Survival in dynamic environments requires that organisms learn to predict danger from situational cues. One key facet of threat prediction is generalization from a predictive cue to similar cues, ensuring that a cue-outcome contingency is applied beyond the original learning environment. Generalization has been observed in laboratory studies of aversive conditioning: Behavioral and physiological processes generalize responses from a stimulus paired with threat (the conditioned stimulus [CS+]) to unpaired stimuli, with response magnitudes varying with CS+ similarity. In contrast, work focusing on sensory responses in visual cortex has found a sharpening pattern, in which responses to stimuli closely resembling the CS+ are maximally suppressed, potentially reflecting lateral inhibitory interactions with the CS+ representation. Originally demonstrated with simple visual cues, changes in visuocortical tuning have also been observed in threat generalization learning across facial identities. It is unclear to what extent these visuocortical changes represent transient or sustained effects and if generalization learning requires prior conditioning to the CS+. The present study addressed these questions using EEG and pupillometry in an aversive generalization paradigm involving hundreds of trials using a gradient of facial identities. Visuocortical steady-state visual evoked potential sharpening occurred after dozens of trials of generalization learning without prior differential conditioning, but diminished as learning continued. By contrast, generalization of alpha power suppression, pupil dilation, and self-reported valence and arousal was seen throughout the experiment. Findings are consistent with threat processing models emphasizing the role of changing visucocortical and attentional dynamics when forming, curating, and shaping fear memories as observers continue learning about stimulus-outcome contingencies.

Recent EEG studies have investigated basic principles of feature-based attention by means of frequency-tagged random dot kinematograms in which different colors are simultaneously presented at different temporal frequencies to elicit steady-state visual evoked potentials (SSVEPs). These experiments consistently showed global facilitation of the to-be-attended random dot kinematogram—a basic principle of feature-based attention. SSVEP source estimation suggested that posterior visual cortex from V1 to area hMT+/V5 is broadly activated by frequency-tagged stimuli. What is presently unknown is whether the feature-based attentional facilitation of SSVEPs is a rather unspecific neural response including all visual areas that follow the “on/off,” or whether SSVEP feature-based amplitude enhancements are driven by activity in visual areas most sensitive to a specific feature, such as V4v in the case of color. Here, we leverage multimodal SSVEP-fMRI recordings in human participants and a multidimensional feature-based attention paradigm to investigate this question. Attending to shape produced significantly greater SSVEP-BOLD covariation in primary visual cortex compared with color. SSVEP-BOLD covariation during color selection increased along the visual hierarchy, with greatest values in areas V3 and V4. Importantly, in area hMT+/V5, we found no differences between shape and color selection. Results suggest that SSVEP amplitude enhancements in feature-based attention is not an unspecific enhancement of neural activity in all visual areas following the “on/off.” These findings open new avenues to investigating neural dynamics of competitive interactions in specific visual areas sensitive to a certain feature in a more economical way and better temporal resolution compared with fMRI.

Using electrophysiology and a classic fear conditioning paradigm, this work examined adaptive visuocortical changes in spatial frequency tuning in a sample of 50 undergraduate students. High-density EEG was recorded while participants viewed 400 total trials of individually presented Gabor patches of 10 different spatial frequencies. Patches were flickered to produce sweep steady-state visual evoked potentials (ssVEPs) at a temporal frequency of 13.33 Hz, with stimulus contrast ramping up from 0% to 41% Michelson over the course of each 2800-msec trial. During the final 200 trials, a selected range of Gabor stimuli (either the lowest or highest spatial frequencies, manipulated between participants) were paired with an aversive 90-dB white noise auditory stimulus. Changes in spatial frequency tuning from before to after conditioning for paired and unpaired gratings were evaluated at the behavioral and electrophysiological level. Specifically, ssVEP amplitude changes were evaluated for lateral inhibition and generalization trends, whereas change in alpha band (8–12 Hz) activity was tested for a generalization trend across spatial frequencies, using permutation-controlled F contrasts. Overall time courses of the sweep ssVEP amplitude envelope and alpha-band power were orthogonal, and ssVEPs proved insensitive to spatial frequency conditioning. Alpha reduction (blocking) was most pronounced when viewing fear-conditioned spatial frequencies, with blocking decreasing along the gradient of spatial frequencies preceding conditioned frequencies, indicating generalization across spatial frequencies. Results suggest that alpha power reduction—conceptually linked to engagement of attention and alertness/arousal mechanisms—to fear-conditioned stimuli operates independently of low-level spatial frequency processing (indexed by ssVEPs) in primary visual cortex.

Emotionally salient cues are detected more readily, remembered better, and evoke greater visual cortical responses compared with neutral stimuli. The current study used concurrent EEG-fMRI recordings to identify large-scale network interactions involved in the amplification of visual cortical activity when viewing aversively conditioned cues. To generate a continuous neural signal from pericalcarine visual cortex, we presented rhythmic (10/sec) phase-reversing gratings, the orientation of which predicted the presence (CS+) or absence (CS−) of a cutaneous electric shock (i.e., the unconditioned stimulus). The resulting single trial steady-state visual evoked potential (ssVEP) amplitude was regressed against the whole-brain BOLD signal, resulting in a measure of ssVEP-BOLD coupling. Across all trial types, ssVEP-BOLD coupling was observed in both primary and extended visual cortical regions, the rolandic operculum, as well as the thalamus and bilateral hippocampus. For CS+ relative to CS− trials during the conditioning phase, BOLD-alone analyses showed CS+ enhancement at the occipital pole, superior temporal sulci, and the anterior insula bilaterally, whereas ssVEP-BOLD coupling was greater in the pericalcarine cortex, inferior parietal cortex, and middle frontal gyrus. Dynamic causal modeling analyses supported connectivity models in which heightened activity in pericalcarine cortex for threat (CS+) arises from cortico-cortical top–down modulation, specifically from the middle frontal gyrus. No evidence was observed for selective pericalcarine modulation by deep cortical structures such as the amygdala or anterior insula, suggesting that the heightened engagement of pericalcarine cortex for threat stimuli is mediated by cortical structures that constitute key nodes of canonical attention networks.

Stimuli of high emotional significance such as social threat cues are preferentially processed in the human brain. However, there is an ongoing debate whether or not these stimuli capture attention automatically and weaken the processing of concurrent stimuli in the visual field. This study examined continuous fluctuations of electrocortical facilitation during competition of two spatially separated facial expressions in high and low socially anxious individuals. Two facial expressions were flickered for 3000 msec at different frequencies (14 and 17.5 Hz) to separate the electrocortical signals evoked by the competing stimuli (“frequency tagging”). Angry faces compared to happy and neutral expressions were associated with greater electrocortical facilitation over visual areas only in the high socially anxious individuals. This finding was independent of the respective competing stimulus. Heightened electrocortical engagement in socially anxious participants was present in the first second of stimulus viewing and was sustained for the entire presentation period. These results, based on a continuous measure of attentional resource allocation, support the view that stimuli of high personal significance are associated with early and sustained prioritized sensory processing. These cues, however, do not interfere with the electrocortical processing of a spatially separated concurrent face, suggesting that they are effective at capturing attention, but are weak competitors for resources.

Habituation refers to a decline in orienting or responding to a repeated stimulus, and can be inferred to reflect learning about the properties of the repeated stimulus when followed by increased orienting to a novel stimulus (i.e., novelty detection). Habituation and novelty detection paradigms have been used for over 40 years to study perceptual and mnemonic processes in the human infant, yet important questions remain about the nature of these processes in infants. The aim of the present study was to examine the neural mechanisms underlying habituation and novelty detection in infants. Specifically, we investigated changes in induced alpha, beta, and gamma activity in 6-month-old infants during repeated presentations of either a face or an object, and examined whether these changes predicted behavioral responses to novelty at test. We found that induced gamma activity over occipital scalp regions decreased with stimulus repetition in the face condition but not in the toy condition, and that greater decreases in the gamma band were associated with enhanced orienting to a novel face at test. The pattern and topography of these findings are consistent with observations of repetition suppression in the occipital–temporal visual processing pathway, and suggest that encoding in infant habituation paradigms may reflect a form of perceptual learning. Implications for the role of repetition suppression in infant habituation and novelty detection are discussed with respect to a biased competition model of visual attention.

The human brain has evolved to process motivationally relevant information in an optimized manner. The perceptual benefit for emotionally arousing material, termed motivated attention, is indexed by electrocortical amplification at various levels of stimulus analysis. An outstanding issue, particularly on a neuronal level, refers to whether and how perceptual enhancement for arousing signals translates into modified processing of information presented in temporal or spatial proximity to the affective cue. The present studies aimed to examine facilitation and interference effects of task-irrelevant emotional pictures on subsequent word identification. In the context of forced-choice lexical decision tasks, pictures varying in hedonic valence and emotional arousal preceded word/ pseudoword targets. Across measures and experiments, high-arousing compared to low-arousing pictures were associated with impaired processing of word targets. Arousing pleasant and unpleasant pictures prolonged word reaction times irrespective of stimulus-onset asynchrony (80 msec, 200 msec, 440 msec) and salient semantic category differences (e.g., erotica vs. mutilation pictures). On a neuronal level, interference was reflected in reduced N1 responses (204–264 msec) to both target types. Paralleling behavioral effects, suppression of the late positivity (404–704 msec) was more pronounced for word compared to pseudoword targets. Regional source modeling indicated that early reduction effects originated from inhibited cortical activity in posterior areas of the left inferior temporal cortex associated with orthographic processing. Modeling of later reduction effects argues for interference in distributed semantic networks comprising left anterior temporal and parietal sources. Thus, affective processing interferes with subsequent lexico-semantic analysis along the ventral stream.

In the present study, subjects selectively attended to the color of checkerboards in a feature-based attention paradigm. Induced gamma band responses (GBRs), the induced alpha band, and the event-related potential (ERP) were analyzed to uncover neuronal dynamics during selective feature processing. Replicating previous ERP findings, the selection negativity (SN) with a latency of about 160 msec was extracted. Furthermore, and similarly to previous EEG studies, a gamma band peak in a time window between 290 and 380 msec was found. This peak had its major energy in the 55to 70-Hz range and was significantly larger for the attended color. Contrary to previous human induced gamma band studies, a much earlier 40to 50-Hz peak in a time window between 160 and 220 msec after stimulus onset and, thus, concurrently to the SN was prominent with significantly more energy for attended as opposed to unattended color. The induced alpha band (9.8–11.7 Hz), on the other hand, exhibited a marked suppression for attended color in a time window between 450 and 600 msec after stimulus onset. A comparison of the time course of the 40to 50-Hz and 55to 70-Hz induced GBR, the induced alpha band, and the ERP revealed temporal coincidences for changes in the morphology of these brain responses. Despite these similarities in the time domain, the cortical source configuration was found to discriminate between induced GBRs and the SN. Our results suggest that large-scale synchronous high-frequency brain activity as measured in the human GBR play a specific role in attentive processing of stimulus features.

Fragmented pictures of an object, which appear meaningless when seen for the first time, can easily be identified after the presentation of an unfragmented version of the same picture. The neuronal mechanism for such a rapid perceptual learning phenomenon is largely unknown. Recently, induced gamma band responses (GBRs) have been discussed as a possible physiological correlate of activity in cell assemblies formed by learning. The present study was designed to investigate the modulation of induced GBRs in a perceptual learning task by using a 128-channel EEG montage. In the first sequence of the experiment, fragmented pictures from the Snodgrass and Vandervart inventory were presented. The fragmentation of the pictures was selected that subjects were unable to identify them. In the second experimental sequence the perceptual learning sequence half of the pictures were displayed in their unfragmented version. In the third sequence, all pictures were presented again in the fragmented version. Now, subjects had to rate whether or not they could identify the images. Results showed an increase in spectral gamma power at parietal electrode sites for identified pictures. In addition, neural activity in the gamma band was highly synchronized between posterior electrodes. For pictures not presented in their complete version, we found no such pattern in the third sequence. From our results, we concluded that induced GBRs might represent a signature of synchronized neural activity in a Hebbian cell assembly, activated by the fragmented picture after perceptual learning took place. No difference between identified and unidentified pictures was found in the visual evoked potential in the same time range and in the evoked GBR in the same frequency range as the induced response.