Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans

Abstract

Because of attentional limitations, the human visual system can process for awareness and response only a fraction of the input received. Lesion and functional imaging studies have identified frontal, temporal, and parietal areas as playing a major role in the attentional control of visual processing, but very little is known about how these areas interact to form a dynamic attentional network. We hypothesized that the network communicates by means of neural phase synchronization, and we used magnetoencephalography to study transient long-range interarea phase coupling in a well studied attentionally taxing dual-target task (attentional blink). Our results reveal that communication within the fronto-parieto-temporal attentional network proceeds via transient long-range phase synchronization in the beta band. Changes in synchronization reflect changes in the attentional demands of the task and are directly related to behavioral performance. Thus, we show how attentional limitations arise from the way in which the subsystems of the attentional network interact. T he human brain faces an inestimable task of reducing a potentially overloading amount of input into a manageable flow of information that reflects both the current needs of the organism and the external demands placed on it. This task is accomplished via a ubiquitous construct known as ''attention,'' whose mechanism, although well characterized behaviorally, is far from understood at the neurophysiological level. Whereas attempts to identify particular neural structures involved in the operation of attention have met with considerable success (1-5) and have resulted in the identification of frontal, parietal, and temporal regions, far less is known about the interaction among these structures in a way that can account for the task-dependent successes and failures of attention. The goal of the present research was, thus, to unravel the means by which the subsystems making up the human attentional network communicate and to relate the temporal dynamics of their communication to observed attentional limitations in humans.A prime candidate for communication among distributed systems in the human brain is neural synchronization (for review, see ref. 6). Indeed, a number of studies provide converging evidence that long-range interarea communication is related to synchronized oscillatory activity (refs. 7-14; for review, see ref. 15). To determine whether neural synchronization plays a role in attentional control, we placed humans in an attentionally demanding task and used magnetoencephalography (MEG) to track interarea communication by means of neural synchronization.In particular, we presented 10 healthy subjects with two visual target letters embedded in streams of 13 distractor letters, appearing at a rate of seven per second. The targets were separated in time by a single distractor. This condition leads to the ''attentional blink'' (AB), a well studied dual-task phenomenon showing the reduced ability to report the second of two targets when an interval Ͻ5...

The Role of the Locus Coeruleus in Mediating the Attentional Blink: A Neurocomputational Theory.

“…First, studies using functional imaging methods have suggested that target processing in the attentional blink task is mediated by a widespread cortical network including parietal cortex, anterior cingulate cortex, and lateral frontal cortex (Marois, Chun, & Gore, 2000) and that activation differences in these cortical areas correlate with T2 performance (Kranczioch, Debener, Schwarzbach, Goebel, & Engel, 2005;Marois, Yi, & Chun, 2004). Converging evidence for a relationship between activity in this network and T2 performance has been reported in a recent MEG study (Gross et al, 2004). It is interesting to note that the parietal and frontal cortex are the cortical areas with the densest noradrenergic innervation (Levitt, Rakic, & Goldman-Rakic, 1984;Morrison & Foote, 1986).…”

Synchronization of fronto-parietal beta and theta networks as a signature of visual awareness in neglect

“…Hipp et al (2011) have identified large scale beta synchronization in a distinctive network of frontal, parietal and extrastriate visual areas in relation to visual perceptual organization. Fronto-parietal synchrony in the beta band also has been associated with visual search (Buschman and Miller, 2007), integration of visual information and perceptual grouping (Srinivasan et al, 1999;Phillips and Takeda, 2009;Phillips et al, 2012;Volberg and Greenlee, 2014;Castellano et al, 2014), visual attention (Gross et al, 2004;Marois et al, 2000;Wróbel, 2000), and visual object recognition (Sehatpour et al, 2008;Castellano et al, 2014). These previous studies, however, point to the existence of ongoing fronto-parietal beta synchronization that modulates brain responses to visual input (Gross et al, 2004;Liang et al 2002;Hipp et al, 2011), or beta synchrony at later stages (150-300 ms) of visual stimulus processing (Phillips et al, 2012;Sehatpour et al, 2008;Dehaene and Changeux, 2011).…”

“…Interestingly, right parietal and left frontal regions were identified by Gross et al (2004) as critical for the functioning of a beta target-related network likely representing a state of increased sensitivity (higher vigilance). Exactly these pairs were pathologically enhanced in patients with right hemisphere lesion without neglect.…”

“…2) Such representations are formed (Rees, 2013) but are not accessible or not functional due to specific impairments in the arousal system Shulman, 2011, Chica al., 2012). 3) The mere formation of top-down representations of spatial and feature-based information may be compromised, since attentional top-down representations engage frontal and parietal regions (Gross et al, 2004;Egner et al, 2008;Chica et al, 2013) and modulate subsequent perception (Hipp et al, 2011;Melloni et al, 2011;Wyart et al, 2012). BIT, Behavioral Inattention Test (scores 167-170, no neglect; 136-166, moderate neglect; 73-135, severe neglect); +, minor involvement by the lesion; ++, partial involvement by the lesion; +++, complete involvement by the lesion; (h), hemorrhage; (sh), minor secondary hemorrhage; n.a., not available.…”

Vigilance, alertness, or sustained attention: physiological basis and measurement

“…A significant advantage of synchrony over coherence for the study of attentional phenomena is that by using wavelet analysis, synchrony can be calculated with higher temporal resolution than FFT methods that require several seconds or more of EEG data to calculate coherence. Using magneto-EEG to investigate the attentional blink phenomenon, neuronal synchrony in the beta band locations was increased during successful detection (non-blink) and decreased during missed letters (attentional blink) (Gross et al, 2004). Event-related covariance is another measure of relationship between different locations and decreases in event-related covariance have been related to performance decrements on sustained attention tasks (Gevins et al, 1987).…”