Frontal-to-Parietal Top-Down Causal Streams along the Dorsal Attention Network Exclusively Mediate Voluntary Orienting of Attention

Takashi J Ozaki,Mitchell Valdes-Sosa

doi:10.1371/journal.pone.0020079

Abstract

Previous effective connectivity analyses of functional magnetic resonance imaging (fMRI) have revealed dynamic causal streams along the dorsal attention network (DAN) during voluntary attentional control in the human brain. During resting state, however, fMRI has shown that the DAN is also intrinsically configured by functional connectivity, even in the absence of explicit task demands, and that may conflict with effective connectivity studies. To resolve this contradiction, we performed an effective connectivity analysis based on partial Granger causality (pGC) on event-related fMRI data during Posner's cueing paradigm while optimizing experimental and imaging parameters for pGC analysis. Analysis by pGC can factor out exogenous or latent influences due to unmeasured variables. Typical regions along the DAN with greater activation during orienting than withholding of attention were selected as regions of interest (ROIs). pGC analysis on fMRI data from the ROIs showed that frontal-to-parietal top-down causal streams along the DAN appeared during (voluntary) orienting, but not during other, less-attentive and/or resting-like conditions. These results demonstrate that these causal streams along the DAN exclusively mediate voluntary covert orienting. These findings suggest that neural representations of attention in frontal regions are at the top of the hierarchy of the DAN for embodying voluntary attentional control.

Highlights

Voluntary visual attentional control has been found to be mediated by large-scale distributed cortical regions across the frontal, parietal and visual cortices, called the dorsal attention network (DAN) [1,2,3,4]
We first performed an event-related functional magnetic resonance imaging (fMRI) experiment using the Posner cueing paradigm [21], after optimizing experimental and imaging parameters for partial Granger causality analysis. This was followed by a pGC analysis on the fMRI data, to quantify and evaluate causal streams along the DAN for orienting, holding, and other attentional states
Our fMRI data and the results of pGC analysis indicate that frontal-to-parietal top-down causal streams along the DAN were exclusively related to voluntary orienting of attention, not to any other less-attentive states

Summary

Introduction

Voluntary visual attentional control has been found to be mediated by large-scale distributed cortical regions across the frontal, parietal and visual cortices, called the dorsal attention network (DAN) [1,2,3,4]. The DAN was first regarded as a parallel processing network, activated immediately upon the demands of voluntary attentional control [10,11,12] This conventional concept has been challenged, since studies in primates have suggested causal relationships between the frontal and parietal regions, as revealed by multi-site single unit recordings [13] and microstimulation [14]. Recent functional magnetic resonance imaging (fMRI) studies with effective connectivity analysis have suggested that voluntary attentional control is mediated by causal streams along the DAN from frontal to parietal or to the visual cortex [15,16]. The combination of transcranial magnetic stimulation (TMS) and fMRI showed similar top-down frontoparietal causal streams during a visuospatial judgment task [17,18], suggesting that the DAN is not a parallel but a serial processing network embodied by causal streams from frontal to parietal or to the visual cortex mediating voluntary attentional control

Methods

Results

Conclusion