Timing and Sequence of Brain Activity in Top-Down Control of Visual-Spatial Attention

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Abstract
Recent brain imaging studies using functional magnetic resonance imaging (fMRI) have implicated a frontal-parietal network in the top-down control of attention. However, little is known about the timing and sequence of activations within this network. To investigate these timing questions, we used event-related electrical brain potentials (ERPs) and a specially designed visual-spatial attentional-cueing paradigm, which were applied as part of a multi-methodological approach that included a closely corresponding event-related fMRI study using an identical paradigm. In the first 400 ms post cue, attention-directing and control cues elicited similar general cue-processing activity, corresponding to the more lateral subregions of the frontal-parietal network identified with the fMRI. Following this, the attention-directing cues elicited a sustained negative-polarity brain wave that was absent for control cues. This activity could be linked to the more medial frontal–parietal subregions similarly identified in the fMRI as specifically involved in attentional orienting. Critically, both the scalp ERPs and the fMRI-seeded source modeling for this orienting-related activity indicated an earlier onset of frontal versus parietal contribution (∼400 versus ∼700 ms). This was then followed (∼800–900 ms) by pretarget biasing activity in the region-specific visual-sensory occipital cortex. These results indicate an activation sequence of key components of the attentional-control brain network, providing insight into their functional roles. More specifically, these results suggest that voluntary attentional orienting is initiated by medial portions of frontal cortex, which then recruit medial parietal areas. Together, these areas then implement biasing of region-specific visual-sensory cortex to facilitate the processing of upcoming visual stimuli. Attention is a fundamental cognitive function that allows us to focus neural resources on events or information in our environment that are most important or interesting to us at any given moment. Recent functional neuroimaging studies have indicated that a network of brain areas in frontal and parietal cortex is involved in directing our attention to specific locations in our visual field. However, little is known about the timing and sequence of activations within the various parts of this attentional control network, thus limiting our understanding of their functional roles. We extracted a more precise picture of the neural mechanisms of attentional control by combining two complementary methods of measuring cognitive brain activity: functional magnetic resonance imaging (fMRI) and electroencephalography (EEG). fMRI offers information on a millimeter scale about the locations of brain activity, whereas EEG offers temporal information on a scale of milliseconds. Our results indicate that visual-spatial attentional control is initiated in frontal brain areas, joined shortly afterwards by parietal involvement. Together, these brain areas then prepare relevant areas in the visual cortex for performing enhanced processing of visual input in the attended region of space.