Jarosław M. Michałowski

Brain dynamics of visual attention during anticipation and encoding of threat- and safe-cues in spider-phobic individuals

This study systematically investigated the sensitivity of the phobic attention system by measuring event-related potentials (ERPs) in spider-phobic and non-phobic volunteers in a context where spider and neutral pictures were presented (phobic threat condition) and in contexts where no phobic but unpleasant and neutral or only neutral pictures were displayed (phobia-irrelevant conditions). In a between-group study, participants were assigned to phobia-irrelevant conditions either before or after the exposure to spider pictures (pre-exposure vs post-exposure participants). Additionally, each picture was preceded by a fixation cross presented in one of three different colors that were informative about the category of an upcoming picture. In the phobic threat condition, spider-phobic participants showed a larger P1 than controls for all pictures and signal cues. Moreover, individuals with spider phobia who were sensitized by the exposure to phobic stimuli (i.e. post-exposure participants) responded with an increased P1 also in phobia-irrelevant conditions. In contrast, no group differences between spider-phobic and non-phobic individuals were observed in the P1-amplitudes during viewing of phobia-irrelevant stimuli in the pre-exposure group. In addition, cues signaling neutral pictures elicited decreased stimulus-preceding negativity (SPN) compared with cues signaling emotional pictures. Moreover, emotional pictures and cues signaling emotional pictures evoked larger early posterior negativity (EPN) and late positive potential (LPP) than neutral stimuli. Spider phobics showed greater selective attention effects than controls for phobia-relevant pictures (increased EPN and LPP) and cues (increased LPP and SPN). Increased sensitization of the attention system observed in spider-phobic individuals might facilitate fear conditioning and promote generalization of fear playing an important role in the maintenance of anxiety disorders.

Characterization of the Nencki Affective Picture System by discrete emotional categories (NAPS BE)

The Nencki Affective Picture System (NAPS; Marchewka, Żurawski, Jednoróg, & Grabowska, Behavior Research Methods, 2014) is a standardized set of 1,356 realistic, high-quality photographs divided into five categories (people, faces, animals, objects, and landscapes). NAPS has been primarily standardized along the affective dimensions of valence, arousal, and approach–avoidance, yet the characteristics of discrete emotions expressed by the images have not been investigated thus far. The aim of the present study was to collect normative ratings according to categorical models of emotions. A subset of 510 images from the original NAPS set was selected in order to proportionally cover the whole dimensional affective space. Among these, using three available classification methods, we identified images eliciting distinguishable discrete emotions. We introduce the basic-emotion normative ratings for the Nencki Affective Picture System (NAPS BE), which will allow researchers to control and manipulate stimulus properties specifically for their experimental questions of interest. The NAPS BE system is freely accessible to the scientific community for noncommercial use as supplementary materials to this article.

Modulation of the ERP repetition effects during exposure to phobia-relevant and other affective pictures in spider phobia

In the present study, dense sensor event-related potentials were measured in spider-phobic individuals and non-anxious controls during incidental encoding of phobia-relevant spider and standard neutral, unpleasant and pleasant pictures. Stimulus repetition effects were assessed by presenting each picture twice--in the first and in the second half of the session. Repeated presentation of standard pleasant, unpleasant and neutral pictures resulted in a late ERP repetition effect that was similarly pronounced in both experimental groups and for all picture categories. Moreover, relative to non-fearful controls spider-phobic individuals showed an overall greater early ERP repetition effect starting at 180 ms after picture onset. At later stages of evaluative processing, repeated as compared with initial presentation of phobia-relevant spider pictures elicited reduced ERP amplitudes over centro-parietal sites (480-580 ms) in spider-phobic but not in control individuals. This pattern of results indicates that in small animal phobics long lasting exposure to their feared pictures leads to an increased mobilization of the perceptual analysis system, an effect that might help to improve emotional control and/or facilitate strategic avoidance of threat resulting in a diminished evaluative threat processing. This phobia-specific processing mechanism might prevent effective stimulus processing and hinder the habituation process during treatment.

What is the effect of basic emotions on directed forgetting? Investigating the role of basic emotions in memory

Studies presenting memory-facilitating effect of emotions typically focused on affective dimensions of arousal and valence. Little is known, however, about the extent to which stimulus-driven basic emotions could have distinct effects on memory. In the present paper we sought to examine the modulatory effect of disgust, fear, and sadness on intentional remembering and forgetting using widely used item-method directed forgetting (DF) paradigm. Eighteen women underwent fMRI scanning during encoding phase in which they were asked either to remember (R) or to forget (F) pictures. In the test phase all previously used stimuli were re-presented together with the same number of new pictures and participants had to categorize them as old or new, irrespective of the F/R instruction. On the behavioral level we found a typical DF effect, i.e., higher recognition rates for to-be-remembered (TBR) items than to-be-forgotten (TBF) ones for both neutral and emotional categories. Emotional stimuli had higher recognition rate than neutral ones, while among emotional those eliciting disgust produced highest recognition, but at the same time induced more false alarms. Therefore, when false alarm corrected recognition was examined the DF effect was equally strong irrespective of emotion. Additionally, even though subjects rated disgusting pictures as more arousing and negative than other picture categories, logistic regression on the item level showed that the effect of disgust on recognition memory was stronger than the effect of arousal or valence. On the neural level, ROI analyses (with valence and arousal covariates) revealed that correctly recognized disgusting stimuli evoked the highest activity in the left amygdala compared to all other categories. This structure was also more activated for remembered vs. forgotten stimuli, but only in case of disgust or fear eliciting pictures. Our findings, despite several limitations, suggest that disgust have a special salience in memory relative to other negative emotions, which cannot be put down to differences in arousal or valence. The current results thereby support the suggestion that a purely dimensional model of emotional influences on cognition might not be adequate to account for observed effects.

Arousal Rather than Basic Emotions Influence Long-Term Recognition Memory in Humans

Emotion can influence various cognitive processes, however its impact on memory has been traditionally studied over relatively short retention periods and in line with dimensional models of affect. The present study aimed to investigate emotional effects on long-term recognition memory according to a combined framework of affective dimensions and basic emotions. Images selected from the Nencki Affective Picture System were rated on the scale of affective dimensions and basic emotions. After 6 months, subjects took part in a surprise recognition test during an fMRI session. The more negative the pictures the better they were remembered, but also the more false recognitions they provoked. Similar effects were found for the arousal dimension. Recognition success was greater for pictures with lower intensity of happiness and with higher intensity of surprise, sadness, fear, and disgust. Consecutive fMRI analyses showed a significant activation for remembered (recognized) vs. forgotten (not recognized) images in anterior cingulate and bilateral anterior insula as well as in bilateral caudate nuclei and right thalamus. Further, arousal was found to be the only subjective rating significantly modulating brain activation. Higher subjective arousal evoked higher activation associated with memory recognition in the right caudate and the left cingulate gyrus. Notably, no significant modulation was observed for other subjective ratings, including basic emotion intensities. These results emphasize the crucial role of arousal for long-term recognition memory and support the hypothesis that the memorized material, over time, becomes stored in a distributed cortical network including the core salience network and basal ganglia.

Remembering the object you fear: brain potentials during recognition of spiders in spider-fearful individuals.

In the present study we investigated long-term memory for unpleasant, neutral and spider pictures in 15 spider-fearful and 15 non-fearful control individuals using behavioral and electrophysiological measures. During the initial (incidental) encoding, pictures were passively viewed in three separate blocks and were subsequently rated for valence and arousal. A recognition memory task was performed one week later in which old and new unpleasant, neutral and spider pictures were presented. Replicating previous results, we found enhanced memory performance and higher confidence ratings for unpleasant when compared to neutral materials in both animal fearful individuals and controls. When compared to controls high animal fearful individuals also showed a tendency towards better memory accuracy and significantly higher confidence during recognition of spider pictures, suggesting that memory of objects prompting specific fear is also facilitated in fearful individuals. In line, spider-fearful but not control participants responded with larger ERP positivity for correctly recognized old when compared to correctly rejected new spider pictures, thus showing the same effects in the neural signature of emotional memory for feared objects that were already discovered for other emotional materials. The increased fear memory for phobic materials observed in the present study in spider-fearful individuals might result in an enhanced fear response and reinforce negative beliefs aggravating anxiety symptomatology and hindering recovery.

Slowing with end-stage renal disease: Attentive but unprepared to act.

Dialyzed patients show longer response latencies to stimuli than healthy controls. This study was designed to learn if this abnormal latency may be related to an impairment in the networks that mediate the allocation of sensory-attention (inducing a delay in stimulus recognition-awareness) and/or an impairment of intentional motor preparation (inducing a delay in action-initiation). Dialyzed patients with end-stage renal disease and matched healthy controls were assessed using reaction time tasks from the ROtman-Baycrest Battery to Investigate Attention (ROBBIA) and event-related potentials (ERPs) to help elucidate the possible attentional and/or intentional brain mechanisms that may account for this slowing. The following ERP components were analyzed for single attentional and intentional processes: response preparation (Contingent Negative Variation); perceptual preparation (P1); selective attention and monitoring (P300/Late Positive Potential). Patients (vs. controls) had a decreased ability to sustain response preparation under the condition of a long (3 s) but not a short (1 s) preparation period. This action-intentional deficit was, however, not accompanied by impaired perceptual preparation and monitoring. Future research may investigate whether deficits observed in dialyzed patients can be reduced with treatments such as kidney transplantation.

Neural response patterns in spider, blood-injection-injury and social fearful individuals: new insights from a simultaneous EEG/ECG-fMRI study.

In the present simultaneous EEG/ECG-fMRI study we compared the temporal and spatial characteristics of the brain responses and the cardiac activity during fear picture processing between spider, blood-injection-injury (BII) and social fearful as well as healthy (non-fearful) volunteers. All participants were presented with two neutral and six fear-related blocks of pictures: two social, two spider and two blood/injection fear blocks. In a social fear block neutral images were occasionally interspersed with photographs of angry faces and social exposure scenes. In spider and blood/injection fear blocks neutral pictures were interspersed with spider fear-relevant and blood/injection pictures, respectively. When compared to healthy controls the social fear group responded with increased activations in the anterior orbital, middle/anterior cingulate and middle/superior temporal areas for pictures depicting angry faces and with a few elevated superior frontal activations for social exposure scenes. In the blood/injection fear group, heart rate was decreased and the activity in the middle/inferior frontal and visual processing regions was increased for blood/injection pictures. The HR decrease for blood/injection pictures correlated with increased frontal responses. In the spider fear group, spider fear-relevant pictures triggered increased activations within a broad subcortical and cortical neural fear network. The HR response for spider fear-relevant stimuli was increased and correlated with an increased insula and hippocampus activity. When compared to healthy controls, all fear groups showed higher LPP amplitudes for their feared cues and an overall greater P1 hypervigilance effect. Contrasts against the fear control groups showed that the increased responses for fear-specific stimuli are mostly related to specific fears and not to general anxiety proneness. The results suggest different engagement of cognitive evaluation and down-regulation strategies and an overall increased sensitization of the fear system in the three fear groups.

Erratum to: Characterization of the Nencki Affective Picture System by discrete emotional categories (NAPS BE)

Erratum to: Behav Res 10.3758/s13428-015-0620-1 The corresponding authors would like to point out that they have separate e-mail addresses: m.riegel@nencki.gov.pl (M. Riegel) and a.marchewka@nencki.gov.pl (A. Marchewka). Additionally, the corresponding authors would like to indicate that the NAPS BE system is freely accessible to the scientific community for noncommercial use by request at http://naps.nencki.gov.pl. The mean ratings of basic emotions for each picture and the results of basic emotion classification are also provided as supplementary materials (Table S2) to this erratum.

Nencki Affective Picture System: Cross-Cultural Study in Europe and Iran

Although emotions have been assumed conventionally to be universal, recent studies have suggested that various aspects of emotions may be mediated by cultural background. The purpose of our research was to test these contradictory views, in the case of the subjective evaluation of visual affective stimuli. We also sought to validate the recently introduced Nencki Affective Picture System (NAPS) database on a different cultural group. Since there has been, to date, no attempt to compare the emotions of a culturally distinct sample of Iranians with those of Europeans, subjective ratings were collected from 40 Iranians and 39 Europeans. Each cultural group was asked separately to provide normative affective ratings and classify pictures according to discrete emotions. The results were analyzed to identify cultural differences in the ratings of individual images. One hundred and seventy NAPS pictures were rated with regard to the intensity of the basic emotions (happiness, sadness, fear, surprise, anger, and disgust) they elicited, as well as in terms of affective dimensions (valence and arousal). Contrary to previous studies using the International Affective Picture System, our results for Europeans and Iranians show that neither the ratings for affective dimensions nor for basic emotions differed across cultural groups. In both cultural groups, the relationship between valence and arousal ratings could be best described by a classical boomerang-shaped function. However, the content of the pictures (animals, faces, landscapes, objects, or people) had a significant effect on the ratings for valence and arousal. These findings indicate that further studies in cross-cultural affective research should control for the content of stimuli.