Complex, multifocal, individual-specific attention-related cortical functional circuits

Recent studies focusing on the analysis of individual patterns of non-sensory-motor CNS activity may significantly alter our view of CNS functional mapping. We have recently provided evidence for highly variable attention-related Slow Potential (SP) generating cortical areas across individuals (Basile et al., 2003, 2006). In this work, we present new evidence, searching for other physiological indexes of attention by a new use of a well established method, for individual-specific sets of cortical areas active during expecting attention. We applied latency corrected peak averaging to oscillatory bursts, from 124-channel EEG recordings, and modeled their generators by current density reconstruction. We first computed event-related total power, and averaging was based on individual patterns of narrow task-induced band-power. This method is sensitive to activity out of synchrony with stimuli, and may detect task-related changes missed by regular Event-Related Potential (ERP) averaging. We additionally analyzed overall inter-electrode phase-coherence. The main results were (1) the detection of two bands of attention-induced beta range oscillations (around 25 and 21 Hz), whose scalp topography and current density cortical distribution were complex multi-focal, and highly variable across subjects, including prefrontal and posterior cortical areas. Most important, however, was the observation that (2) the generators of task-induced oscillations are largely the same individual-specific sets of cortical areas active during the resting, baseline state. We concluded that attention-related electrical cortical activity is highly individual-specific (significantly different from sensory-related visual evoked potentials or delta and theta induced band-power), and to a great extent already established during mere wakefulness. We discuss the critical implications of those results, in combination with other studies presenting individual data, to functional mapping: the need to abandon group averaging of task-related cortical activity and to revise studies on group averaged data, since the assumption of universal function to each cortical area appears deeply challenged. Clinical implications regard the interpretation of focal lesion consequences, functional reorganization, and neurosurgical planning.     

Individual Topographic Variability Is Inherent to Cortical Physiology but Task-Related Differences May Be Noise

The observation of highly variable sets of association neocortical areas across individuals, containing the estimated generators of Slow Potentials (SPs) and beta oscillations, lead to the persistence in individual analyses. This brought to notice an unexpected within individual topographic similarity between task conditions, despite our original interest in task-related differences. A recent related work explored the quantification of the similarity in beta topography between largely differing tasks. In this article, we used Independent Component Analysis (ICA) for the decomposition of beta activity from a visual attention task, and compared it with quiet resting, recorded by 128-channel EEG in 62 subjects. We statistically tested whether each ICA component obtained in one condition could be explained by a linear regression model based on the topographic patterns from the other condition, in each individual. Results were coherent with the previous report, showing a high topographic similarity between conditions. From an average of 12 beta component maps obtained for each task, over 80% were satisfactorily explained by the complementary task. Once more, the component maps including those considered unexplained, putatively “task-specific”, had their scalp distribution and estimated cortical sources highly variable across subjects. These findings are discussed along with other studies based on individual data and the present fMRI results, reinforcing the increasingly accepted view that individual variability in sets of active neocortical association areas is not noise, but intrinsic to cortical physiology. Actual ‘noise’, mainly stemming from group “brain averaging” and the emphasis on statistical differences as opposed to similarities, may explain the overall hardship in replication of the vast literature on supposed task-specific forms of activity, and the ever inconclusive status of a universal functional mapping of cortical association areas. A new hypothesis, that individuals may use the same idiosyncratic sets of areas, at least by their fraction of activity in the sub-delta and beta range, in various non-sensory-motor forms of conscious activities, is a corollary of the discussed variability.     

The mapping of brain biopotentials during the solving of a verbal task]

Reverse averaging of cortical potentials from the moment of the motor response followed the verbal task solving (anagram riddle) revealed some brain potentials correlations with the process of a decision making. In the case of task solving the negative frontal wave with the latency 900-400 ms from the motor response was recorded. Intracortical interaction mapping of this potential showed the regular patterns of cortical functional connections in different frequency ranges (alpha, beta). Successful solving of the task was characterized with predominant interaction foci topography in the frontal and left-temporal cortical areas in alpha band and parietal zones in beta. The absence of the task solution was characterized with the parieto-occipital interaction foci in alpha band and their frontal localization in beta.     

The Primary Visual Cortex Is Differentially Modulated by Stimulus-Driven and Top-Down Attention

Selective attention can be focused either volitionally, by top-down signals derived from task demands, or automatically, by bottom-up signals from salient stimuli. Because the brain mechanisms that underlie these two attention processes are poorly understood, we recorded local field potentials (LFPs) from primary visual cortical areas of cats as they performed stimulus-driven and anticipatory discrimination tasks. Consistent with our previous observations, in both tasks, we found enhanced beta activity, which we have postulated may serve as an attention carrier. We characterized the functional organization of task-related beta activity by (i) cortical responses (EPs) evoked by electrical stimulation of the optic chiasm and (ii) intracortical LFP correlations. During the anticipatory task, peripheral stimulation that was preceded by high-amplitude beta oscillations evoked large-amplitude EPs compared with EPs that followed low-amplitude beta. In contrast, during the stimulus-driven task, cortical EPs preceded by high-amplitude beta oscillations were, on average, smaller than those preceded by low-amplitude beta. Analysis of the correlations between the different recording sites revealed that beta activation maps were heterogeneous during the bottom-up task and homogeneous for the top-down task. We conclude that bottom-up attention activates cortical visual areas in a mosaic-like pattern, whereas top-down attentional modulation results in spatially homogeneous excitation.     

Selective disruption of one Cartesian axis of cortical maps and receptive fields by deficiency in ephrin-As and structured activity

The topographic representation of visual space is preserved from retina to thalamus to cortex. We have previously shown that precise mapping of thalamocortical projections requires both molecular cues and structured retinal activity. To probe the interaction between these two mechanisms, we studied mice deficient in both ephrin-As and retinal waves. Functional and anatomical cortical maps in these mice were nearly abolished along the nasotemporal (azimuth) axis of the visual space. Both the structure of single-cell receptive fields and large-scale topography were severely distorted. These results demonstrate that ephrin-As and structured neuronal activity are two distinct pathways that mediate map formation in the visual cortex and together account almost completely for the formation of the azimuth map. Despite the dramatic disruption of azimuthal topography, the dorsoventral (elevation) map was relatively normal, indicating that the two axes of the cortical map are organized by separate mechanisms.     

Changes in the EEG spectral power during perception of neutral and emotionally salient words in schizophrenic patients, their relatives and healthy individuals from the general population

To search for EEG-correlates of emotional processing that might be indicators of genetic predisposition to schizophrenia, changes in EEG spectral power during perception of neutral and emotionally salient words were examined in 36 schizophrenic patients, 50 of their unaffected first-degree relatives, and 47 healthy individuals without any family history of psychoses. In healthy persons, passive listening to neutral words induced minimum changes in cortical rhythmical activity, predominantly in the form of synchronization of slow and fast waves, whereas perception of emotional words was followed by a generalized depression of the alpha and beta1 activity and a locally specific decrease in the power of theta and beta2 frequency bands. The patients and their relatives showed a decrease in the alpha and beta1 activity simultaneously with an increase in the power of delta activity in response to both groups of words. Thus, in the patients and their relatives, reactions to neutral and emotional words were ulterior as a result of augmented reactions to the neutral words. These findings suggest that the EEG changes reflect familial and possibly hereditable abnormal involuntary attention. No prominent decrease in reactivity to emotional stimuli was revealed in schizophrenic families.     

Neuronal dynamics underlying high- and low-frequency EEG oscillations contribute independently to the human BOLD signal

Work on animals indicates that BOLD is preferentially sensitive to local field potentials, and that it correlates most strongly with gamma band neuronal synchronization. Here we investigate how the BOLD signal in humans performing a cognitive task is related to neuronal synchronization across different frequency bands. We simultaneously recorded EEG and BOLD while subjects engaged in a visual attention task known to induce sustained changes in neuronal synchronization across a wide range of frequencies. Trial-by-trial BOLD fluctuations correlated positively with trial-by-trial fluctuations in high-EEG gamma power (60-80 Hz) and negatively with alpha and beta power. Gamma power on the one hand, and alpha and beta power on the other hand, independently contributed to explaining BOLD variance. These results indicate that the BOLD-gamma coupling observed in animals can be extrapolated to humans performing a task and that neuronal dynamics underlying high- and low-frequency synchronization contribute independently to the BOLD signal.     

EEG Topographic Mapping of Visual and Kinesthetic Imagery in Swimmers

This study investigated differences in QEEG measures between kinesthetic and visual imagery of a 100-m swim in 36 elite competitive swimmers. Background information and post-trial checks controlled for the modality of imagery, swimming skill level, preferred imagery style, intensity of image and task equality. Measures of EEG relative magnitude in theta, low (7–9 Hz) and high alpha (8–10 Hz), and low and high beta were taken from 19 scalp sites during baseline, visual, and kinesthetic imagery. QEEG magnitudes in the low alpha band during the visual and kinesthetic conditions were attenuated from baseline in low band alpha but no changes were seen in any other bands. Swimmers produced more low alpha EEG magnitude during visual versus kinesthetic imagery. This was interpreted as the swimmers having a greater efficiency at producing visual imagery. Participants who reported a strong intensity versus a weaker feeling of the image (kinesthetic) had less low alpha magnitude, i.e., there was use of more cortical resources, but not for the visual condition. These data suggest that low band (7–9 Hz) alpha distinguishes imagery modalities from baseline, visual imagery requires less cortical resources than kinesthetic imagery, and that intense feelings of swimming requires more brain activity than less intense feelings.     

Effect of thyrotropin-releasing hormone (TRH) on EEG topography

EEG topography by a microcomputer system (ATAC-3700 Nihon-Kohden) was performed in the rabbit in order to investigate the mechanism of TRH action on the brain wave. Power spectral analysis was carried out using a fast Fourier transform algorithm. The square root of the power spectra was defined as the equivalent potential over each frequency band by Ueno & Matsuoka's method. Potential fields of EEG frequency band were printed out on the topographic maps. The potentials of the electrocortical delta and theta waves were high, while the potentials of the alpha, beta 1 and beta 2 waves were low. Stimulation of the nucleus ventralis anterior (VA) by 3 Hz and 8 Hz resulted in a decrease in these potentials, especially, those of the alpha, beta 1 and beta 2 waves. The potentials of the alpha and fast waves were increased following unilateral destruction of VA. In the rabbit, in which TRH 0.5 mg/kg had been administered beforehand, there was no decrease in the potential of each wave induced by stimulation of VA with frequencies of 3 Hz and 8 Hz. The findings suggest involvement of the diffuse thalamocortical projection system in the activation of EEG by TRH.     

Reflection of the Emotional Significance of Visual Stimuli in the Characteristics of Evoked EEG Potentials

Healthy subjects (n = 88) were asked to passively visualize positive and passive emotiogenic visual stimuli and also stimuli with a neutral emotional content. Images of the International Affective Picture System (IAPS) were used. Amplitude/time characteristics of the components of evoked EEG potentials (EPs), P1, N1, P2, N2, and P3 and topographic distribution of the latter components were analyzed. The latencies, amplitudes, and topography of the EP waves induced by presentation of positive and negative stimuli were found to be different from the respective values for the EPs induced by neutral stimuli. The level and pattern of these differences typical of different EP components were dissimilar and depended on the sign of the emotions. Specificities related to the valency of an identified stimulus were observed within nearly all stages of processing of visual signals, for the negative stimuli, beginning from an early stage of sensory analysis corresponding to the development of wave Р1. The latencies of components Р1 in the case of presentation of emotiogenic negative stimuli and those of components N1, N2, and Р3 in the case of presentation of the stimuli of both valencies were shorter than the latencies observed at neutral stimuli. The amplitude of component N2 at perception of positive stimuli was, on average, lower, while the Р3 amplitude at perception of all emotiogenic stimuli was higher than in the case of presentation of neutral stimuli. The time dynamics of topographic peculiarities of processing of emotiogenic information were complicated. Activation of the left hemisphere was observed during the earliest stages of perception, while the right hemisphere was activated within the intermediate stages. Generalized activation of the cortex after the action of negative signals and dominance of the left hemisphere under conditions of presentation of positive stimuli were observed only within the final stages. As is supposed, emotiogenic stimuli possess a greater biological significance than neutral ones, and this is why the former attract visual attention first; they more intensely activate the respective cortical zones, and the corresponding visual information is processed more rapidly. The observed effects were more clearly expressed in the case of action of negative stimuli; these effects involved more extensive cortical zones. These facts are indicative of the higher intensity of activating influences of negative emotiogenic stimuli on neutral systems of the higher CNS structures.     

Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor

Spontaneous activity patterns in the developing retina appear important for the functional organization of the visual system. We show here that an absence of early retinal waves in mice lacking the beta2 subunit of the nicotinic acetylcholine receptor (nAChR) is associated with both gain and loss of functional organization in the dorsal lateral geniculate nucleus (dLGN). Anatomical studies show normal gross retinotopy in the beta2(-/-) dLGN but suggest reduced topographic precision in the retinogeniculate projection. Physiological recordings reveal normal topography in the dorsoventral visual axis but a lack of fine-scale mapping in the nasotemporal visual plane. In contrast, unlike wild-type mice, on- and off-center cells in the beta2(-/-) dLGN are spatially segregated. The presence of the beta2 subunit of the nAChR in the CNS is therefore important for normal functional organization in the retinogeniculate projection.     

Changes in early cortical visual processing predict enhanced reactivity in deaf individuals

Individuals with profound deafness rely critically on vision to interact with their environment. Improvement of visual performance as a consequence of auditory deprivation is assumed to result from cross-modal changes occurring in late stages of visual processing. Here we measured reaction times and event-related potentials (ERPs) in profoundly deaf adults and hearing controls during a speeded visual detection task, to assess to what extent the enhanced reactivity of deaf individuals could reflect plastic changes in the early cortical processing of the stimulus. We found that deaf subjects were faster than hearing controls at detecting the visual targets, regardless of their location in the visual field (peripheral or peri-foveal). This behavioural facilitation was associated with ERP changes starting from the first detectable response in the striate cortex (C1 component) at about 80 ms after stimulus onset, and in the P1 complex (100-150 ms). In addition, we found that P1 peak amplitudes predicted the response times in deaf subjects, whereas in hearing individuals visual reactivity and ERP amplitudes correlated only at later stages of processing. These findings show that long-term auditory deprivation can profoundly alter visual processing from the earliest cortical stages. Furthermore, our results provide the first evidence of a co-variation between modified brain activity (cortical plasticity) and behavioural enhancement in this sensory-deprived population.     

Attention and eye movements in human: psychophysiological concepts, neurophysiological models and EEG correlates

A review. Recently published articles concerning the problem of attention are discussed, the most popular psychophysiological concepts and neurophysiological models of attention are described, and correlation of spatial attention and saccadic eyes movements is shown. The evidence for reflection of attention mechanisms and saccade preparation in intensity and topography of the visual evoked potentials and event-related potentials is given. On the basis of the results obtained by the authors and literature data, the contribution of attention to preparation of a saccade and its programming is shown. Different kinds of attention are reflected in a complex of EEG potentials of various duration and polarity. The analysis of parameters and topography of these potentials can serve a tool for investigation of the attention mechanisms.     

Changes in the spatial organization of the cortical electrical activity during formation and actualization of a cognitive set to facial expression

Coherence function of the EEG in the bands of 8-13 (alpha rhythm) and 14-25 Hz (beta rhythm) was analyzed in 35 healthy adult subjects during formation and testing of a visual cognitive set to pictures of faces with different emotional expressions. The intra- and interhemispheric coherences of the potentials in the frontal area and coherence between the right frontal and temporal derivation were shown to increase at the stage of set actualization. The results of the analysis confirm the suggestion that the frontal cortical areas are predominantly involved in formation and actualization of the set to facial emotional expression. The conclusion is based on the idea that the spatial synchronization of the brain electrical potentials is an index of the functional relations between the corresponding cortical areas and their cooperative involvement in a certain kind of activity (their simultaneous activation).     

Top-Down Beta Rhythms Support Selective Attention via Interlaminar Interaction: A Model

Cortical rhythms have been thought to play crucial roles in our cognitive abilities. Rhythmic activity in the beta frequency band, around 20 Hz, has been reported in recent studies that focused on neural correlates of attention, indicating that top-down beta rhythms, generated in higher cognitive areas and delivered to earlier sensory areas, can support attentional gain modulation. To elucidate functional roles of beta rhythms and underlying mechanisms, we built a computational model of sensory cortical areas. Our simulation results show that top-down beta rhythms can activate ascending synaptic projections from L5 to L4 and L2/3, responsible for biased competition in superficial layers. In the simulation, slow-inhibitory interneurons are shown to resonate to the 20 Hz input and modulate the activity in superficial layers in an attention-related manner. The predicted critical roles of these cells in attentional gain provide a potential mechanism by which cholinergic drive can support selective attention.     

Mental Fatigue Affects Visual Selective Attention

Mental fatigue is a form of fatigue, induced by continuous task performance. Mentally fatigued people often report having a hard time keeping their attention focussed and being easily distracted. In this study, we examined the relation between mental fatigue, as induced by time on task, and attention-related changes in event-related potentials (ERPs). EEG, reaction times and response accuracies were obtained from 17 healthy volunteers during two hours of task performance on an adapted Eriksen flanker task. In this task, the size of targets and flankers was manipulated to discern neuronal processes that are related to processing of relevant information from processes related to the processing of irrelevant information. The ERP data showed that effects induced by target size manipulation were not affected by time on task, while an initial effect of flanker size manipulation decreased gradually with increasing time on task. We conclude that attention was affected by mental fatigue, in the form of a decrease in the ability to suppress irrelevant information. In behavioural results, this was reflected by a tendency of participants to increasingly base their response decision on irrelevant information, resulting in decreased response accuracies.     

Cell-type-specific synchronization of neural activity in FEF with V4 during attention

Shifts of gaze and shifts of attention are closely linked and it is debated whether they result from the same neural mechanisms. Both processes involve the frontal eye fields (FEF), an area which is also a source of top-down feedback to area V4 during covert attention. To test the relative contributions of oculomotor and attention-related FEF signals to such feedback, we recorded simultaneously from both areas in a covert attention task and in a saccade task. In the attention task, only visual and visuomovement FEF neurons showed enhanced responses, whereas movement cells were unchanged. Importantly, visual, but not movement or visuomovement cells, showed enhanced gamma frequency synchronization with activity in V4 during attention. Within FEF, beta synchronization was increased for movement cells during attention but was suppressed in the saccade task. These findings support the idea that the attentional modulation of visual processing is not mediated by movement neurons.     

Cholinergic enhancement of visual attention and neural oscillations in the human brain

Cognitive processes such as visual perception and selective attention induce specific patterns of brain oscillations. The neurochemical bases of these spectral changes in neural activity are largely unknown, but neuromodulators are thought to regulate processing. The cholinergic system is linked to attentional function in vivo, whereas separate in vitro studies show that cholinergic agonists induce high-frequency oscillations in slice preparations. This has led to theoretical proposals that cholinergic enhancement of visual attention might operate via gamma oscillations in visual cortex, although low-frequency alpha/beta modulation may also play a key role. Here we used MEG to record cortical oscillations in the context of administration of a cholinergic agonist (physostigmine) during a spatial visual attention task in humans. This cholinergic agonist enhanced spatial attention effects on low-frequency alpha/beta oscillations in visual cortex, an effect correlating with a drug-induced speeding of performance. By contrast, the cholinergic agonist did not alter high-frequency gamma oscillations in visual cortex. Thus, our findings show that cholinergic neuromodulation enhances attentional selection via an impact on oscillatory synchrony in visual cortex, for low rather than high frequencies. We discuss this dissociation between high- and low-frequency oscillations in relation to proposals that lower-frequency oscillations are generated by feedback pathways within visual cortex.     

Changes in visual receptive fields with microstimulation of frontal cortex

The influence of attention on visual cortical neurons has been described in terms of its effect on the structure of receptive fields (RFs), where multiple stimuli compete to drive neural responses and ultimately behavior. We stimulated the frontal eye field (FEF) of passively fixating monkeys and produced changes in V4 responses similar to known effects of voluntary attention. Subthreshold FEF stimulation enhanced visual responses at particular locations within the RF and altered the interaction between pairs of RF stimuli to favor those aligned with the activated FEF site. Thus, we could influence which stimulus drove the responses of individual V4 neurons. These results suggest that spatial signals involved in saccade preparation are used to covertly select among multiple stimuli appearing within the RFs of visual cortical neurons.