared with controls, PTSD patients had more incorrect responses to standard stimuli. On the brain level, PTSD patients showed hyperactivity in the dorsolateral prefrontal cortex and anterior cingulate cortex in response to standard sounds, decreased activity in those regions in response to threatening distractors, and decreased orbitofrontal activity in response to target stimuli. CONCLUSIONS: Increased frontal activation in response to standard, neutral, stimuli may reflect greater resource allocation dedicated to cognitive control mechanisms during routine functioning in PTSD. Decreased frontal activation in response to rare stimuli may reflect subsequently reduced residual resources for detecting rare stimuli and for emotion regulation. This may explain the hypervigilance and attention problems commonly reported by patients. SIGNIFICANCE: The current findings contribute to a better understanding of the mechanisms underlying the attention deficiency in PTSD, and highlight altered activity in specific frontal regions as potential biomarkers.

Effects of age and task difficulty on ERP responses to novel sounds presented during a speech-perception-in-noise test.

OBJECTIVE: Event-related potentials (ERPs) to task-irrelevant novel sounds have been shown to increase in amplitude with increasing task difficulty and might therefore reflect listening effort. Here we investigated whether this effect is similar in two groups of younger and older listeners with normal hearing. METHODS: Novel sounds were presented during a speech-perception-in noise test and task difficulty was adjusted decreasing the signal-to-noise ratio (SNR) relative to the individual 50% correct speech recognition SNR (easy +10 dB, medium +2dB, hard 0 dB). RESULTS: Amplitudes of the Novelty P3 and a late positive potential (LPP) were significantly larger in younger compared to older participants. Novelty P3 amplitude increased with increasing task difficulty in both age groups, but the effect was more robust in younger listeners. By contrast, LPP amplitude increases were observed only in older listeners. CONCLUSIONS: Novelty P3 and LPP were found to be differently affected by task difficulty in the two age groups indicating sustained and more effortful processing under challenging listening conditions in older listeners. SIGNIFICANCE: These results confirmed the potential use of novel sounds during an auditory task as an indirect measure of listening effort in younger and older listeners, but the different focus on Novelty P3 and LPP should be taken into account.

Dual routes to cortical orienting responses: novelty detection and uncertainty reduction.

Sokolov distinguished between reactive and proactive variants of the orienting response (OR). The Novelty P3 is considered as an electrophysiological signature of the reactive OR. Recent work suggests that the proactive OR is reflected in frontally distributed P3 activity elicited by uncertainty-reducing stimuli in task-switching paradigms. Here, we directly compare the electrophysiological signatures of reactive and proactive ORs. Participants completed a novelty oddball task and a task-switching procedure while the electroencephalogram was measured. Novel and uncertainty-reducing stimuli evoked prominent fronto-centrally distributed Novelty P3 and Uncertainty P3 waves, respectively. We found a substantial negative correlation between Novelty P3 and Uncertainty P3 across participants, suggesting that reactive and proactive ORs converge on a common neural pathway, but also that distinguishable routes to orienting exist. Moreover, response accuracy was associated with reduced Novelty-P3 and enhanced Uncertainty-P3 amplitudes. The relation between Novelty P3 and Uncertainty P3 might serve as an index of individual differences in distractibility and cognitive control.

Psychophysiological support of increasing attentional reserve during the development of a motor skill.

The aim of this study was to determine the relationship between motor skill and attentional reserve. Participants practiced a reaching task with the dominant upper extremity, to which a distortion of the visual feedback was applied, while a control group performed the same task without distortion. Event-related brain potentials (ERPs), elicited by auditory stimuli were recorded throughout practice. Performance, as measured by initial directional error, was initially worse relative to controls and improved over trials. Analyses of the ERPs revealed that exogenous components, N1 and P2, were undifferentiated between the groups and did not change with practice. Notably, amplitude of the novelty P3 component, an index of the involuntary orienting of attention, was initially attenuated relative to controls, but progressively increased in amplitude over trials in the learning group only. The results provide psychophysiological evidence that attentional reserve increases as a function of motor skill acquisition.

EEG delta oscillations index inhibitory control of contextual novelty to both irrelevant distracters and relevant task-switch cues.

Delta oscillations contribute to the human P300 event-related potential evoked by oddball targets, although it is unclear whether they index contextual novelty (event oddballness, novelty P3, nP3), or target-related processes (event targetness, target P3b). To examine this question, the electroencephalogram (EEG) was recorded during a cued task-switching version of the Wisconsin card-sorting test. Each target card was announced by a tone cueing either to switch or repeat the task. Novel sound distracters were interspersed among trials. Time-frequency EEG analyses revealed bursts of delta (2-4 Hz) power associated with enhanced nP3 amplitudes to both task-switch cues and novel distracters-but no association with target P3b. These findings indicate that the P300-delta response indexes contextual novelty regardless of whether novelty emanates from endogenous (new task rules) or exogenous (novel distracters) sources of information.

Novel sounds as a psychophysiological measure of listening effort in older listeners with and without hearing loss.

OBJECTIVE: To investigate whether task-irrelevant novel sounds presented during an auditory task can provide information about the level of listening effort. METHODS: Event-related potentials (ERPs) were recorded for novel sounds presented during two Experiments, a frequency discrimination task and a speech-perception-in-noise (SPIN) test, each with varying degrees of task difficulty (easy, medium, hard). Difficulty was adjusted to the individual frequency discrimination threshold and 50% speech recognition signal-to-noise ratio (SNR), respectively. Older listeners (age range 60-86 years) with either normal hearing for their age or a mild-to-moderate hearing loss participated. RESULTS: Amplitudes of Novelty P3 and late positive potential (LPP) increased with increasing task difficulty, whereas amplitudes of N1 and N2 decreased. Participants with hearing loss had significantly larger LPP amplitudes in the easy condition of the SPIN test than did normal-hearing listeners. Most correlations between ERP amplitudes and behavioral data were not significant suggesting that listening effort is not a simple equivalent of behavioral performance. CONCLUSIONS: LPP amplitude appeared to be the most sensitive component for capturing listening effort reflecting the arousal level of the listener. SIGNIFICANCE: ERPs to novel sounds could be easily recorded during hearing tests and provide an objective physiological measure of listening effort, thus supplementing behavioral performance data.

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.

The dissociation between the P3a event-related potential and behavioral distraction.

Unexpected novel sounds can capture our attention and impair performance. Recent behavioral research revealed that only novel sounds that provided target-related (but not task-related) information impaired performance. This poses the question of the automaticity of novelty processing and its expression at the behavioral level. In an auditory-visual oddball paradigm, the informational content of sounds regarding the time and probability of target occurrence was varied. Independent from the informational content, novel, and deviant sounds elicited the P3a, an ERP-component related to novelty processing. In contrast, impaired performance was only observed if target-related information was provided. Results indicate that distractor sounds are automatically evaluated as potentially significant, but that the consequences for behavior depend on further processes such as the processing of the given information.