Christoph Bledowski

Localizing P300 Generators in Visual Target and Distractor Processing: A Combined Event-Related Potential and Functional Magnetic Resonance Imaging Study

Constraints from functional magnetic resonance imaging (fMRI) were used to identify the sources of the visual P300 event-related potential (ERP). Healthy subjects performed a visual three-stimulus oddball paradigm with a difficult discrimination task while fMRI and high-density ERP data were acquired in separate sessions. This paradigm allowed us to differentiate the P3b component of the P300, which has been implicated in the detection of rare events in general (target and distractor), from the P3a component, which is mainly evoked by distractor events. The fMRI-constrained source model explained >99% of the variance of the scalp ERP for both components. The P3b was mainly produced by parietal and inferior temporal areas, whereas frontal areas and the insula contributed mainly to the P3a. This source model reveals that both higher visual and supramodal association areas contribute to the visual P3b and that the P3a has a strong frontal contribution, which is compatible with its more anterior distribution on the scalp. The results point to the involvement of distinct attentional subsystems in target and distractor processing.

Common neural substrates for visual working memory and attention

Humans are severely limited in their ability to memorize visual information over short periods of time. Selective attention has been implicated as a limiting factor. Here we used functional magnetic resonance imaging to test the hypothesis that this limitation is due to common neural resources shared by visual working memory (WM) and selective attention. We combined visual search and delayed discrimination of complex objects and independently modulated the demands on selective attention and WM encoding. Participants were presented with a search array and performed easy or difficult visual search in order to encode one or three complex objects into visual WM. Overlapping activation for attention-demanding visual search and WM encoding was observed in distributed posterior and frontal regions. In the right prefrontal cortex and bilateral insula blood oxygen-level-dependent activation additively increased with increased WM load and attentional demand. Conversely, several visual, parietal and premotor areas showed overlapping activation for the two task components and were severely reduced in their WM load response under the condition with high attentional demand. Regions in the left prefrontal cortex were selectively responsive to WM load. Areas selectively responsive to high attentional demand were found within the right prefrontal and bilateral occipital cortex. These results indicate that encoding into visual WM and visual selective attention require to a high degree access to common neural resources. We propose that competition for resources shared by visual attention and WM encoding can limit processing capabilities in distributed posterior brain regions.

Mental chronometry of working memory retrieval: a combined functional magnetic resonance imaging and event-related potentials approach

We used the combination of functional magnetic resonance imaging and event-related potentials to decompose the processing stages (mental chronometry) of working memory retrieval. Our results reveal an early transient activation of inferotemporal cortex, which was accompanied by the onset of a sustained activation of posterior parietal cortex. We furthermore observed late transient responses in ventrolateral prefrontal cortex and late sustained activity in medial frontal and premotor areas. We propose that these neural signatures reflect the cognitive stages of task processing, perceptual evaluation (inferotemporal cortex), storage buffer operations (posterior parietal cortex), active retrieval (ventrolateral prefrontal cortex), and action selection (medial frontal and premotor cortex). This is also supported by their differential temporal contribution to specific subcomponents of the P300 cognitive potential.

What “Works” in Working Memory? Separate Systems for Selection and Updating of Critical Information

Cognition depends critically on working memory, the active representation of a limited number of items over short periods of time. In addition to the maintenance of information during the course of cognitive processing, many tasks require that some of the items in working memory become transiently more important than others. Based on cognitive models of working memory, we hypothesized two complementary essential cognitive operations to achieve this: a selection operation that retrieves the most relevant item, and an updating operation that changes the focus of attention onto it. Using functional magnetic resonance imaging, high-resolution oculometry, and behavioral analysis, we demonstrate that these two operations are functionally and neuroanatomically dissociated. Updating the attentional focus elicited transient activation in the caudal superior frontal sulcus and posterior parietal cortex. In contrast, increasing demands on selection selectively modulated activation in rostral superior frontal sulcus and posterior cingulate/precuneus. We conclude that prioritizing one memory item over others invokes independent mechanisms of mnemonic retrieval and attentional focusing, each with its distinct neuroanatomical basis within frontal and parietal regions. These support the developing understanding of working memory as emerging from the interaction between memory and attentional systems.

The Timing of Feedback to Early Visual Cortex in the Perception of Long-Range Apparent Motion

When 2 visual stimuli are presented one after another in different locations, they are often perceived as one, but moving object. Feedback from area human motion complex hMT/V5+ to V1 has been hypothesized to play an important role in this illusory perception of motion. We measured event-related responses to illusory motion stimuli of varying apparent motion (AM) content and retinal location using Electroencephalography. Detectable cortical stimulus processing started around 60-ms poststimulus in area V1. This component was insensitive to AM content and sequential stimulus presentation. Sensitivity to AM content was observed starting around 90 ms post the second stimulus of a sequence and most likely originated in area hMT/V5+. This AM sensitive response was insensitive to retinal stimulus position. The stimulus sequence related response started to be sensitive to retinal stimulus position at a longer latency of 110 ms. We interpret our findings as evidence for feedback from area hMT/V5+ or a related motion processing area to early visual cortices (V1, V2, V3).

Visual target modulation of functional connectivity networks revealed by self-organizing group ICA

We applied a data‐driven analysis based on self‐organizing group independent component analysis (sogICA) to fMRI data from a three‐stimulus visual oddball task. SogICA is particularly suited to the investigation of the underlying functional connectivity and does not rely on a predefined model of the experiment, which overcomes some of the limitations of hypothesis‐driven analysis. Unlike most previous applications of ICA in functional imaging, our approach allows the analysis of the data at the group level, which is of particular interest in high order cognitive studies. SogICA is based on the hierarchical clustering of spatially similar independent components, derived from single subject decompositions. We identified four main clusters of components, centered on the posterior cingulate, bilateral insula, bilateral prefrontal cortex, and right posterior parietal and prefrontal cortex, consistently across all participants. Post hoc comparison of time courses revealed that insula, prefrontal cortex and right fronto‐parietal components showed higher activity for targets than for distractors. Activation for distractors was higher in the posterior cingulate cortex, where deactivation was observed for targets. While our results conform to previous neuroimaging studies, they also complement conventional results by showing functional connectivity networks with unique contributions to the task that were consistent across subjects. SogICA can thus be used to probe functional networks of active cognitive tasks at the group‐level and can provide additional insights to generate new hypotheses for further study. Hum Brain Mapp, 2008.

At Your Own Peril: An ERP Study of Voluntary Task Set Selection Processes in the Medial Frontal Cortex

A tool that is commonly used to investigate selection among different alternatives in a changing environment is the task-switching paradigm. Functional neuroimaging has pointed out a role for the posterior medial frontal cortex and the posterior parietal cortex in the voluntary selection of task sets. In the present study, we set out to investigate the temporal dynamics of these agency-related processes (in task choice vs. no-choice conditions) using event-related brain potentials (ERPs). The results revealed agency-related modulations of a series of ERP components, including (1) an early parieto-occipital activation, taken to reflect the evaluation of choice versus no choice; (2) a subsequent medial frontal expression of the voluntary selection between task sets; (3) a CNV-like sustained negativity in preparation for the target; (4) a target-induced N210—P210 complex, taken to reflect early sensory-perceptual processing; and (5) a target-induced P3, associated with the evaluation of the stimulus and its designated response vis-à-vis the chosen versus competing task sets. Together, these results indicate that the opportunity to choose between tasks invokes activity originating from the medial frontal cortex, associated with voluntary task set selection, but also activation at different time points in a number of other brain areas, not necessarily captured by functional neuroimaging.

Separable Neural Bases for Subprocesses of Recognition in Working Memory

Working memory supports the recognition of objects in the environment. Memory models have postulated that recognition relies on 2 processes: assessing the degree of similarity between an external stimulus and memory representations and testing the resulting summed-similarity value against a critical level for recognition. Here, we varied the similarity between samples held in working memory and a probe to investigate these 2 processes with magnetoencephalography. Two separable components matched our expectations: First, from 280 ms after probe onset, clearly nonmatching probes differed from both similar nonmatches and matches over left frontal cortex. At 350-400 ms, these signals evolved into a pattern of gradually increasing activation as a function of sample-probe similarity, as expected for a neural representation of summed similarity. Second, a signal potentially reflecting criterion testing was observed at 600-700 ms at right frontotemporal sensors that differentiated between matches and nonmatches without further differences between similar and dissimilar probes. Thus, analysis of the time course of recognition provided strong evidence that similarity summation and criterion testing have separable neural bases. As probably both working and long-term memory recognition draw on these processes, they may be involved in many domains of behavior.

Activity in Human Visual and Parietal Cortex Reveals Object-Based Attention in Working Memory

Visual attention enables observers to select behaviorally relevant information based on spatial locations, features, or objects. Attentional selection is not limited to physically present visual information, but can also operate on internal representations maintained in working memory (WM) in service of higher-order cognition. However, only little is known about whether attention to WM contents follows the same principles as attention to sensory stimuli. To address this question, we investigated in humans whether the typically observed effects of object-based attention in perception are also evident for object-based attentional selection of internal object representations in WM. In full accordance with effects in visual perception, the key behavioral and neuronal characteristics of object-based attention were observed in WM. Specifically, we found that reaction times were shorter when shifting attention to memory positions located on the currently attended object compared with equidistant positions on a different object. Furthermore, functional magnetic resonance imaging and multivariate pattern analysis of visuotopic activity in visual (areas V1–V4) and parietal cortex revealed that directing attention to one position of an object held in WM also enhanced brain activation for other positions on the same object, suggesting that attentional selection in WM activates the entire object. This study demonstrated that all characteristic features of object-based attention are present in WM and thus follows the same principles as in perception.

Superior Intraparietal Sulcus Controls the Variability of Visual Working Memory Precision

Limitations of working memory (WM) capacity depend strongly on the cognitive resources that are available for maintaining WM contents in an activated state. Increasing the number of items to be maintained in WM was shown to reduce the precision of WM and to increase the variability of WM precision over time. Although WM precision was recently associated with neural codes particularly in early sensory cortex, we have so far no understanding of the neural bases underlying the variability of WM precision, and how WM precision is preserved under high load. To fill this gap, we combined human fMRI with computational modeling of behavioral performance in a delayed color-estimation WM task. Behavioral results replicate a reduction of WM precision and an increase of precision variability under high loads (5 > 3 > 1 colors). Load-dependent BOLD signals in primary visual cortex (V1) and superior intraparietal sulcus (IPS), measured during the WM task at 2–4 s after sample onset, were modulated by individual differences in load-related changes in the variability of WM precision. Although stronger load-related BOLD increase in superior IPS was related to lower increases in precision variability, thus stabilizing WM performance, the reverse was observed for V1. Finally, the detrimental effect of load on behavioral precision and precision variability was accompanied by a load-related decline in the accuracy of decoding the memory stimuli (colors) from left superior IPS. We suggest that the superior IPS may contribute to stabilizing visual WM performance by reducing the variability of memory precision in the face of higher load. SIGNIFICANCE STATEMENT This study investigates the neural bases of capacity limitations in visual working memory by combining fMRI with cognitive modeling of behavioral performance, in human participants. It provides evidence that the superior intraparietal sulcus (IPS) is a critical brain region that influences the variability of visual working memory precision between and within individuals (Fougnie et al., 2012; van den Berg et al., 2012) under increased memory load, possibly in cooperation with perceptual systems of the occipital cortex. These findings substantially extend our understanding of the nature of capacity limitations in visual working memory and their neural bases. Our work underlines the importance of integrating cognitive modeling with univariate and multivariate methods in fMRI research, thus improving our knowledge of brain-behavior relationships.