Top-down versus bottom-up attention differentially modulate frontal-parietal connectivity.

Jake T Bowling,Karl J Friston,Joseph B Hopfinger

doi:10.1002/hbm.24850

Abstract

The moment‐to‐moment focus of our mind's eye results from a complex interplay of voluntary and involuntary influences on attention. Previous neuroimaging studies suggest that the brain networks of voluntary versus involuntary attention can be segregated into a frontal‐versus‐parietal or a dorsal‐versus‐ventral partition—although recent work suggests that the dorsal network may be involved in both bottom‐up and top‐down attention. Research with nonhuman primates has provided evidence that a key distinction between top‐down and bottom‐up attention may be the direction of connectivity between frontal and parietal areas. Whereas typical fMRI connectivity analyses cannot disambiguate the direction of connections, dynamic causal modeling (DCM) can model directionality. Using DCM, we provide new evidence that directed connections within the dorsal attention network are differentially modulated for voluntary versus involuntary attention. These results suggest that the intraparietal sulcus exerts a baseline inhibitory effect on the frontal eye fields that is strengthened during exogenous orienting and attenuated during endogenous orienting. Furthermore, the attenuation from endogenous attention occurs even with salient peripheral cues when those cues are known to be counter predictive. Thus, directed connectivity between frontal and parietal regions of the dorsal attention network is highly influenced by the type of attention that is engaged.

Highlights

Accurate perception and action depend on the ability of attention systems to focus processing resources on the most salient stimuli in the environment
Involuntary attention—often referred to as exogenous attention because it is thought to be triggered by external stimuli—can be engaged more rapidly and is more resistant to interference than is the type of attention referred to as voluntary, or endogenous attention (e.g., Jonides, 1981; Müller & Rabbitt, 1989)
The present study aims to advance previous work by measuring directed connectivity in the dorsal frontoparietal network for endogenous and exogenous attention, using an optimized fMRI protocol and dynamic causal modeling (DCM), an established method for investigating directed connectivity in the brain (Friston, Harrison, & Penny, 2003)

Summary

| INTRODUCTION

Accurate perception and action depend on the ability of attention systems to focus processing resources on (i.e., select) the most salient stimuli in the environment. These same brain regions showed the opposite temporal pattern— with parietal activation leading frontal activity—when orienting was triggered in an exogenous manner by salient, uninformative, stimuli Despite this definitive finding, functional neuroimaging results have typically found highly similar patterns of activity across these two types; primarily showing activation in a bilateral frontoparietal network (Corbetta et al, 1993; Kim et al, 1999; Kincade, Abrams, Astafiev, Shulman, & Corbetta, 2005; Nobre et al, 1997; Peelen, Heslenfeld, & Theeuwes, 2004), even in the complete absence of any cue stimulus (Hopfinger, Camblin, & Parks, 2010). Based on Buschman and Miller's (2007) results, we asked if the directed connectivity between dorsal frontal and parietal attentional control regions is differentially modified by the type of attention being engaged

| METHODS

| Participants

| RESULTS

| DISCUSSION

Findings

DATA AVAILABILITY STATEMENT