Frequency-specific mechanism links human brain networks for spatial attention

Abstract

Selective attention allows us to filter out irrelevant information in the environment and focus neural resources on information relevant to our current goals. Functional brain-imaging studies have identified networks of broadly distributed brain regions that are recruited during different attention processes; however, the dynamics by which these networks enable selection are not well understood. Here, we first used functional MRI to localize dorsal and ventral attention networks in human epileptic subjects undergoing seizure monitoring. We subsequently recorded cortical physiology using subdural electrocorticography during a spatialattention task to study network dynamics. Attention networks become selectively phase-modulated at low frequencies (δ, θ) during the same task epochs in which they are recruited in functional MRI. This mechanism may alter the excitability of task-relevant regions or their effective connectivity. Furthermore, different attention processes (holding vs. shifting attention) are associated with synchrony at different frequencies, which may minimize unnecessary cross-talk between separate neuronal processes.O ne of the hallmarks of effective behavior is the ability to flexibly attend to particular stimuli in the environment. Selective attention can be driven endogenously by one's current goals or by salient external stimuli. Human neuroimaging studies have identified two sets of fronto-parietal regions that are recruited during these two types of attention. A set of dorsal fronto-parietal regions (dorsal attention network or DAN) shows sustained activity during endogenous or goal-driven attention (1), and reorienting to unexpected targets transiently activates both the DAN and a second set of regions, the ventral attention network (VAN) (2). Although functional MRI (fMRI) has identified the brain regions that are involved in these attentional operations (3, 4), the slow nature of the hemodynamic response has severely limited the study of network dynamics at behaviorally relevant time scales (5). Here, we report results obtained by cortical surface (electrocorticography or ECoG) recordings in epilepsy patients undergoing clinical monitoring to identify seizure foci. Electrode locations for each subject were colocalized with functional brain networks, including the DAN and VAN identified in the same subjects using fMRI. This experimental paradigm allowed us to objectively link fast electrophysiological dynamics, during performance of an attention task, to well-studied functional brain networks.ECoG measures nonspiking, local field potential oscillations across a range of frequencies, which are thought to reflect fluctuations in local neuronal excitability (6, 7). Phase modulations of activity within a region and between regions may therefore affect, respectively, their ability to respond to inputs and to transfer information between one another (8, 9). In support of this theory, previous studies in both animals and humans have shown that either local or long-distance synchrony change in a tas...

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

“…These dynamic and functional characteristics appear to correspond closely to the ventral and dorsal attention networks operating in the theta range identified by Daitch et al (2013). Previous studies have found a consistent correlation between theta fronto-parietal synchronization and attentional processing in working memory tasks (Sauseng et al, 2005(Sauseng et al, , 2010Deiber et al, 2007), especially in the right hemisphere (Astle et al, 2015).…”

“…The current observation that theta PLV was increased during target processing is in line with these studies by indicating enhanced reactivity to task relevance. Hence, the frontoparietal theta synchronization analyzed here appears associated with mechanisms of top-down control and may therefore capture the activation of attentional networks (Daitch et al, 2013).…”

The roles of cortical oscillations in sustained attention

“…This communication may also be facilitated by long-range, low-frequency (<14 Hz) phase synchronisation. Increased low-frequency phase synchronisation between frontal and posterior areas is commonly observed during the orientation of attention [46][47][48], and has been found to predict improvements in attention following momentary attentional lapses [49,50]. Furthermore, during sustained attention tasks, fronto-posterior phase synchronisation in the alpha band has been found to decrease with cognitive fatigue [51,52] and to increase during periods of participantassessed 'on-task' performance [53].…”

Increases in Functional Connectivity between Prefrontal Cortex and Striatum during Category Learning

“…We sought to test for functional connectivity between the PFC and STR by examining synchrony between oscillations of their local field potentials (LFPs; Friston et al, 2013). Frequency-dependent synchrony between LFPs suggests neural communication and has been observed in perceptual (Hipp et al, 2011), motor (Brovelli et al, 2004), and cognitive tasks (Daitch et al, 2013). The functional connectivity between BG and PFC is of particular interest, as the network between them has been implicated in several neurological and psychiatric conditions, such as autism and schizophrenia (Padmanabhan et al, 2013; Uhlhaas and Singer, 2012; Yoon et al, 2012).…”