Integrating brain function and structure in the study of the human attentional networks: a functionnectome study

Abstract

Attention is a heterogeneous function theoretically divided into different systems. While functional magnetic resonance imaging (fMRI) has extensively characterized their functioning, the role of white matter in cognitive function has gained recent interest due to diffusion-weighted imaging advancements. However, most evidence relies on correlations between white matter properties and behavioral or cognitive measures. This study used a new method that combines the signal from distant voxels of fMRI images using the probability of structural connection given by high-resolution normative tractography. We analyzed three fMRI datasets with a visual perceptual task and three attentional manipulations: phasic alerting, spatial orienting, and executive attention. The phasic alerting network engaged temporal areas and their communication with frontal and parietal regions, with left hemisphere dominance. The orienting network involved bilateral fronto-parietal and midline regions communicating by association tracts and interhemispheric fibers. The executive attention network engaged a broad set of brain regions and white matter tracts connecting them, with a particular involvement of frontal areas and their connections with the rest of the brain. These results partially confirm and extend previous knowledge on the neural substrates of the attentional system, offering a more comprehensive understanding through the integration of structure and function.

Keywords: Attention; Executive attention; Phasic alerting; Spatial orienting; White matter; fMRI.

Fig. 1

Pipeline of the fMRI procedure including key steps. CCS, cluster detection threshold; CDT, cluster-defining threshold; GLM, general linear model; MNI, Montreal Neurological Institute

Fig. 2

Sequence and timing of events in a given trial of each of the three attentional tasks: (A) alerting task, (B) orienting task, and (C) executive attention task. Adapted with permission from Chica et al. , ; Martín-Signes et al.

Fig. 3

(A) Brain sections showing activations obtained in the contrast Tone > No tone for the alerting task at a cluster-defining threshold of Z > 2.3 and a corrected cluster significance threshold of p = 0.05. The color bar denotes Z-values. (B) Representation of activations depicted in panel A over a normalized template of tractography. Tractography slices are 10 mm thick to create a 3D effect. Blue color represents the skeleton of fibers and colors from purple to red denote Z-values. IFG, inferior frontal gyrus; MLF, middle longitudinal fasciculus; SLF III; superior longitudinal fasciculus, ventral branch; T-O cortex, temporo-occipital cortex

Fig. 4

Whole-brain voxel-wise correlations between the behavioral indices of the use of attentional signals (see methods section for calculation method) and the contrast of interest at a cluster-defining threshold of Z > 2.3 and a corrected cluster significance threshold of p = 0.05 for (A) the alerting task and (B) the orienting task. The color bars denote Z-values

Fig. 5

(A) Brain sections showing activations obtained in the contrast Cue > Null for the orienting task at a cluster-defining threshold of Z > 2.3 and a corrected cluster significance threshold of p = 0.05 The color bar denotes Z-values. (B) Representation of activations depicted in panel A over a normalized template of tractography. Tractography slices are 10 mm thick to create a 3D effect. Blue color represents the skeleton of fibers and colors from purple to red denote Z-values. ACC, anterior cingulate cortex; FEF, frontal eye field; SMA, supplementary motor area; SLF I/II, superior longitudinal fasciculus, dorsal and medial branches; SPL, superior parietal lobe; T-O cortex, temporo-occipital cortex

Fig. 6

(A) Brain sections showing activations obtained in the contrast Incongruent > Congruent for the executive attention task at a cluster-defining threshold of Z > 2.3 and a corrected cluster significance threshold of p = 0.05. (B) Representation of activations depicted in panel A over a normalized template of tractography. Tractography slices are 10 mm thick to create a 3D effect. Blue color represents the skeleton of fibers and colors from purple to red denote Z-values. ACC, anterior cingulate cortex; FAT, frontal aslant tract; IFG, inferior frontal gyrus; MLF, middle longitudinal fasciculus; MFG, middle frontal gyrus; PrCG, precentral frontal gyrus; SLF, superior longitudinal fasciculus; SMA, supplementary motor area; SPL, superior parietal lobe; T-O cortex, temporo-occipital cortex