Luis Carretié

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.

Emotion and Attention Interaction Studied through Event-Related Potentials

Several studies on hemodynamic brain activity indicate that emotional visual stimuli elicit greater activation than neutral stimuli in attention-related areas such as the anterior cingulate cortex (ACC) and the visual association cortex (VAC). In order to explore the temporo-spatial characteristics of the interaction between attention and emotion, two processes characterized by involving short and rapid phases, event-related potentials (ERPs) were measured in 29 subjects using a 60-electrode array and the LORETA source localization software. A cue/target paradigm was employed in order to investigate both expectancy-related and input processing related attention. Four categories of stimuli were presented to subjects: positive arousing, negative arousing, relaxing, and neutral. Three attention-related components were finally analyzed: N280pre (from pretarget ERPs), P200post and P340post (both from posttarget ERPs). N280pre had a prefrontal focus (ACC and/or medial prefrontal cortex) and presented significantly lower amplitudes in response to cues announcing negative targets. This result suggests a greater capacity of nonaversive stimuli to generate expectancy-related attention. P200post and P340post were both elicited in the VAC, and showed their highest amplitudes in response to negative- and to positive-arousing stimuli, respectively. The origin of P200post appears to be located dorsally with respect to the clear ventral-stream origin of P340post. The conjunction of temporal and spatial characteristics of P200post and P340post leads to the deduction that input processing-related attention associated with emotional visual stimulation involves an initial, rapid, and brief early attentional response oriented to rapid motor action, being more prominent towards negative stimulation. This is followed by a slower but longer late attentional response oriented to deeper processing, elicited to a greater extent by appetitive stimulation.

Emotional context modulates response inhibition: Neural and behavioral data

Although recent hemodynamic studies indicate that neural activity related to emotion and that associated with response inhibition constitute closely interrelated and mutually dependent processes, the nature of this relationship is still unclear. In order to explore the temporo-spatial characteristics of the interaction between emotion and inhibition, event-related potentials (ERPs) were measured as participants (N=30) performed a modified version of the Go/Nogo task that required the inhibition of prepotent responses to neutral cues during three different emotional contexts: negative, neutral, and positive. Temporal and spatial principal component analyses were employed to detect and quantify, in a reliable manner, those ERP components related to response inhibition (i.e., Nogo-N2 and Nogo-P3), and a source-localization technique (sLORETA) provided information on their neural origin. Behavioral analyses revealed that reaction times (RTs) to Go cues were shorter during the positive context than during neutral and negative contexts. ERP analyses showed that suppressing responses to Nogo cues within the positive context elicited larger frontocentral Nogo-P3 amplitudes and enhanced anterior cingulate cortex (ACC) activation than within the negative context. Regression analyses revealed that Nogo-P3 (i) was inversely related to RTs, supporting its association with the inhibition of a prepotent response, and (ii) was associated with contextual valence (amplitude increased as context valence was more positive), but not with contextual arousal. These results suggest that withholding a prepotent response within positively valenced contexts is more difficult and requires more inhibitory control than within negatively valenced contexts.

Exogenous (automatic) attention to emotional stimuli: a review.

Current knowledge on the architecture of exogenous attention (also called automatic, bottom-up, or stimulus-driven attention, among other terms) has been mainly obtained from studies employing neutral, anodyne stimuli. Since, from an evolutionary perspective, exogenous attention can be understood as an adaptive tool for rapidly detecting salient events, reorienting processing resources to them, and enhancing processing mechanisms, emotional events (which are, by definition, salient for the individual) would seem crucial to a comprehensive understanding of this process. This review, focusing on the visual modality, describes 55 experiments in which both emotional and neutral irrelevant distractors are presented at the same time as ongoing task targets. Qualitative and, when possible, meta-analytic descriptions of results are provided. The most conspicuous result is that, as confirmed by behavioral and/or neural indices, emotional distractors capture exogenous attention to a significantly greater extent than do neutral distractors. The modulatory effects of the nature of distractors capturing attention, of the ongoing task characteristics, and of individual differences, previously proposed as mediating factors, are also described. Additionally, studies reviewed here provide temporal and spatial information—partially absent in traditional cognitive models—on the neural basis of preattention/evaluation, reorienting, and sensory amplification, the main subprocesses involved in exogenous attention. A model integrating these different levels of information is proposed. The present review, which reveals that there are several key issues for which experimental data are surprisingly scarce, confirms the relevance of including emotional distractors in studies on exogenous attention.

N170 sensitivity to facial expression: A meta-analysis

The N170 component is the most important electrophysiological index of face processing. Early studies concluded that it was insensitive to facial expression, thus supporting dual theories postulating separate mechanisms for identity and expression encoding. However, recent evidence contradicts this assumption. We conducted a meta-analysis to resolve inconsistencies and to derive theoretical implications. A systematic revision of 128 studies analyzing N170 in response to neutral and emotional expressions yielded 57 meta-analyzable experiments (involving 1645 healthy adults). First, the N170 was found to be sensitive to facial expressions, supporting proposals arguing for integrated rather than segregated mechanisms in the processing of identity and expression. Second, this sensitivity is heterogeneous, with anger, fear and happy faces eliciting the largest N170 amplitudes. Third, we explored some modulatory factors, including the focus of attention - N170 amplitude was found to be also sensitive to unattended expressions - or the reference electrode -common reference reinforcing the effects- . In sum, N170 is a valuable tool to study the neural processing of facial expressions in order to develop current theories.

Electrophysiological differences in the processing of affective information in words and pictures.

It is generally assumed that affective picture viewing is related to higher levels of physiological arousal than is the reading of emotional words. However, this assertion is based mainly on studies in which the processing of either words or pictures has been investigated under heterogenic conditions. Positive, negative, relaxing, neutral, and background (stimulus fragments) words and pictures were presented to subjects in two experiments under equivalent experimental conditions. In Experiment 1, neutral words elicited an enhanced late positive component (LPC) that was associated with an increased difficulty in discriminating neutral from background stimuli. In Experiment 2, high-arousing pictures elicited an enhanced early negativity and LPC that were related to a facilitated processing for these stimuli. Thus, it seems that under some circumstances, the processing of affective information captures attention only with more biologically relevant stimuli. Also, these data might be better interpreted on the basis of those models that postulate a different access to affective information for words and pictures.

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.

Spatiotemporal characterization of response inhibition

Despite an extensive literature on the neural substrates of response inhibition, when and where this process occurs in the brain remain unclear. The present study aimed to shed light on this issue by exploiting the high temporal resolution of the event-related potentials (ERPs) and recent advances in source localization. Temporo-spatial principal component analysis was employed to define more precisely the two ERP components most often associated with response inhibition (i.e., frontocentral N2 and frontocentral P3), as well as to improve the accuracy of source localization. In addition, participants (N=40) performed a modified Go/Nogo task composed of three types of stimuli (frequent-Go, infrequent-Go, and infrequent-Nogo), which allowed us to dissociate neural activity associated with response inhibition from that related to novelty processing by directly contrasting nogo and go trials matched with respect to frequency of occurrence. Scalp ERP data indicated that the frontocentral P3, but not the frontocentral N2, showed larger amplitudes for infrequent-Nogo than for infrequent-Go trials. Source localization data parallel the results obtained at the scalp level: only P3-related activity showed differences between infrequent-Nogo and infrequent-Go trials. This increased activation was observed predominantly in the presupplementary motor area (preSMA). Present results suggest that the frontocentral P3 and the preSMA play a core role in response inhibition. The findings of this study substantiate and complement previous results obtained by hemodynamic procedures.