Action Observation Network Activity Related to Object-Directed and Socially-Directed Actions in Adolescents.

The human action observation network (AON) encompasses brain areas consistently engaged when we observe other's actions. Although the core nodes of the AON are present from childhood, it is not known to what extent they are sensitive to different action features during development. Because social cognitive abilities continue to mature during adolescence, the AON response to socially-oriented actions, but not to object-related actions, may differ in adolescents and adults. To test this hypothesis, we scanned with functional magnetic resonance imaging (fMRI) male and female typically-developing teenagers (n = 28; 13 females) and adults (n = 25; 14 females) while they passively watched videos of manual actions varying along two dimensions: sociality (i.e., directed toward another person or not) and transitivity (i.e., involving an object or not). We found that action observation recruited the same fronto-parietal and occipito-temporal regions in adults and adolescents. The modulation of voxel-wise activity according to the social or transitive nature of the action was similar in both groups of participants. Multivariate pattern analysis, however, revealed that decoding accuracies in intraparietal sulcus (IPS)/superior parietal lobe (SPL) for both sociality and transitivity were lower for adolescents compared with adults. In addition, in the lateral occipital temporal cortex (LOTC), generalization of decoding across the orthogonal dimension was lower for sociality only in adolescents. These findings indicate that the representation of the content of others' actions, and in particular their social dimension, in the adolescent AON is still not as robust as in adults.SIGNIFICANCE STATEMENT The activity of the action observation network (AON) in the human brain is modulated according to the purpose of the observed action, in particular the extent to which it involves interaction with an object or with another person. How this conceptual representation of actions is implemented during development is largely unknown. Here, using multivoxel pattern analysis (MVPA) of functional magnetic resonance imaging (fMRI) data, we discovered that, while the action observation network is in place in adolescence, the fine-grain organization of its posterior regions is less robust than in adults to decode the abstract social dimensions of an action. This finding highlights the late maturation of social processing in the human brain.

Brain Activity During Antisaccades to Faces in Adolescence.

Cognitive control and social perception both change during adolescence, but little is known of the interaction of these 2 processes. We aimed to characterize developmental changes in brain activity related to the influence of a social stimulus on cognitive control and more specifically on inhibitory control. Children (age 8-11, n = 19), adolescents (age 12-17, n = 20), and adults (age 24-40, n = 19) performed an antisaccade task with either faces or cars as visual stimuli, during functional magnetic resonance brain imaging. We replicate the finding of the engagement of the core oculomotor and face perception brain regions in all age-groups, with increased involvement of frontoparietal oculomotor regions and fusiform face regions with age. The antisaccade-related activity was modulated by stimulus category significantly only in adolescents. This interaction was observed mainly in occipitotemporal regions as well as in supplementary motor cortex and postcentral gyrus. These results indicate a special treatment of social stimuli during adolescence.

Preserved Contextual Cueing in Realistic Scenes in Patients with Age-Related Macular Degeneration.

Foveal vision loss has been shown to reduce efficient visual search guidance due to contextual cueing by incidentally learned contexts. However, previous studies used artificial (T- among L-shape) search paradigms that prevent the memorization of a target in a semantically meaningful scene. Here, we investigated contextual cueing in real-life scenes that allow explicit memory of target locations in semantically rich scenes. In contrast to the contextual cueing deficits in artificial scenes, contextual cueing in patients with age-related macular degeneration (AMD) did not differ from age-matched normal-sighted controls. We discuss this in the context of visuospatial working-memory demands for which both eye movement control in the presence of central vision loss and memory-guided search may compete. Memory-guided search in semantically rich scenes may depend less on visuospatial working memory than search in abstract displays, potentially explaining intact contextual cueing in the former but not the latter. In a practical sense, our findings may indicate that patients with AMD are less deficient than expected after previous lab experiments. This shows the usefulness of realistic stimuli in experimental clinical research.

Intact Contextual Cueing for Search in Realistic Scenes with Simulated Central or Peripheral Vision Loss.

Purpose: Search in repeatedly presented visual search displays can benefit from implicit learning of the display items' spatial configuration. This effect has been named contextual cueing. Previously, contextual cueing was found to be reduced in observers with foveal or peripheral vision loss. Whereas this previous work used symbolic (T among L-shape) search displays with arbitrary configurations, here we investigated search in realistic scenes. Search in meaningful realistic scenes may benefit much more from explicit memory of the target location. We hypothesized that this explicit recall of the target location reduces visuospatial working memory demands on search considerably, thereby enabling efficient search guidance by learnt contextual cues in observers with vision loss. Methods: Two experiments with gaze-contingent scotoma simulation (Experiment 1: central scotoma, Experiment 2: peripheral scotoma) were carried out with normal-sighted observers (total n = 39/40). Observers had to find a cup in pseudorealistic indoor scenes and discriminate the direction of the cup's handle. Results: With both central and peripheral scotoma simulation, contextual cueing was observed in repeatedly presented configurations. Conclusions: The data show that patients suffering from central or peripheral vision loss may benefit more from memory-guided visual search than would be expected from scotoma simulation and patient studies using abstract symbolic search displays. Translational Relevance: In the assessment of visual search in patients with vision loss, semantically meaningless abstract search displays may gain insights into deficient search functions, but more realistic meaningful search scenes are needed to assess whether search deficits can be compensated.

Not scene learning, but attentional processing is superior in team sport athletes and action video game players.

We tested if high-level athletes or action video game players have superior context learning skills. Incidental context learning was tested in a spatial contextual cueing paradigm. We found comparable contextual cueing of visual search in repeated displays in high-level amateur handball players, dedicated action video game players and normal controls. In contrast, both handball players and action video game players showed faster search than controls, measured as search time per display item, independent of display repetition. Thus, our data do not indicate superior context learning skills in athletes or action video game players. Rather, both groups showed more efficient visual search in abstract displays that were not related to sport-specific situations.

Impairment of visual memory for objects in natural scenes by simulated central scotomata.

Because of the close link between foveal vision and the spatial deployment of attention, typically only objects that have been foveated during scene exploration may form detailed and persistent memory representations. In a recent study on patients suffering from age-related macular degeneration, however, we found surprisingly accurate visual long-term memory for objects in scenes. Normal exploration patterns that the patients had learned to rereference saccade targets to an extrafoveal retinal location. This rereferencing may allow use of an extrafoveal location as a focus of attention for efficient object encoding into long-term memory. Here, we tested this hypothesis in normal-sighted observers with gaze-contingent central scotoma simulations. As these observers were inexperienced in scene exploration with central vision loss and had not developed saccadic rereferencing, we expected deficits in long-term memory for objects. We used the same change detection task as in our patient study, probing sensitivity to object changes after a period of free scene exploration. Change detection performance was significantly reduced for two types of scotoma simulation diminishing foveal and parafoveal vision--a visible gray disc and a more subtle image warping--compared with unimpaired controls, confirming our hypothesis. The impact of a smaller scotoma covering specifically foveal vision was less distinct, leading to a marginally significant decrease of long-term memory performance compared with controls. We conclude that attentive encoding of objects is deficient when central vision is lost as long as successful saccadic rereferencing has not yet developed.

Central and peripheral vision loss differentially affects contextual cueing in visual search.

Visual search for targets in repeated displays is more efficient than search for the same targets in random distractor layouts. Previous work has shown that this contextual cueing is severely impaired under central vision loss. Here, we investigated whether central vision loss, simulated with gaze-contingent displays, prevents the incidental learning of contextual cues or the expression of learning, that is, the guidance of search by learned target-distractor configurations. Visual search with a central scotoma reduced contextual cueing both with respect to search times and gaze parameters. However, when the scotoma was subsequently removed, contextual cueing was observed in a comparable magnitude as for controls who had searched without scotoma simulation throughout the experiment. This indicated that search with a central scotoma did not prevent incidental context learning, but interfered with search guidance by learned contexts. We discuss the role of visuospatial working memory load as source of this interference. In contrast to central vision loss, peripheral vision loss was expected to prevent spatial configuration learning itself, because the restricted search window did not allow the integration of invariant local configurations with the global display layout. This expectation was confirmed in that visual search with a simulated peripheral scotoma eliminated contextual cueing not only in the initial learning phase with scotoma, but also in the subsequent test phase without scotoma.

Visual memory for objects following foveal vision loss.

Allocation of visual attention is crucial for encoding items into visual long-term memory. In free vision, attention is closely linked to the center of gaze, raising the question whether foveal vision loss entails suboptimal deployment of attention and subsequent impairment of object encoding. To investigate this question, we examined visual long-term memory for objects in patients suffering from foveal vision loss due to age-related macular degeneration. We measured patients' change detection sensitivity after a period of free scene exploration monocularly with their worse eye when possible, and under binocular vision, comparing sensitivity and eye movements to matched normal-sighted controls. A highly salient cue was used to capture attention to a nontarget location before a target change occurred in half of the trials, ensuring that change detection relied on memory. Patients' monocular and binocular sensitivity to object change was comparable to controls, even after more than 4 intervening fixations, and not significantly correlated with visual impairment. We conclude that extrafoveal vision suffices for efficient encoding into visual long-term memory.

Prediction of higher visual function in macular degeneration with multifocal electroretinogram and multifocal visual evoked potential.

OBJECTIVE: Visual search can be guided by past experience of regularities in our visual environment. This search guidance by contextual memory cues is impaired by foveal vision loss. Here we compared retinal and cortical visually evoked responses in their predictive value for contextual cueing impairment and visual acuity. METHODS: Multifocal electroretinograms to flash stimulation (mfERGs; 103 locations; 55.8° diameter) and visual evoked potentials to pattern-reversal stimulation (mfVEPs; 60 locations; 48.6° diameter) were recorded monocularly in participants with age-related macular degeneration (n = 14 and 16, respectively). Response magnitudes were calculated as the respective signal-to-noise ratios for each eccentricity. Visual acuities (logMAR, range: 0.0-1.2) and contextual cueing effects on visual search (reaction time gain, range: -0.14-0.15) were correlated with the signal-to-noise ratios. A step-wise regression analysis was applied separately to the mfERG- and mfVEP-dataset to determine the eccentricity range and the processing stage that is critical for these visual functions. RESULTS: Central mfERGs (1.0-3.2°) were the sole predictor of contextual cueing of visual search (p = 0.006), but they were not significant predictors of visual acuity. In contrast, central mfVEPs (1.3-3.2°) were the sole predictor of visual acuity (p < 0.001), but they were not significant predictors of contextual cueing. CONCLUSIONS: Contextual cueing is more dependent on parafoveal mfERG magnitude while visual acuity is more dependent on parafoveal mfVEP magnitude. The relation of contextual cueing to parafoveal mfERG magnitudes indicates the predictive value of retinal bipolar cell activity for this advanced level of visual function.

The right temporo-parietal junction contributes to visual feature binding.

We investigated the neural basis of conjoined processing of color and spatial frequency with functional magnetic resonance imaging (fMRI). A multivariate classification algorithm was trained to differentiate between either isolated color or spatial frequency differences, or between conjoint differences in both feature dimensions. All displays were presented in a singleton search task, avoiding confounds between conjunctive feature processing and search difficulty that arose in previous studies contrasting single feature and conjunction search tasks. Based on patient studies, we expected the right temporo-parietal junction (TPJ) to be involved in conjunctive feature processing. This hypothesis was confirmed in that only conjoined color and spatial frequency differences, but not isolated feature differences could be classified above chance level in this area. Furthermore, we could show that the accuracy of a classification of differences in both feature dimensions was superadditive compared to the classification accuracies of isolated color or spatial frequency differences within the right TPJ. These data provide evidence for the processing of feature conjunctions, here color and spatial frequency, in the right TPJ.

Attentional adjustment to conflict strength: evidence from the effects of manipulating flanker-target SOA on response times and prestimulus pupil size.

Current models of cognitive control assume gradual adjustment of processing selectivity to the strength of conflict evoked by distractor stimuli. Using a flanker task, we varied conflict strength by manipulating target and distractor onset. Replicating previous findings, flanker interference effects were larger on trials associated with advance presentation of the flankers compared to simultaneous presentation. Controlling for stimulus and response sequence effects by excluding trials with feature repetitions from stimulus administration (Experiment 1) or from the statistical analyses (Experiment 2), we found a reduction of the flanker interference effect after high-conflict predecessor trials (i.e., trials associated with advance presentation of the flankers) but not after low-conflict predecessor trials (i.e., trials associated with simultaneous presentation of target and flankers). This result supports the assumption of conflict-strength-dependent adjustment of visual attention. The selective adaptation effect after high-conflict trials was associated with an increase in prestimulus pupil diameter, possibly reflecting increased cognitive effort of focusing attention.

Contextual cueing impairment in patients with age-related macular degeneration.

Visual attention can be guided by past experience of regularities in our visual environment. In the contextual cueing paradigm, incidental learning of repeated distractor configurations speeds up search times compared to random search arrays. Concomitantly, fewer fixations and more direct scan paths indicate more efficient visual exploration in repeated search arrays. In previous work, we found that simulating a central scotoma in healthy observers eliminated this search facilitation. Here, we investigated contextual cueing in patients with age-related macular degeneration (AMD) who suffer from impaired foveal vision. AMD patients performed visual search using only their more severely impaired eye (n = 13) as well as under binocular viewing (n = 16). Normal-sighted controls developed a significant contextual cueing effect. In comparison, patients showed only a small nonsignificant advantage for repeated displays when searching with their worse eye. When searching binocularly, they profited from contextual cues, but still less than controls. Number of fixations and scan pattern ratios showed a comparable pattern as search times. Moreover, contextual cueing was significantly correlated with acuity in monocular search. Thus, foveal vision loss may lead to impaired guidance of attention by contextual memory cues.

A behavioral task for the validation of a gaze-contingent simulated scotoma.

Gaze-contingent displays provide a valuable method in visual research for controlling visual input and investigating its visual and cognitive processing. Although the body of research using gaze-contingent retinal stabilization techniques has grown considerably during the last decade, only few studies have been concerned with the reliability of the specific real-time simulations applied. Using a Landolt ring discrimination task, we present a behavioral validation of gaze-contingent central scotoma simulation in healthy observers. Importantly, behavioral testing is necessary to show whether the simulation impairs foveal processing of visual information. This test becomes even more crucial when researchers are faced with null results in a task performed with the scotoma, as compared with a control condition. It must be ruled out that the lack of behavioral effects results from a type II error caused by improper implementation before conclusions about foveal contributions to the given task may be drawn. In our experiment, the scotoma effectively prevented foveal processing of the visual stimuli, leading to significantly reduced response accuracies, as compared with unimpaired vision. Moreover, the final fixation at the time of the participants' responses was placed close to the target position in the unimpaired condition, whereas the distance to the target was enhanced with the scotoma, indicating that the observers were not able to discriminate visual target stimuli from distractors, due to the scotoma. The present work presents a validated behavioral testing method for the efficiency of gaze-contingent scotoma simulations, including code for implementation. In addition, solutions for common methodological problems are discussed.

Evidence for feature binding in the superior parietal lobule.

The neural substrates of feature binding are an old, yet still not completely resolved problem. While patient studies suggest that posterior parietal cortex is necessary for feature binding, imaging evidence has been inconclusive in the past. These studies compared visual feature and conjunction search to investigate the neural substrate of feature conjunctions. However, a common problem of these comparisons was a confound with search difficulty. To circumvent this confound, we directly investigated the localized representation of features (color and spatial frequency) and feature conjunctions in a single search task by using multivariate pattern analysis at high field strength (7T). In right superior parietal lobule, we found evidence for the representation of feature conjunctions that could not be explained by the summation of individual feature representations and thus indicates conjoined processing of color and spatial frequency.

Simulated loss of foveal vision eliminates visual search advantage in repeated displays.

In the contextual cueing paradigm, incidental visual learning of repeated distractor configurations leads to faster search times in repeated compared to new displays. This contextual cueing is closely linked to the visual exploration of the search arrays as indicated by fewer fixations and more efficient scan paths in repeated search arrays. Here, we examined contextual cueing under impaired visual exploration induced by a simulated central scotoma that causes the participant to rely on extrafoveal vision. We let normal-sighted participants search for the target either under unimpaired viewing conditions or with a gaze-contingent central scotoma masking the currently fixated area. Under unimpaired viewing conditions, participants revealed shorter search times and more efficient exploration of the display for repeated compared to novel search arrays and thus exhibited contextual cueing. When visual search was impaired by the central scotoma, search facilitation for repeated displays was eliminated. These results indicate that a loss of foveal sight, as it is commonly observed in maculopathies, e.g., may lead to deficits in high-level visual functions well beyond the immediate consequences of a scotoma.

Visual search facilitation in repeated displays depends on visuospatial working memory.

When distractor configurations are repeated over time, visual search becomes more efficient, even if participants are unaware of the repetition. This contextual cueing is a form of incidental, implicit learning. One might therefore expect that contextual cueing does not (or only minimally) rely on working memory resources. This, however, is debated in the literature. We investigated contextual cueing under either a visuospatial or a nonspatial (color) visual working memory load. We found that contextual cueing was disrupted by the concurrent visuospatial, but not by the color working memory load. A control experiment ruled out that unspecific attentional factors of the dual-task situation disrupted contextual cueing. Visuospatial working memory may be needed to match current display items with long-term memory traces of previously learned displays.