Functionally defined white matter of the macaque monkey brain reveals a dorso-ventral attention network.

Ilaria Sani,Winrich A Freiwald,Franco Pestilli,Heiko Stemmann,Brent C Mcpherson

doi:10.7554/elife.40520

Ilaria Sani, Winrich A Freiwald + Show 3 more

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https://doi.org/10.7554/elife.40520

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Abstract

Classical studies of attention have identified areas of parietal and frontal cortex as sources of attentional control. Recently, a ventral region in the macaque temporal cortex, the posterior infero-temporal dorsal area PITd, has been suggested as a third attentional control area. This raises the question of whether and how spatially distant areas coordinate a joint focus of attention. Here we tested the hypothesis that parieto-frontal attention areas and PITd are directly interconnected. By combining functional MRI with ex-vivo high-resolution diffusion MRI, we found that PITd and dorsal attention areas are all directly connected through three specific fascicles. These results ascribe a new function, the communication of attention signals, to two known fiber-bundles, highlight the importance of vertical interactions across the two visual streams, and imply that the control of endogenous attention, hitherto thought to reside in macaque dorsal cortical areas, is exerted by a dorso-ventral network.

Highlights

Attention is the neuro-cognitive function that selects currently relevant pieces of information at the expense of irrelevant ones (Carrasco, 2011; Chelazzi et al, 2011)
To unravel whether PITd communicates with attention areas lateral intraparietal area (LIP) and frontal eye field (FEF) in parietal and frontal cortex, we combined functional magnetic resonance imaging (fMRI) localization of attention-modulated areas PITd, LIP, and FEF with ex-vivo dMRI (Figure 1A–C)
We tested whether the connections between functionally defined areas LIP and FEF conform to the previously established finding, that direct LIP-FEF connections run through a component of the Superior Longitudinal Fasciculus (SLF; Figure 1D dark and light blue dashed lines; Blatt et al, 1990; Lewis and Van Essen, 2000; Petrides and Pandya, 2006), a notion obtained without targeting attentional areas

Summary

Introduction

Attention is the neuro-cognitive function that selects currently relevant pieces of information at the expense of irrelevant ones (Carrasco, 2011; Chelazzi et al, 2011). The fronto-parietal theory of attentional control is supported by recent whole-brain functional magnetic resonance imaging (fMRI) studies in the macaque monkey using a wide range of attention tasks (Caspari et al, 2015; Patel et al, 2015; Stemmann and Freiwald, 2016) One of these studies (Stemmann and Freiwald, 2016), found that an area in the lower bank of the Superior Temporal Sulcus (STS), the dorsal posterior infero-temporal area, PITd (Felleman and Van Essen, 1991; Saleem and Logothetis, 2007) was even more strongly attention-modulated than LIP, was engaged by multiple attention tasks, and was not modulated by the task-relevant feature dimension.

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