Dynamic changes in phase-amplitude coupling facilitate spatial attention control in fronto-parietal cortex.

Attention is a core cognitive mechanism that allows the brain to allocate limited resources depending on current task demands. A number of frontal and posterior parietal cortical areas, referred to collectively as the fronto-parietal attentional control network, are engaged during attentional allocation in both humans and non-human primates. Numerous studies have examined this network in the human brain using various neuroimaging and scalp electrophysiological techniques. However, little is known about how these frontal and parietal areas interact dynamically to produce behavior on a fine temporal (sub-second) and spatial (sub-centimeter) scale. We addressed how human fronto-parietal regions control visuospatial attention on a fine spatiotemporal scale by recording electrocorticography (ECoG) signals measured directly from subdural electrode arrays that were implanted in patients undergoing intracranial monitoring for localization of epileptic foci. Subjects (n = 8) performed a spatial-cuing task, in which they allocated visuospatial attention to either the right or left visual field and detected the appearance of a target. We found increases in high gamma (HG) power (70-250 Hz) time-locked to trial onset that remained elevated throughout the attentional allocation period over frontal, parietal, and visual areas. These HG power increases were modulated by the phase of the ongoing delta/theta (2-5 Hz) oscillation during attentional allocation. Critically, we found that the strength of this delta/theta phase-HG amplitude coupling predicted reaction times to detected targets on a trial-by-trial basis. These results highlight the role of delta/theta phase-HG amplitude coupling as a mechanism for sub-second facilitation and coordination within human fronto-parietal cortex that is guided by momentary attentional demands.

Functional and structural architecture of the human dorsal frontoparietal attention network.

The dorsal frontoparietal attention network has been subdivided into at least eight areas in humans. However, the circuitry linking these areas and the functions of different circuit paths remain unclear. Using a combination of neuroimaging techniques to map spatial representations in frontoparietal areas, their functional interactions, and structural connections, we demonstrate different pathways across human dorsal frontoparietal cortex for the control of spatial attention. Our results are consistent with these pathways computing object-centered and/or viewer-centered representations of attentional priorities depending on task requirements. Our findings provide an organizing principle for the frontoparietal attention network, where distinct pathways between frontal and parietal regions contribute to multiple spatial representations, enabling flexible selection of behaviorally relevant information.

Shifting attentional priorities: control of spatial attention through hemispheric competition.

Regions of frontal and posterior parietal cortex are known to control the allocation of spatial attention across the visual field. However, the neural mechanisms underlying attentional control in the intact human brain remain unclear, with some studies supporting a hemispatial theory emphasizing a dominant function of the right hemisphere and others supporting an interhemispheric competition theory. We previously found neural evidence to support the latter account, in which topographically organized frontoparietal areas each generate a spatial bias, or "attentional weight," toward the contralateral hemifield, with the sum of the weights constituting the overall bias that can be exerted across visual space. Here, we used a multimodal approach consisting of functional magnetic resonance imaging (fMRI) of spatial attention signals, behavioral measures of spatial bias, and fMRI-guided single-pulse transcranial magnetic stimulation (TMS) to causally test this interhemispheric competition account. Across the group of fMRI subjects, we found substantial individual differences in the strengths of the frontoparietal attentional weights in each hemisphere, which predicted subjects' respective behavioral preferences when allocating spatial attention, as measured by a landmark task. Using TMS to interfere with attentional processing within specific topographic frontoparietal areas, we then demonstrated that the attentional weights of individual subjects, and thus their spatial attention behavior, could be predictably shifted toward one visual field or the other, depending on the site of interference. The results of our multimodal approach, combined with an emphasis on neural and behavioral individual differences, provide compelling evidence that spatial attention is controlled through competitive interactions between hemispheres rather than a dominant right hemisphere in the intact human brain.

Periodic attention deficits after frontoparietal lesions provide causal evidence for rhythmic attentional sampling.

Contemporary models conceptualize spatial attention as a blinking spotlight that sequentially samples visual space. Hence, behavior fluctuates over time, even in states of presumed "sustained" attention. Recent evidence has suggested that rhythmic neural activity in the frontoparietal network constitutes the functional basis of rhythmic attentional sampling. However, causal evidence to support this notion remains absent. Using a lateralized spatial attention task, we addressed this issue in patients with focal lesions in the frontoparietal attention network. Our results revealed that frontoparietal lesions introduce periodic attention deficits, i.e., temporally specific behavioral deficits that are aligned with the underlying neural oscillations. Attention-guided perceptual sensitivity was on par with that of healthy controls during optimal phases but was attenuated during the less excitable sub-cycles. Theta-dependent sampling (3-8 Hz) was causally dependent on the prefrontal cortex, while high-alpha/low-beta sampling (8-14 Hz) emerged from parietal areas. Collectively, our findings reveal that lesion-induced high-amplitude, low-frequency brain activity is not epiphenomenal but has immediate behavioral consequences. More generally, these results provide causal evidence for the hypothesis that the functional architecture of attention is inherently rhythmic.

Mechanisms of spatial attention control in frontal and parietal cortex.

Theories of spatial attentional control have been largely based upon studies of patients suffering from visuospatial neglect, resulting from circumscribed lesions of frontal and posterior parietal cortex. In the intact brain, the control of spatial attention has been related to a distributed frontoparietal attention network. Little is known about the nature of the control mechanisms exerted by this network. Here, we used a novel region-of-interest approach to relate activations of the attention network to recently described topographic areas in frontal cortex [frontal eye field (FEF), PreCC/IFS (precentral cortex/inferior frontal sulcus)] and parietal cortex [intraparietal sulcus areas (IPS1-IPS5) and an area in the superior parietal lobule (SPL1)] to examine their spatial attention signals. We found that attention signals in most topographic areas were spatially specific, with stronger responses when attention was directed to the contralateral than to the ipsilateral visual field. Importantly, two hemispheric asymmetries were found. First, a region in only right, but not left SPL1 carried spatial attention signals. Second, left FEF and left posterior parietal cortex (IPS1/2) generated stronger contralateral biasing signals than their counterparts in the right hemisphere. These findings are the first to characterize spatial attention signals in topographic frontal and parietal cortex and provide a neural basis in support of an interhemispheric competition account of spatial attentional control.

Neural Mechanisms of Sustained Attention Are Rhythmic.

Classic models of attention suggest that sustained neural firing constitutes a neural correlate of sustained attention. However, recent evidence indicates that behavioral performance fluctuates over time, exhibiting temporal dynamics that closely resemble the spectral features of ongoing, oscillatory brain activity. Therefore, it has been proposed that periodic neuronal excitability fluctuations might shape attentional allocation and overt behavior. However, empirical evidence to support this notion is sparse. Here, we address this issue by examining data from large-scale subdural recordings, using two different attention tasks that track perceptual ability at high temporal resolution. Our results reveal that perceptual outcome varies as a function of the theta phase even in states of sustained spatial attention. These effects were robust at the single-subject level, suggesting that rhythmic perceptual sampling is an inherent property of the frontoparietal attention network. Collectively, these findings support the notion that the functional architecture of top-down attention is intrinsically rhythmic.

Insights into human behavior from lesions to the prefrontal cortex.

The prefrontal cortex (PFC), a cortical region that was once thought to be functionally insignificant, is now known to play an essential role in the organization and control of goal-directed thought and behavior. Neuroimaging, neurophysiological, and modeling techniques have led to tremendous advances in our understanding of PFC functions over the last few decades. It should be noted, however, that neurological, neuropathological, and neuropsychological studies have contributed some of the most essential, historical, and often prescient conclusions regarding the functions of this region. Importantly, examination of patients with brain damage allows one to draw conclusions about whether a brain area is necessary for a particular function. Here, we provide a broad overview of PFC functions based on behavioral and neural changes resulting from damage to PFC in both human patients and nonhuman primates.

Human fronto-parietal and parieto-hippocampal pathways represent behavioral priorities in multiple spatial reference frames.

We represent behaviorally relevant information in different spatial reference frames in order to interact effectively with our environment. For example, we need an egocentric (e.g., body-centered) reference frame to specify limb movements and an allocentric (e.g., world-centered) reference frame to navigate from one location to another. Posterior parietal cortex (PPC) is vital for performing transformations between these different coordinate systems. Here, we review evidence for multiple pathways in the human brain, from PPC to motor, premotor, and supplementary motor areas, as well as to structures in the medial temporal lobe. These connections are important for transformations between egocentric reference frames to facilitate sensory-guided action, or from egocentric to allocentric reference frames to facilitate spatial navigation.

Transcranial magnetic stimulation studies of visuospatial attentional control.

Transcranial magnetic stimulation (TMS) is an established technique in cognitive neuroscience which is used to interrupt processing in the brain, creating a brief 'virtual lesion'. Here, we review recent studies that have employed TMS to gain insight into the roles of frontal and parietal cortex in visuospatial attention control.

Topographic maps in human frontal cortex revealed in memory-guided saccade and spatial working-memory tasks.

We used fMRI at 3 Tesla and improved spatial resolution (2 x 2 x 2 mm(3)) to investigate topographic organization in human frontal cortex using memory-guided response tasks performed at 8 or 12 peripheral locations arranged clockwise around a central fixation point. The tasks required the location of a peripheral target to be remembered for several seconds after which the subjects either made a saccade to the remembered location (memory-guided saccade task) or judged whether a test stimulus appeared in the same or a slightly different location by button press (spatial working-memory task). With these tasks, we found two topographic maps in each hemisphere, one in the superior branch of precentral cortex and caudalmost part of the superior frontal sulcus, in the region of the human frontal eye field, and a second in the inferior branch of precentral cortex and caudalmost part of the inferior frontal sulcus, both of which greatly overlapped with activations evoked by visually guided saccades. In each map, activated voxels coded for saccade directions and memorized locations predominantly in the contralateral hemifield with neighboring saccade directions and memorized locations represented in adjacent locations of the map. Particular saccade directions or memorized locations were often represented in multiple locations of the map. The topographic activation patterns showed individual variability from subject to subject but were reproducible within subjects. Notably, only saccade-related activation, but no topographic organization, was found in the region of the human supplementary eye field in dorsomedial prefrontal cortex. Together these results show that topographic organization can be revealed outside sensory cortical areas using more complex behavioral tasks.