Elsevier

NeuroImage

Volume 65, 15 January 2013, Pages 395-407
NeuroImage

Oscillatory alpha-band suppression mechanisms during the rapid attentional shifts required to perform an anti-saccade task

https://doi.org/10.1016/j.neuroimage.2012.09.061Get rights and content

Abstract

Neuroimaging has demonstrated anatomical overlap between covert and overt attention systems, although behavioral and electrophysiological studies have suggested that the two systems do not rely on entirely identical circuits or mechanisms. In a parallel line of research, topographically-specific modulations of alpha-band power (~ 8–14 Hz) have been consistently correlated with anticipatory states during tasks requiring covert attention shifts. These tasks, however, typically employ cue–target-interval paradigms where attentional processes are examined across relatively protracted periods of time and not at the rapid timescales implicated during overt attention tasks. The anti-saccade task, where one must first covertly attend for a peripheral target, before executing a rapid overt attention shift (i.e. a saccade) to the opposite side of space, is particularly well-suited for examining the rapid dynamics of overt attentional deployments. Here, we asked whether alpha-band oscillatory mechanisms would also be associated with these very rapid overt shifts, potentially representing a common neural mechanism across overt and covert attention systems. High-density electroencephalography in conjunction with infra-red eye-tracking was recorded while participants engaged in both pro- and anti-saccade task blocks. Alpha power, time-locked to saccade onset, showed three distinct phases of significantly lateralized topographic shifts, all occurring within a period of less than 1 s, closely reflecting the temporal dynamics of anti-saccade performance. Only two such phases were observed during the pro-saccade task. These data point to substantially more rapid temporal dynamics of alpha-band suppressive mechanisms than previously established, and implicate oscillatory alpha-band activity as a common mechanism across both overt and covert attentional deployments.

Highlights

► Alpha-band oscillatory mechanism was evoked in covert and overt attentional tasks. ► Alpha-band dynamics lateralize across hemiscalp more rapidly than established. ► Provide evidence of shared mechanisms of attention across overt and covert paradigms

Introduction

Effective interaction with a complex environment often involves rapid focusing of limited cognitive resources on locations, objects or other information sources of interest. Humans accomplish this using both ‘overt’ and ‘covert’ attention systems (Helmholtz, 1910/1924). Overt attention refers to explicit engagement of a motor system to bring an object of interest into attentional focus, such as pointing, head-turning or eye movements, whereas covert attention, as its name implies, refers to the surreptitious deployment of the focus of spatial attention without a change in gaze direction. Despite the lack of motor engagement, covert attention has often been referred to as a form of ‘movement’ (Posner et al., 1982), and it has been theorized that both ‘overt’ and ‘covert’ attention systems rely on the same underlying neural mechanisms, a thesis known as the “premotor theory of attention” (Rizzolatti et al., 1987). Certainly, behavioral evidence has pointed to considerable overlap between covert and overt attention mechanisms (Deubel and Schneider, 1996, Hoffman and Subramaniam, 1995, Kowler et al., 1995), although studies have also shown dissociation is possible (Montagnini and Castet, 2007). Premotor theory also receives considerable support from functional neuroimaging studies where significant anatomical overlap between the covert and overt systems has been shown (Corbetta, 1998, Corbetta et al., 1998). In turn, electrophysiological studies have shown both common and dissociable processes (Eimer et al., 2007, Kelly et al., 2010, Van Der Werf et al., 2008). Thus, there is good evidence for both shared and dissociable mechanisms, but what precisely these shared mechanisms are remains a matter of considerable research interest.

A very well-studied class of overt attention shifts is the saccadic eye movements used to scan the visual world and bring objects of interest into focus on the highly innervated foveal region of the retina. This rapid scanning of visual space involves complex spatial transformations and motor planning. Saccade-targeting also seems to parallel the spatial cuing enhancements observed during covert attention tasks such as increased discrimination of difficult to detect inputs. For example, increased discrimination at saccade target locations is seen prior to the actual movement itself (Deubel and Schneider, 1996), and enhanced detection at saccade target locations is seen even when the movement is aborted prior to action (Hoffman and Subramaniam, 1995). However, by separating the saccadic target from a covertly attended location with probabilistic cues (i.e. 25–75% valid), it was found that covert attention and saccade targeting could in fact be separated when the covertly attended target was likely to be in a different place than the saccadic target (Montagnini and Castet, 2007). Interestingly, this dissociation waned as the moment of the overt movement approached, such that attention targets that were not saccade targets did not receive enhancement when presented in close temporal proximity to saccade onset. Like covert attention, which can be both rapidly drawn to features in the world (i.e. exogenous attention), and also deployed intentionally and voluntarily to features or locations (i.e. endogenous attention), the saccadic system allows for rapid overt shifts that can be captured exogenously or deployed endogenously (i.e. voluntarily). It certainly seems a reasonable proposition that these two systems might rely on at least partially shared mechanisms.

Covert visual attention shifts have also been very well-studied and have been correlated with substantial modulation of sensory processing as indexed by visual evoked potentials (Foxe and Simpson, 2005, Foxe et al., 2003, Gould et al., 2011, Mangun and Hillyard, 1991), as well as strong modulations of oscillatory neural activity (Chalk et al., 2010, Womelsdorf and Fries, 2006). Of particular interest to the present investigation, changes in alpha-band power (~ 8–14 Hz) have been consistently shown to correlate with preparatory states in tasks that require covert shifting of attention (Foxe and Snyder, 2011). It has been demonstrated that increases in alpha power are associated with active suppression of distracters in unattended spatial locations (Banerjee et al., 2011, Kelly et al., 2006, Thut et al., 2006, Worden et al., 2000), as well as suppression of ignored visual features (Snyder and Foxe, 2010) and irrelevant sensory modalities (Foxe et al., 1998, Fu et al., 2001, Gomez-Ramirez et al., 2011, Jones et al., 2010). Moreover, anticipatory alpha power has been directly linked to behavioral outcomes (Haegens et al., 2011a, O'Connell et al., 2009) and the disruption of alpha synchrony via trans-cranial magnetic stimulation affects performance in a target discrimination task (Capotosto et al., 2009). Similarly, it has been shown that spatially-specific measures of anticipatory alpha power over visual cortex are predictive of reaction times (Gould et al., 2011) and subsequent discrimination performance during covert spatial deployments (Handel et al., 2011, Kelly et al., 2009, Thut et al., 2006). In the current study, we set out to establish whether alpha-band oscillatory suppression mechanisms were also invoked during the rapid overt attentional shifts that are characteristic of saccadic targeting. If true, this finding would dramatically reduce the timescale at which alpha might be understood to operate, and further expand the role of alpha rhythms as a mechanism of overt attention.

To date, studies of alpha activity in covert attention have typically employed so-called cue–target-interval paradigms where the preparatory attentional processes are examined across relatively protracted periods of time. In these tasks, participants receive an instructional cue (e.g. an arrow) that tells them to direct their attention to a particular location or to a particular stimulus feature. Then after a delay period, typically on the order of 1–2 s, and sometimes longer, a potential target stimulus is presented upon which the attentional task is then performed. The tradition has been to examine the oscillatory activity during the relatively prolonged anticipatory intervals between the cue and the target stimuli. As such, these studies have not examined alpha-band processes at the more rapid timescales that are implicated during overt attention tasks. Here, we reasoned that if the alpha oscillatory suppression mechanisms also play a role during deployments of the overt attention system, one should observe topographically specific alpha-power shifts that follow the rapid dynamics of the saccadic system. That is, since saccades can be executed with latencies well below 200 ms (Fischer and Boch, 1983), up to 3-to-4 times per second, similarly rapid redeployments of alpha-suppression should be observable.

To address this issue, we examined the temporal dynamics of alpha-band oscillatory activity using a combination of pro- and anti-saccade tasks. During pro-saccades, participants make rapid eye movements to stimuli appearing to the left or right of fixation, whereas during anti-saccade performance, they are required to move their eyes to a position equi-opposite to the location at which the stimulus appeared (i.e. in the opposite hemifield). We made particular use of the anti-saccade task because of its peculiar attentional demands relative to standard saccadic targeting. Successful anti-saccades involve first deploying covert attention to the hemifield of cue appearance, which must then be suppressed to execute an overt shift of attention to the opposite hemifield. It is precisely this sort of rapid attentional shifting that was of primary interest to us here. Since lateralization of alpha-band power has been previously shown to be correlated with retinotopic attention shifts (Thut et al., 2006, Worden et al., 2000), we asked whether this same mechanism might also be flexible and rapid enough in the deployments of attention during anti-saccade performance. Since saccades naturally occur at intervals that are much faster than those studied in most previous alpha-band investigations (Gutteling et al., 2010), it would stand to reason that if alpha-power dynamics represent a shared mechanism for covert and overt attention, such rapid dynamics should be revealed as a shift in power across hemifields from the cue-side to the saccade-side, during the anti-saccade task.

Section snippets

Participants

Sixteen healthy volunteers (2 left-handed, 8 female, mean age = 29.4 with a standard deviation = 7.5 years) participated in this study, the procedures for which were approved by the Institutional Review Boards of the City College of New York and the Albert Einstein College of Medicine. All experimental procedures were carried out in accordance with the ethical standards codified by the World Medical Association in the Declaration of Helsinki (World Medical Organization, 1996). All subjects gave

Results

Overall, as hypothesized the lateralization of alpha power was indeed found to shift rapidly across hemispheres during the performance of overt attention tasks and was particularly evident in the anti-saccade condition. We will first describe the observed pattern of results, followed by a formal statistical analysis as described in the Materials and methods section.

Discussion

A growing body of research on the ongoing oscillatory activity of the brain points to a prominent role for the ~ 8–14 Hz alpha rhythm in attentional processes (Dockree et al., 2007, Foxe and Snyder, 2011, Romei et al., 2012). Previous work has clearly demonstrated that increases in alpha power correlate with active suppression of unattended space under both visuospatial (Kelly et al., 2006, Rihs et al., 2007, Worden et al., 2000) and audiospatial (Banerjee et al., 2011, Kerlin et al., 2010) task

Conclusions

The data presented here suggest that rapidly shifting alpha power is a shared neural mechanism during both covert and overt attention tasks. These results not only expand the conception of an active role of 8–14 Hz alpha rhythms to overt attention tasks, but they also suggest a more rapid timescale for the deployment of spatial attention by capitalizing on the very rapid shifts of attention across hemifields necessary in the anti-saccade task.

The following are the supplementary data related to

Acknowledgments

This work was primarily supported by a National Science Foundation (NSF) grant to J.J.F. (BCS0642584). Additional support was derived from a National Institute of Mental Health (NIMH) grant (MH085322 to J.J.F.). Support for the work of J.W. and M.R.H. was derived from NSF grant BCS0842464 and a National Eye Institute grant (EY019508 to J.W. and M.R.H.). Dr. Snyder was supported by a Ruth L. Kirschstein National Research Service Award (NRSA) pre-doctoral fellowship from the NIMH (MH087077).

Dr.

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