Manuel Tapia

Automatic attention to emotional stimuli: Neural correlates

We investigated the capability of emotional and nonemotional visual stimulation to capture automatic attention, an aspect of the interaction between cognitive and emotional processes that has received scant attention from researchers. Event‐related potentials were recorded from 37 subjects using a 60‐electrode array, and were submitted to temporal and spatial principal component analyses to detect and quantify the main components, and to source localization software (LORETA) to determine their spatial origin. Stimuli capturing automatic attention were of three types: emotionally positive, emotionally negative, and nonemotional pictures. Results suggest that initially (P1: 105 msec after stimulus), automatic attention is captured by negative pictures, and not by positive or nonemotional ones. Later (P2: 180 msec), automatic attention remains captured by negative pictures, but also by positive ones. Finally (N2: 240 msec), attention is captured only by positive and nonemotional stimuli. Anatomically, this sequence is characterized by decreasing activation of the visual association cortex (VAC) and by the growing involvement, from dorsal to ventral areas, of the anterior cingulate cortex (ACC). Analyses suggest that the ACC and not the VAC is responsible for experimental effects described above. Intensity, latency, and location of neural activity related to automatic attention thus depend clearly on the stimulus emotional content and on its associated biological importance. Hum. Brain Mapp. 22:290–299, 2004.

Cortical response to subjectively unconscious danger

Cortical involvement in the evolution-favored automatic reaction to danger was studied. Electrical neural activity was recorded from 31 subjects, reporting fear of spiders, at 60 scalp locations. Visual stimuli containing spiders (negative elements) or, alternatively, nonnegative elements were presented to subjects, though they were unaware of their presence: a concurrent visual detection task using consciously perceived targets was administered. Spatial and temporal principal component analyses were employed to define and quantify, in a reliable manner, the main components of the neuroelectrical response to unconscious stimuli, and a source localization algorithm provided information on their neural origin. Results indicated that around 150 ms after stimulus onset, ventromedial prefrontal areas previously reported as responding rapidly to danger-related (conscious) stimuli were activated by unconsciously perceived spiders more markedly than by nonnegative unconscious stimuli. Subsequently, around 500 ms after stimulus onset, activation of the posterior cingulate and visual association cortices increased in this same direction. These data support previous results indicating that the ventromedial prefrontal cortex is involved in the top-down regulation of attention (through its capability to modulate the activity of posterior cortices in charge of visual processing) and that it automatically facilitates danger processing.

An electrophysiological study on the interaction between emotional content and spatial frequency of visual stimuli

Previous studies suggest that the magnocellular pathway, a visual processing system that rapidly provides low spatial frequency information to fast-responding structures such as the amygdala, is more involved in the processing of emotional facial expressions than the parvocellular pathway (which conveys all spatial frequencies). The present experiment explored the spatio-temporal characteristics of the spatial frequency modulation of affect-related neural processing, as well as its generalizability to non-facial stimuli. To that aim, the event-related potentials (ERPs) elicited by low-pass filtered (i.e., high spatial frequencies are eliminated) and intact non-facial emotional images were recorded from 31 participants using a 60-electrode array. The earliest significant effect of spatial frequency was observed at 135 ms from stimulus onset: N135 component of the ERPs. In line with previous studies, the origin of N135 was localized at secondary visual areas for low-pass filtered stimuli and at primary areas for intact stimuli. Importantly, this component showed an interaction between spatial frequency and emotional content: within low-pass filtered pictures, negative stimuli elicited the highest N135 amplitudes. By contrast, within intact stimuli, neutral pictures were those eliciting the highest amplitudes. These results suggest that high spatial frequencies are not essential for the initial affect-related processing of visual stimuli, which would mainly rely on low spatial frequency visual information. According to present data, high spatial frequencies would come into play later on.

The role of the anterior cingulate cortex in emotional response inhibition

Although the involvement of the anterior cingulate cortex (ACC) in emotional response inhibition is well established, there are several outstanding issues about the nature of this involvement that are not well understood. The present study aimed to examine the precise contribution of the ACC to emotion‐modulated response inhibition by capitalizing on fine temporal resolution of the event‐related potentials (ERPs) and the recent advances in source localization. To this end, participants (N = 30) performed an indirect affective Go/Nogo task (i.e., unrelated to the emotional content of stimulation) that required the inhibition of a motor response to three types of visual stimuli: arousing negative (A−), neutral (N), and arousing positive (A+). Behavioral data revealed that participants made more commission errors to A+ than to N and A−. Electrophysiological data showed that a specific region of the ACC at the intersection of its dorsal and rostral subdivisions was significantly involved in the interaction between emotional processing and motor inhibition. Specifically, activity reflecting this interaction was observed in the P3 (but not in the N2) time range, and was greater during the inhibition of responses to A+ than to N and A−. Additionally, regression analyses showed that inhibition‐related activity within this ACC region was associated with the emotional content of the stimuli (its activity increased as stimulus valence was more positive), and also with behavioral performance (both with reaction times and commission errors). The present results provide additional data for understanding how, when, and where emotion interacts with response inhibition within the ACC. Hum Brain Mapp 33:2147–2160, 2012.

Voltage-based versus factor score-based source localization analyses of electrophysiological brain activity: a comparison.

SummaryThough, traditionally, electrophysiological recordings have been limited to provide temporal information on neural activity, the development of mathematical algorithms capable of solving the inverse problem is facilitating, in recent years, the access to spatial information (i.e., on the origin of neural activation). This study explored a new strategy in order to increase the reliability of inverse problem solutions: applying these algorithms on factor scores (and not on voltages), a parameter that can be defined as “clean amplitude”. Factor scores derive from Principal Component Analysis (PCA) applied to event-related potentials (ERPs). The main advantage of PCA is its capability to extract and quantify ERP components free of the influence of adjacent or subjacent components. The LORETA algorithm for source localization was applied on peak voltage, average voltage and factor scores for the motor potential recorded from 25 subjects, who had to repeatedly press a button with their right hand. The solutions given by LORETA in these three modalities were compared. The motor potential, a negative wave that begins just before any voluntary movement and is centrally distributed in the scalp, is particularly useful to the scope of this study, since its origin is known: contralateral motor cortex. Results show that the three modalities (peak voltage, mean voltage and factor scores) provided the same main focus (left motor cortex), though the “cleanest” solution (i.e., the main focus was more salient with respect to other secondary, noisy foci) was achieved by the factor score‐based LORETA.

THE STRIATUM BEYOND REWARD: CAUDATE RESPONDS INTENSELY TO UNPLEASANT PICTURES

The involvement of striatum in affective processes has been consistently reported in recent years. However, studies within this field have mainly focused on positive affect, revealing the involvement of striatum in reward situations. The present research aimed to explore the involvement of striatum in negative affect through fMRI. To that aim, participants (n=18) were presented with negative, positive and neutral pictures while they performed an indirect task, a strategy repeatedly recommended to avoid cognitive interferences. Positive and negative stimuli did not differ in their arousal levels, as assessed by participants themselves. Analyses of variance showed that caudate nucleus was sensitive to the emotional content of stimulation, negative pictures eliciting greater caudate responses than positive and neutral. Regression analyses indicated that both valence and arousal content of visual stimuli synergically contributed to explain the activation of caudate, whose strong response to negative pictures supports models proposing striatum as a key element in withdrawal situations.

Danger is worse when it moves: neural and behavioral indices of enhanced attentional capture by dynamic threatening stimuli.

Both dynamic non-emotional stimuli (moving dots or digits) and danger-related static stimuli have previously shown to capture attention. This study explored whether the combination of the two factors (i.e., threatening moving stimuli), frequent in natural situations, enhances attentional capture. To this end, static and moving distractors containing emotionally negative and non-negative information were presented to 30 volunteers while they were engaged in a digit categorization task. Behavioral responses and event-related potentials (ERPs) were analyzed. Behavioral and electrophysiological data were convergent: moving negative distractors produced the longest reaction times in the digit categorization task, and elicited the highest amplitudes in the P1 component of the ERPs (peaking at 112ms), an electrophysiological signal of attentional capture. These results suggest that motion provides additional salience to threatening stimuli that facilitates attentional capture.

Differential neural mechanisms underlying exogenous attention to peripheral and central distracters

Mechanisms underlying exogenous attention to central and peripheral distracters were temporally and spatially explored while 30 participants performed a digit categorization task. Neural (event-related potentials-ERPs-, analyzed both at the scalp and at the voxel level) and behavioral indices of exogenous attention were analyzed. Distracters were either biologically salient or neutral, in order to test whether the exogenous attention bias to the former observed in previous studies is independent of, or interacts with, distracter eccentricity. Two subcomponents of the N2 component of the ERPs, N2olp and N2ft, reflected processes related to peripheral distracters processing. N2olp effects, located in the dorsal attention network (supplementary motor area), were probably related to covert reorientation to peripheral distracters. N2ft effects, located in the default mode network (posterior cingulate cortex), appeared to reflect less effort in the ongoing task when peripheral distracters were presented. N2ft also showed a biological saliency effect which was independent of eccentricity and was located in the polar/ventral prefrontal cortex. P3 showed greater amplitudes to centrally presented distracters. These latter effects were located in TEO (visual cortex), and would be functionally associated with spatial interference between the target and central distracters. Behavior showed the relevance of both central and peripheral distracters in exogenous attention. These results indicate that exogenous attention to peripheral distracters differed in temporal and spatial terms from exogenous attention to central distracters and that it is biased towards biologically salient events irrespective of their eccentricity.

Recognition of emotional pictures: Behavioural and electrophysiological measures

The effects of emotional content of images on recognition memory were studied, bringing together electrophysiological (Event-Related brain Potentials, ERPs) and behavioural (accuracy and speed of recognition, and remember/know judgements) indices. In the study phase, participants assessed 120 images on the scales of valence and arousal. In the test phase, ERPs were recorded while participants viewed again the images, put together with 120 new, and were asked to make old/new decisions and remember/know judgements on them. A clear arousal bias was obtained for remember/know judgements, which revealed that correctly recognised arousing images (negative and positive) received more remember judgements than nonarousing images (neutral and relaxing). Moreover, a Late Positive Component (LPC) activation revealed an old/new effect enhanced by arousing images. The LPC activation was located in parietal areas (precuneus), which appears to be mostly related to successful retrieval based on recollection. The results obtained through different indices supported the emotional bias found in previous studies for arousing material, but do not clarify the effect of the emotional valence on recognition.

Working memory of emotional stimuli: Electrophysiological characterization

Memorizing emotional stimuli in a preferential way seems to be one of the adaptive strategies brought on by evolution for supporting survival. However, there is a lack of electrophysiological evidence on this bias in working memory. The present study analyzed the influence of emotion on the updating component of working memory. Behavioral and electrophysiological indices were measured from a 3-back task using negative, neutral, and positive faces. Electrophysiological data evidenced an emotional influence on the working memory sensitive P3 component, which presented larger amplitudes for negative matching faces compared to neutral ones. This effect originated in the superior parietal cortex, previously reported to be involved in N-back tasks. Additionally, P3 results showed a correlation with reaction times, where higher amplitudes were associated with faster responses for negative matching faces. These findings indicate that electrophysiological measures seem to be very suitable indices of the emotional influence on working memory.