Feature-based attention in the frontal eye field and area V4 during visual search

When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target.     

Interacting roles of attention and visual salience in V4

Attention increases the contrast gain of V4 neurons, causing them to respond to an attended stimulus as though its contrast had increased. When multiple stimuli appear within a neuron's receptive field (RF), the neuron responds primarily to the attended stimulus. This suggests that cortical cells may be "hard wired" to respond preferentially to the highest-contrast stimulus in their RF, and neural systems for attention capitalize on this mechanism by dynamically increasing the effective contrast of the stimulus that is task relevant. To test this, we varied the relative contrast of two stimuli within the recorded neurons' RFs, while the monkeys attended away to another location. Increasing the physical contrast of one stimulus caused V4 neurons to respond preferentially to that stimulus and reduced their responses to competing stimuli. When attention was directed to the lower-contrast stimulus, it partially overcame the influence of a competing, higher-contrast stimulus.     

Information quantification of empirical mode decomposition and applications to field potentials

The empirical mode decomposition (EMD) method can adaptively decompose a non-stationary time series into a number of amplitude or frequency modulated functions known as intrinsic mode functions. This paper combines the EMD method with information analysis and presents a framework of information-preserving EMD. The enhanced EMD method has been exploited in the analysis of neural recordings. It decomposes a signal and extracts only the most informative oscillations contained in the non-stationary signal. Information analysis has shown that the extracted components retain the information content of the signal. More importantly, a limited number of components reveal the main oscillations presented in the signal and their instantaneous frequencies, which are not often obvious from the original signal. This information-coupled EMD method has been tested on several field potential datasets for the analysis of stimulus coding in visual cortex, from single and multiple channels, and for finding information connectivity among channels. The results demonstrate the usefulness of the method in extracting relevant responses from the recorded signals. An investigation is also conducted on utilizing the Hilbert phase for cases where phase information can further improve information analysis and stimulus discrimination. The components of the proposed method have been integrated into a toolbox and the initial implementation is also described.     

Functionally independent components of early event-related potentials in a visual spatial attention task.

Spatial visual attention modulates the first negative-going deflection in the human averaged event-related potential (ERP) in response to visual target and non-target stimuli (the N1 complex). Here we demonstrate a decomposition of N1 into functionally independent subcomponents with functionally distinct relations to task and stimulus conditions. ERPs were collected from 20 subjects in response to visual target and non-target stimuli presented at five attended and non-attended screen locations. Independent component analysis, a new method for blind source separation, was trained simultaneously on 500 ms grand average responses from all 25 stimulus-attention conditions and decomposed the non-target N1 complexes into five spatially fixed, temporally independent and physiologically plausible components. Activity of an early, laterally symmetrical component pair (N1aR and N1aL) was evoked by the left and right visual field stimuli, respectively. Component N1aR peaked ca. 9 ms earlier than N1aL. Central stimuli evoked both components with the same peak latency difference, producing a bilateral scalp distribution. The amplitudes of these components were no reliably augmented by spatial attention. Stimuli in the right visual field evoked activity in a spatio-temporally overlapping bilateral component (N1b) that peaked at ca. 180 ms and was strongly enhanced by attention. Stimuli presented at unattended locations evoked a fourth component (P2a) peaking near 240 ms. A fifth component (P3f) was evoked only by targets presented in either visual field. The distinct response patterns of these components across the array of stimulus and attention conditions suggest that they reflect activity in functionally independent brain systems involved in processing attended and unattended visuospatial events.     

Differential attention-dependent response modulation across cell classes in macaque visual area V4

The cortex contains multiple cell types, but studies of attention have not distinguished between them, limiting understanding of the local circuits that transform attentional feedback into improved visual processing. Parvalbumin-expressing inhibitory interneurons can be distinguished from pyramidal neurons based on their briefer action potential durations. We recorded neurons in area V4 as monkeys performed an attention-demanding task. We find that the distribution of action potential durations is strongly bimodal. Neurons with narrow action potentials have higher firing rates and larger attention-dependent increases in absolute firing rate than neurons with broad action potentials. The percentage increase in response is similar across the two classes. We also find evidence that attention increases the reliability of the neuronal response. This modulation is more than two-fold stronger among putative interneurons. These findings lead to the surprising conclusion that the strongest attentional modulation occurs among local interneurons that do not transmit signals between areas.     

Time course of attention reveals different mechanisms for spatial and feature-based attention in area V4

Attention can facilitate visual processing, emphasizing specific locations and highlighting stimuli containing specific features. To dissociate the mechanisms of spatial and feature-based attention, we compared the time course of visually evoked responses under different attention conditions. We recorded from single neurons in area V4 during a delayed match-to-sample task that controlled both spatial and feature-based attention. Neuronal responses increased when spatial attention was directed toward the receptive field and were modulated by the identity of the target of feature-based attention. Modulation by spatial attention was weaker during the early portion of the visual response and stronger during the later portion of the response. In contrast, modulation by feature-based attention was relatively constant throughout the response. It appears that stimulus onset transients disrupt spatial attention, but not feature attention. We conclude that spatial attention reflects a combination of stimulus-driven and goal-driven processes, while feature-based attention is purely goal driven.     

The role of attention in figure-ground segregation in areas V1 and V4 of the visual cortex

Our visual system segments images into objects and background. Figure-ground segregation relies on the detection of feature discontinuities that signal boundaries between the figures and the background and on a complementary region-filling process that groups together image regions with similar features. The neuronal mechanisms for these processes are not well understood and it is unknown how they depend on visual attention. We measured neuronal activity in V1 and V4 in a task where monkeys either made an eye movement to texture-defined figures or ignored them. V1 activity predicted the timing and the direction of the saccade if the figures were task relevant. We found that boundary detection is an early process that depends little on attention, whereas region filling occurs later and is facilitated by visual attention, which acts in an object-based manner. Our findings are explained by a model with local, bottom-up computations for boundary detection and feedback processing for region filling.     

Neurons in area V4 of the macaque translate attended visual features into behaviorally relevant categories

Neural processing at most stages of the primate visual system is modulated by selective attention, such that behaviorally relevant information is emphasized at the expenses of irrelevant, potentially distracting information. The form of attention best understood at the cellular level is when stimuli at a given location in the visual field must be selected (space-based attention). In contrast, fewer single-unit recording studies have so far explored the cellular mechanisms of attention operating on individual stimulus features, specifically when one feature (e.g., color) of an object must guide behavioral responses while a second feature (e.g., shape) of the same object is potentially interfering and therefore must be ignored. Here we show that activity of neurons in macaque area V4 can underlie the selection of elemental object features and their "translation" into a categorical format that can directly contribute to the control of the animal's behavior.     

The effect of selective attention on pattern-specific visual evoked potentials

In a complex choice reaction time experiment, patterned stimuli without luminance change were presented, and pattern-specific visual evoked potentials to lower half-field stimulation were recorded. Two experimental conditions were used. The first was the between-field selection, where square patterns were presented in either the lower or the upper half of the visual field. In a given stimulus run one of the half-fields was task-relevant, and the subjects' task was to press a microswitch to stimuli of higher duration value (GO stimuli), while they had to ignore shorter ones, i. e. stimuli of lower apparent spatial contrast (NOGO stimuli). They had to ignore the stimuli appearing in the irrelevant half-field (IRR stimuli). In order to ensure proper fixation, the subjects had to press another microswitch at the onset of a dim light at the fixation point (CRT stimuli). Our second experimental condition was the within-field selection, where the GO, NOGO, and IRR stimuli appeared in the lower half of the visual field. GO and NOGO were square patterns while IRR stimuli were constructed of circles, or vice versa. (The CRT stimuli were the same as in the previous condition.) Three pattern-specific visual evoked potential components were identified, i. e. CI (70 ms latency), CII (100 ms latency), and CIII (170 ms latency). There were marked selective attention effects on both the CI-CII and CII-CIII peak-to-peak amplitudes. In both experimental conditions, responses with the highest amplitude were evoked by the GO type of stimuli, while the IRR stimuli evoked the smallest responses. According to these results, attention effects on the pattern-specific visual evoked potentials in the first 200 ms cannot be attributed to a simple stimulus set kind of selection.     

Object selectivity of local field potentials and spikes in the macaque inferior temporal cortex

Local field potentials (LFPs) arise largely from dendritic activity over large brain regions and thus provide a measure of the input to and local processing within an area. We characterized LFPs and their relationship to spikes (multi and single unit) in monkey inferior temporal cortex (IT). LFP responses in IT to complex objects showed strong selectivity at 44% of the sites and tolerance to retinal position and size. The LFP preferences were poorly predicted by the spike preferences at the same site but were better explained by averaging spikes within approximately 3 mm. A comparison of separate sites suggests that selectivity is similar on a scale of approximately 800 microm for spikes and approximately 5 mm for LFPs. These observations imply that inputs to IT neurons convey selectivity for complex shapes and that such input may have an underlying organization spanning several millimeters.     

Evaluation of local field potential signals in decoding of visual attention

In the field of brain research, attention as one of the main issues in cognitive neuroscience is an important mechanism to be studied. The complicated structure of the brain cannot process all the information it receives at any moment. Attention, in fact, is considered as a possible useful mechanism in which brain concentrates on the processing of important information which is required at any certain moment. The main goal of this study is decoding the location of visual attention from local field potential signals recorded from medial temporal (MT) area of a macaque monkey. To this end, feature extraction and feature selection are applied in both the time and the frequency domains. After applying feature extraction methods such as the short time Fourier transform, continuous wavelet transform (CWT), and wavelet energy (scalogram), feature selection methods are evaluated. Feature selection methods used here are T-test, Entropy, receiver operating characteristic, and Bhattacharyya. Subsequently, different classifiers are utilized in order to decode the location of visual attention. At last, the performances of the employed classifiers are compared. The results show that the maximum information about the visual attention in area MT exists in the low frequency features. Interestingly, low frequency features over all the time-axis and all of the frequency features at the initial time interval in the spectrogram domain contain the most valuable information related to the decoding of spatial attention. In the CWT and scalogram domains, this information exists in the low frequency features at the initial time interval. Furthermore, high performances are obtained for these features in both the time and the frequency domains. Among different employed classifiers, the best achieved performance which is about 84.5 % belongs to the K-nearest neighbor classifier combined with the T-test method for feature selection in the time domain. Additionally, the best achieved result (82.9 %) is related to the spectrogram with the least number of selected features as large as 200 features using the T-test method and SVM classifier in the time−frequency domain.     

Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory

We compared behavioral and neural effects of cholinergic enhancement between spatial attention, spatial working memory (WM), and visual control tasks, using fMRI and the anticholinesterase physostigmine. Physostigmine speeded responses nonselectively but increased accuracy selectively for attention. Physostigmine also decreased activations to visual stimulation across all tasks within primary visual cortex, increased extrastriate occipital cortex activation selectively during maintained attention and WM encoding, and decreased parietal activation selectively during maintained attention. Finally, lateralization of occipital activation as a function of the visual hemifield toward which attention or memory was directed was decreased under physostigmine. In the case of attention, this effect correlated strongly with a decrease in a behavioral measure of selective spatial processing. Our results suggest that, while cholinergic enhancement facilitates visual attention by increasing activity in extrastriate cortex generally, it accomplishes this in a manner that reduces expectation-driven selective biasing of extrastriate cortex.     

Selective attention and memory: evoked potentials in visual and auditory verbal competition

The brain mechanisms of the selective verbal attention were studied using evoked potential (EP) technique. It was shown that the late "cognitive" EP components (400-800 ms) related to memory function were more positive to the words presented via a relevant sensory channel and more negative to irrelevant words. The hypothesis is advanced that words delivered via two competing sensory channels, such as visual and auditory, are perceived, i.e., the subject sees and hears them. However, irrelevant signals are not stored in episodic memory due to the active inhibition of the information transmission to the hippocampal structures.     

Spatiotopic coding of BOLD signal in human visual cortex depends on spatial attention

The neural substrate of the phenomenological experience of a stable visual world remains obscure. One possible mechanism would be to construct spatiotopic neural maps where the response is selective to the position of the stimulus in external space, rather than to retinal eccentricities, but evidence for these maps has been inconsistent. Here we show, with fMRI, that when human subjects perform concomitantly a demanding attentive task on stimuli displayed at the fovea, BOLD responses evoked by moving stimuli irrelevant to the task were mostly tuned in retinotopic coordinates. However, under more unconstrained conditions, where subjects could attend easily to the motion stimuli, BOLD responses were tuned not in retinal but in external coordinates (spatiotopic selectivity) in many visual areas, including MT, MST, LO and V6, agreeing with our previous fMRI study. These results indicate that spatial attention may play an important role in mediating spatiotopic selectivity.     

Manifestations of selective visual attention in human parietal and temporal cortex according to evoked potentials

The event-related potentials (ERPs) in visual discrimination task in parietal and temporal cortical areas were recorded in 11 young adults during passive observation (involuntary attention) and target selection (voluntary attention). The voluntary selective attention resulted in: 1) increased ERP correlation between the parietal; and temporal cortical areas; 2) increased correlation of sequential ERPs in monopolar leads (P3, P4, T3, T4, T5, T6); and 3) increased correlation of sequential ERPs in bipolar leads (P3-T3, P3-T5, P4-T4, P4-T6). The findings suggest that voluntary attention maintains a concordant activity of the parietal and temporal cortical areas in execution of visual selection tasks.     

Directed attention influence on the human brain potentials under conditions of probability visual stimulation

Saccadic latency and averaged EEG-potentials connected with switching on of the set and cue visual stimuli were examined in 12 right-handed healthy subjects in M. Posner's "cost-benefit" experimental paradigm. It was shown that attention was reflected in parameters of positive potential P100 evoked by switching on of set and cue stimuli and P300 and slow positive wave PMP1 evoked by switching on of the set stimulus in the relevant conditions. The spatiotemporal pattern of P100 probably reflects the involvement of the frontoparietal network of spacial attention in the perception of a relevant stimulus. Prevalence of the P300 and PMP1 potentials in the right parietal cortex suggests that these potentials reflect processes of space attention and visual fixation. Late positive potentials in a 600-900-ms interval after switching on of the set stimulus were found. Their amplitude was higher in backward averaging and they were predominantly localized in the left frontal cortex. These findings suggest that the late potentials reflect the anticipation and motor attention processes.     

Active vision and visual activation in area V4

During normal vision, the focus of gaze continually jumps from one important image feature to the next. In this issue of Neuron, Mazer and Gallant analyze neural activity in higher-level visual cortex during this kind of active visual exploration, and they demonstrate a localized enhancement of visual responses that predicts the target of the upcoming eye movement.