Oscillatory alpha-band suppression mechanisms during the rapid attentional shifts required to perform an anti-saccade task
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.
References (78)
- et al.
Event-related power modulations of brain activity preceding visually guided saccades
Brain Res.
(2007) - et al.
Attention reduces stimulus-driven gamma frequency oscillations and spike field coherence in V1
Neuron
(2010) - et al.
A common network of functional areas for attention and eye movements
Neuron
(1998) - et al.
Saccade target selection and object recognition: evidence for a common attentional mechanism
Vision Res.
(1996) - et al.
ERP correlates of shared control mechanisms involved in saccade preparation and in covert attention
Brain Res.
(2007) - et al.
Beta-band oscillations — signalling the status quo?
Curr. Opin. Neurobiol.
(2010) - et al.
Saccadic eye movements after extremely short reaction times in the monkey target
Brain Res.
(1983) - et al.
Right hemisphere control of visuospatial attention: line-bisection judgments evaluated with high-density electrical mapping and source analysis
NeuroImage
(2003) - et al.
Attention-dependent suppression of distracter visual input can be cross-modally cued as indexed by anticipatory parieto-occipital alpha-band oscillations
Brain Res. Cogn. Brain Res.
(2001) - et al.
Shifting visual attention in space: an electrophysiological analysis using high spatial resolution mapping
Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology
(2000)
An oscillatory mechanism for prioritizing salient unattended stimuli
Trends Cogn. Sci.
EEG alpha oscillations: the inhibition-timing hypothesis
Brain Res. Rev.
The role of attention in the programming of saccades
Vision Res.
Basal ganglia beta oscillations accompany cue utilization
Neuron
Neural mechanisms underlying brain waves: from neural membranes to networks
Electroencephalogr. Clin. Neurophysiol.
Multisensory auditory–visual interactions during early sensory processing in humans: a high-density electrical mapping study
Brain Res. Cogn. Brain Res.
Occipital gamma-oscillations modulated during eye movement tasks: simultaneous eye tracking and electrocorticography recording in epileptic patients
NeuroImage
Covert visual spatial orienting and saccades: overlapping neural systems
NeuroImage
A bias for posterior alpha-band power suppression versus enhancement during shifting versus maintenance of spatial attention
NeuroImage
Reorienting attention across the horizontal and vertical meridians: evidence in favor of a premotor theory of attention
Neuropsychologia
Look who's talking: the deployment of visuo-spatial attention during multisensory speech processing under noisy environmental conditions
NeuroImage
Electroencephalographic cortical oscillations and saccadic eye movements in humans
Neurosci. Lett.
The slow time-course of visual attention
Cogn. Psychol.
Neuronal coherence during selective attentional processing and sensory–motor integration
J. Physiol. Paris
Oscillatory alpha-band mechanisms and the deployment of spatial attention to anticipated auditory and visual target locations: supramodal or sensory-specific control mechanisms
J. Neurosci.
Saccades during object viewing modulate oscillatory phase in the superior temporal sulcus
J. Neurosci.
The phase of ongoing EEG oscillations predicts visual perception
J. Neurosci.
Frontoparietal cortex controls spatial attention through modulation of anticipatory alpha rhythms
J. Neurosci.
Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems?
Proc. Natl. Acad. Sci. U.S.A.
ERP correlates of anticipatory attention: spatial and non-spatial specificity and relation to subsequent selective attention
Experimental brain research Experimentelle Hirnforschung Expérimentation cérébrale
Optimal sustained attention is linked to the spectral content of background EEG activity: greater ongoing tonic alpha (approximately 10 Hz) power supports successful phasic goal activation
Eur. J. Neurosci.
Over de snelheid van psycholische processen
This is the rhythm of your eyes: the phase of ongoing electroencephalogram oscillations modulates saccadic reaction time
J. Neurosci.
Biasing the brain's attentional set: II. Effects of selective intersensory attentional deployments on subsequent sensory processing
Exp. Brain Res.
The role of alpha-band brain oscillations as a sensory suppression mechanism during selective attention
Front Psychol.
Parieto-occipital approximately 10 Hz activity reflects anticipatory state of visual attention mechanisms
Neuroreport
Oscillatory sensory selection mechanisms during intersensory attention to rhythmic auditory and visual inputs: a human electrocorticographic investigation
J. Neurosci.
Indexing the graded allocation of visuospatial attention using anticipatory alpha oscillations
J. Neurophysiol.
Cited by (27)
Microsaccades transiently lateralise EEG alpha activity
2023, Progress in NeurobiologyNeural Substrates of Inhibitory Control Maturation in Adolescence
2019, Trends in NeurosciencesCitation Excerpt :Beta rhythms have been associated with cortical glutamatergic function in deep layers [68], through top-down inputs activating pyramidal neurons. Alpha rhythms have been associated with dampening of neuronal activities through inhibitory processes [69], supporting inhibitory mechanisms in the AS task [70]. These results, consistent with ideas discussed earlier, indicate that dlPFC executive systems are on-line by adolescence, but prefrontal systems are not readily engaged during executive responses, undermining optimal inhibitory control.
Meta-analytic review of the effects of a single dose of intranasal oxytocin on threat processing in humans
2018, Journal of Affective DisordersCitation Excerpt :Short stimulus presentation duration is believed to tap into early attentional responses while longer stimulus duration is believed to examine late attention (Bantin et al., 2016). However, there are still some uncertainties regarding what should be used as the cut-off for early and late attention, with some eye tracking and electroencephalogram (EEG) studies reporting attentional shifts as early as 200 ms after stimulus onset (Bantin et al., 2016; Belyusar et al., 2013; Hedge and Leonards, 2013). Additionally, working memory and executive functioning studies have demonstrated that varying the inter-trial interval can impact performance, with shorter inter-trial intervals utilising more automated responding, while longer inter-trial intervals allow for more controlled responding (Cermak, 1970; Shipstead and Engle, 2013).