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). Attentional selection results from the interplay between exogenous factors, like intrinsic object saliency, and endogenous processes, like the relevance of an object for the task at hand. Endogenous attention is thought to be controlled by a fronto-parietal network (Corbetta et al., 2008; Kastner and Ungerleider, 2000). In the macaque monkey brain, the lateral intraparietal area (LIP; Bisley and Goldberg, 2010; Gottlieb et al., 1998) and the frontal eye field (FEF; Thompson and Bichot, 2005) exhibit key properties of attentional control and are thought to form the core of the endogenous attention network (Stemmann and Freiwald, 2016).

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. Thus PITd was shown to exhibit key properties of an attentional control area (Figure 1A–B; Stemmann and Freiwald, 2016). These results raised the possibility that the network for endogenous control of attention may not be confined to fronto-parietal (dorsal) structures, but also includes a ventral region in the temporal lobe.

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A ventral attention network has been previously proposed in humans (Corbetta et al., 2008; Geng and Vossel, 2013). However, its functional properties are profoundly different from those of macaque area PITd. First, human dorsal and ventral attention networks have a different functional profile, with the first primarily supporting endogenous attention, and the latter primarily supporting exogenous attention (Corbetta et al., 2008), along with context updating (Geng and Vossel, 2013) and social cognition (Carter and Huettel, 2013; Mars et al., 2013; Schwiedrzik et al., 2015). On the contrary ventral area PITd shared similar functional properties with dorsal areas LIP and FEF (Stemmann and Freiwald, 2016). Second, the most prominent part of the human ventral attention network, the temporo-parietal-junction (TPJ), is suppressed during endogenous attention, and activated during target detection and shifts of attention, particularly when stimuli are salient or unexpected (Corbetta et al., 2008; Corbetta and Shulman, 2002), whereas PITd was strongly activated during prolonged sustained attention (Stemmann and Freiwald, 2016). Third, macaque PITd possesses a putative human homolog, phPITd, an area located far ventrally to TPJ (Glasser et al., 2016; Kolster et al., 2010). Thus the discovery of attention area PITd located ventrally to the ventral attention network raises important questions about attentional control mechanisms and their support circuitry.

In the brain imaging literature, the term network is often used loosely to describe a set of co-activated brain regions without explicit reference to their physical connections (Petersen and Sporns, 2015). The fact that multiple brain areas exhibit similar functional profiles across visual and cognitive conditions, like PITd, LIP and FEF did in (Stemmann and Freiwald, 2016), could be for a number of fundamentally different reasons. Co-activation might be initiated by a common driver outside the brain, like the visual stimulus, it could result from a common source inside the brain, with functional nodes only indirectly connected, or from connections that directly link the areas of interest. Only the characterization of the connectivity pattern between functionally identified areas establishes true network status. Understanding the structure of connectivity between putative attention control areas would thus be critical to establish whether they form an attention control network and help to answer the question of how they might coordinate a common focus of attention.

Long-range inter-areal connectivity is supported by the white matter. Uncovering the white matter tracts supporting endpoint-to-endpoint connections is important to know for at least two reasons. First, fascicles respond to behavior by adapting density, shape, and molecular composition in a manner that corresponds to individual abilities in health and disease (Fields, 2008; Jbabdi et al., 2015; Pestilli, 2018; Rokem et al., 2017; Thomason and Thompson, 2011; Wandell, 2016), and thus take an active role in shaping network function. To fully understand brain functionality, we thus need to combine knowledge about brain function and structure. Second, connectivity is crucial to elucidating how neurons and neural networks process information. The main organizing principle of the visual system is its separation into two major posterior-anterior information-processing streams: a dorsal path for spatial processing, and a ventral path for feature and object processing (Kravitz et al., 2013; Milner and Goodale, 1995). Each pathway may contain multiple, largely parallel routes (Kravitz et al., 2013), a conclusion that seems to be confirmed by the existence of dorsal and ventral attention areas. In this view, the study of connectivity between parietal and temporal attention nodes can serve as a model system for a general understanding of information flow between the dorsal and ventral visual pathways and between the parietal and temporal lobes at large.

Here we sought to, first, determine connections between attention areas PITd, LIP, and FEF, and, second, to delineate the long association fascicles of this postulated endogenous attention control network. Previous anatomical studies have demonstrated strong and direct connections between parietal area LIP and frontal area FEF (Blatt et al., 1990; Lewis and Van Essen, 2000; Petrides and Pandya, 2006) mainly via the Superior Longitudinal Fasciculus (SLF). However, function and anatomy of PITd have, so far, received little attention. More specifically, to date only a single classical anatomical study has targeted PITd (Distler et al., 1993), but due to the study’s paucity of data and lack of functional characterization, the relationship to attention networks remains unclear. We thus asked whether PITd connects to LIP, whether it connects to the FEF, and which fiber pathways these cortical areas use to exchange attentional information (Figure 1D). The general anatomy of macaque white matter organization suggests different candidate pathways: PITd may connect to LIP through the Vertical Occipital Fasciculus (VOF), a fascicle that has been shown to have some ventral terminations in the temporal cortex (Takemura et al., 2017). Alternatively, PITd and LIP might connect through a more anterior fascicle, the vertical branch of the Inferior Longitudinal Fasciculus (vILF). Similarly, it would be possible for PITd and the FEF to connect via one of two major pathways: fibers might run via the Arcuate Fasciculus (AF), as areas in the caudal superior temporal regions do (Petrides and Pandya, 2006). Alternatively, fibers connecting PITd and FEF could course via the Extreme Capsule (EmC), as the middle superior temporal region and some anterior patches of the inferior temporal sulcus do (Petrides and Pandya, 1988; Petrides and Pandya, 2006).

To test these hypotheses, we developed a new approach that combines in-vivo fMRI with high-resolution ex-vivo diffusion imaging (dMRI) and ensemble probabilistic tractography. This experimental approach was specifically designed to facilitate the comparison of dMRI with classical tracer studies, and overcome some of the limitations of dMRI and tractography. For example, this approach reduces artifacts and distortions, improves robustness to crossing fibers, and advances anatomical accuracy. This technique allows for the study of the connectivity of functionally specific brain areas, the exploration of fine-grain structural connectivity, and the description of the pathways connecting the functional areas. These three aspects are key to the understanding of brain functional networks, and the lack of a method combining them all has prevented, so far, the full characterization of the macaque attention network. High-resolution dMRI, combined with functionally-defined tractography, also facilitates the comparison between human and non-human cognitive networks, helps define which circuitry in the macaque attention system can serve as an accurate model for humans, and bridges the gap between traditional tracer studies and dMRI in humans.

Endogenous attentional control in both humans and macaque monkeys is thought to be exerted by a fronto-parietal network (Corbetta et al., 2008; Gottlieb et al., 1998; Kastner and Ungerleider, 2000; Thompson and Bichot, 2005). Here we show that, in the macaque brain, classical attentional control areas LIP, in posterior parietal cortex, and FEF, in prefrontal cortex, are connected to PITd, an area in temporal cortex only recently implied in endogenous attention (Stemmann and Freiwald, 2016). We thus provide new evidence that PITd might be an endogenous attention control area, that attentional control may not be limited to dorsal fronto-parietal structures in the macaque brain, and that these areas form an attention network through direct connections (Figure 5 and Figure 5—video 1). The fine anatomical characterization of the bundles connecting the three areas constitutes the first connectivity model of the macaque endogenous attention and should inform future theories of attentional processing.

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PITd is a visual area located in the lower bank of the STS, it contains neurons that are shape- and color-selective (Conway and Tsao, 2009; Hikosaka, 1998) and have circumscribed receptive fields slightly larger than those of V4 (Hikosaka, 1998). Its anatomical connectivity and its role in cognition have been little explored. While LIP-FEF connectivity has been established through tracer studies (Blatt et al., 1990; Lewis and Van Essen, 2000; Petrides and Pandya, 2006), connectivity of either area with the attention-modulated part of PITd has hitherto remained unknown. Even general connectivity with PITd, anatomically defined, was not fully established. One previous anatomical study investigated cortical connections of inferior temporal areas (Distler et al., 1993) and, through a single tracer injection in PITd, provided some evidence for connectivity between PITd and LIP. Due to the study’s paucity of data and lack of relating connectivity to functional characterization, the relationship to attentional control networks remained unclear. Similarly, tracer studies targeting LIP and FEF showed variable results in terms of existence and strength of connections with PITd (Barbas and Mesulam, 1981; Barbas, 1988; Blatt et al., 1990; Bullier et al., 1996; Distler et al., 1993; Schall et al., 1995). These inconsistencies are likely the result of differences in tracing methods, injection sites, anatomical definitions, and possibly even nomenclature (Felleman and Van Essen, 1991; Kötter, 2004; Stephan et al., 2001). We resolved these difficulties by combining functional mapping with dMRI. The part of PITd that is strongly modulated by attention in ways similar to those of LIP and FEF, is directly connected to these two classical attentional control regions. The comparative tractography we conducted between PITd and nearby functional areas (Figure 4—figure supplement 4) confirms the existence of tract-specific connections from PITd and demonstrates that, structurally, this connectivity is part of a larger-scale pattern of connectivity that PITd shares with its immediate neighborhood. Yet, functionally, PITd differs fundamentally from nearby STS areas in not being motion selective, while being very strongly attention modulated during attentive motion discrimination. Thus, functional specificity of PITd does not arise as a simple consequence of its connectivity with LIP and FEF. It is noteworthy that this connectivity scheme is different from the nearby face-processing network (Grimaldi et al., 2016; Moeller et al., 2008), which encompasses two face areas right next to attention-modulated area PITd (Stemmann and Freiwald, 2016). In the face-processing network, tight connectivity between face areas helps to ensure domain specificity (for faces) (Grimaldi et al., 2016; Moeller et al., 2008). Yet, for attention control networks shared connectivity fulfills the need to exert control over multiple areas and gather visual information from across multiple visual domains (Fecteau and Munoz, 2006). In particular, PITd’s position within the ventral visual pathway is likely crucial to collect attention-relevant information about properties of objects (Conway and Tsao, 2009; Hikosaka, 1998), including faces (Tsao et al., 2006) and gaze (Marciniak et al., 2014), possibly providing information on object value (Ghazizadeh et al., 2018). Through the described connections, PITd might thus make important contributions to core functionality of endogenous attention and to a wide range of attention-related functions.

In humans, attention has been proposed to be controlled by two networks with different functions, located in the dorsal and ventral part of the brain (Corbetta et al., 2008). The most prominent part of the ventral attention network is the temporo-parietal-junction (TPJ). TPJ is suppressed during endogenous attention, and activated during target detection and shifts of attention, particularly when stimuli are salient or unexpected (Corbetta et al., 2008; Corbetta and Shulman, 2002). It is thus thought to be functionally, but also anatomically, distinct from the dorsal fronto-parietal network (Corbetta et al., 2008). An area homologous to TPJ in the macaque has been hypothesized, but not yet found (Patel et al., 2015). Macaque PITd is activated during sustained attention (Stemmann and Freiwald, 2016), does not activate during attentional shift (Caspari et al., 2015), and, as we show here, is structurally connected to the dorsal fronto-parietal network. PITd thus bears neither functional nor structural similarity to human TPJ. One of the macaque candidate regions previously suggested for the putative correspondence to the human TPJ is the dorsal bank of STS and the adjacent superior temporal gyrus. Lesions of this region cause neglect-like (or spatial extinction-like) syndromes (Luh et al., 1986; Scalaidhe et al., 1995; Watson et al., 1994), which led to a suggestion of a possible homology to the (right hemisphere) superior temporal gyrus (STG) in humans, one of the major lesion foci in neglect patients (Karnath, 2001). Alternatively, macaque TPO/STP and neighboring parietal area seven were hypothesized to correspond to human TPJ. These dorsal STS areas show, similarly to areas LIP and FEF, memory delay activity during saccade preparation (Kagan et al., 2010), and exhibit task-specific changes after reversible LIP inactivation (Wilke et al., 2012). Furthermore, recent work on the social brain also suggested that a potential precursor to human TPJ may reside in macaque posterior dorsal STS (Schwiedrzik et al., 2015) or in area 7a (Sliwa and Freiwald, 2017). Furthermore, macaque PITd possesses a putative human homolog, phPITd, an area located far ventrally to TPJ (Glasser et al., 2016; Kolster et al., 2010). Human phPITd occupies a similar positions in retinotopic cortex as macaque PITd, and, like PITd, is sensitive to two-dimensional shapes and is insensitive to motion (Kolster et al., 2010). Our results predict, under a homology argument of attention network organization, this area as the ventral node of the human endogenous attention network.

PITd connects to LIP and FEF through specific white matter tracts. Knowing these tracts is important for a full characterization of endogenous attentional control circuits, their vulnerabilities, and developmental potential. For example, the properties of specific fiber-bundles have been found to correlate with attentive behaviors (Chechlacz et al., 2015; Chica et al., 2018; Parlatini et al., 2017), and their disconnection results in attentional deficits like spatial neglect (Carter et al., 2017; Lunven and Bartolomeo, 2017), it is therefore of great importance to characterize their structure and path. Traditional tracer studies typically focus on the analysis of the origins and terminations of white matter fibers, without characterizing the white matter pathways between the endpoints. Our experimental approach, by capitalizing on the macroscopic bird-eye view of dMRI (Jbabdi et al., 2015; Rokem et al., 2017) combined with behaviorally guided fMRI (Stemmann and Freiwald, 2016), allowed us also to describe the cortico-cortical pathways of the endogenous control attention. We established that the vertical branch of the ILF, but not the VOF, connects the two posterior attention areas PITd with LIP, and that the ILF and the EmC, but not the AF, connects PITd to the dorsal prefrontal area FEF. Our results thus imply a role in attentional control for the vILF and the ILF/EmC. (Figure 5 and Figure 5—video 1).

We have used quality data, combined multimodal data, and used advanced quantification and statistical evaluation methods (see Material and methods), yet we fully acknowledge that tractography has limitations and is challenged by the trade-off between specificity and sensitivity (Thomas et al., 2014). Recent studies have demonstrated limitations of dMRI-based tractography in three important way: (1) in the ability to solve crossing fibers (Maier-Hein et al., 2017; Roebroeck et al., 2008), (2) in the dependency on tractography algorithms or parameter settings (Bastiani et al., 2012; Chamberland et al., 2014; Domin et al., 2014; Kunimatsu et al., 2004; Parizel et al., 2007; Takemura et al., 2016a; Taoka et al., 2009; Thomas et al., 2014), and (3) in the accuracy for estimating fiber projections into cortical gray matter (Reveley et al., 2015). Our results set the foundation for future investigations using other modalities to infer the connectivity of attentional control circuitry in macaque monkeys and other species, like human subjects.

In humans, two distinct vertical fiber bundles that connect the dorsal and ventral visual streams have been described, the VOF and the posterior Arcuate Fasciculus (pAF). The VOF supports a variety of perceptual functions, like skilled reading and spatial orienting (Takemura et al., 2016b; Yeatman et al., 2014; Yeatman et al., 2013), the pAF, located anterior to the VOF (Catani and Thiebaut de Schotten, 2008; Thiebaut de Schotten et al., 2014; Weiner et al., 2017), is thought to support language (Catani and Thiebaut de Schotten, 2008; Thiebaut de Schotten et al., 2014) and action-to-object coordination (Budisavljevic et al., 2018). The existence of two separated vertical tracts in the posterior part of the human brain resembles the connectivity profile of the monkey described here and suggest a possible resolution of current cross-species inconsistencies in the literature. Because of its anatomical location, its cortical endpoints, and its separation from the VOF, human pAF may be a candidate tract for the exchange of attentional information between dorsal and ventral attention areas in the posterior part of the human brain, thus being functionally and anatomically similar to the vILF. The fronto-temporal connection between macaque PITd and FEF via the EmC we found in this study, may also have a human homolog. Human EmC is important for language (Catani and Bambini, 2014; Friederici and Gierhan, 2013) and may also carry attentional information (Umarova et al., 2010). Umarova and colleagues found that human EmC connects ventral frontal cortex and insula to the TPJ, namely the core nodes of the human exogenous attention network (Corbetta et al., 2008; Corbetta and Shulman, 2002). A direct connection via EmC between phPITd and FEF would suggest a division of function between phPITd and TPJ, but similar frontal lobe connectivity. Alternatively, the functional difference between PITd and TPJ may be paralleled by a difference in structural connectivity: the AF may be a good candidate to exchange endogenous attention information between human frontal and temporal lobes. Future work examining both structure and function in the human brain should be able clarify the structural similarity between macaque and human attention networks and thus reveal putative constraints by white-matter fascicles on the evolution of functional networks. Determining the mesoscopic correspondence between structure and function across species is a fundamental challenge for neuroscience (Zhang et al., 2013), a challenge that cannot be met by pure functional and pure anatomical measurements alone (Pollen and Hofmann, 2008). The first fine-scale functional characterization of the white matter tracts supporting endogenous attention described here sets up a new framework to understand the evolution of function in white matter bundles, and to determine the relationship between brain structure and function during evolution.

The main organizing principle of the visual system is its separation into two major posterior-anterior information-processing streams: a dorsal path for spatial processing, and a ventral path for feature and object processing (Kravitz et al., 2013; Milner and Goodale, 1995). Separation of information into different streams, however, appears to be at odds with the requirements of visual attention which generally needs to integrate spatial and featural information (Baylis et al., 2001; Milner, 2017; Treisman and Gelade, 1980). One possible solution to this binding problem, is the development of shape-selectivity in the dorsal stream (Theys et al., 2015). Alternatively, vertical connections between the dorsal and ventral attention areas as described here, provide a structural substrate for attentional integration that capitalizes on the full functional repertoire of both streams. This vertical connectivity may thus be a general theme, a second organizing principle of the visual system in humans (Kay and Yeatman, 2017; Pestilli et al., 2014) and macaques (Nelissen et al., 2011), extending from attention to other functions requiring vertical integration like language (Cloutman, 2013) or skilled grasping (van Polanen and Davare, 2015).

Taken together, our work advances the understanding of the architecture of attentional control by suggesting a three-node cortical network, with nodes in three different cortical lobes as the structural substrate of this cognitive function. The description of direct structural connections between these nodes we provide here, now allows investigations of the ‘effective connectivity’ between attention areas and the causal impact of these interactions. The findings reported here have important consequences for the understanding of the mechanisms and functional capabilities of endogenous attention, for cognitive theories of endogenous attention (Itti et al., 2005), for the evolution of attention systems, and for the functional organization of the primate brain.

All data generated or analysed during this study are included in the manuscript and supporting files. Source data for Figures 2, 3, 4, 5, have been made available via the Open Science Framework (https://osf.io/8ks5t/).

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Author details

1. Ilaria Sani

   Laboratory of Neural Systems, The Rockefeller University, New York, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   isani01@rockefeller.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4389-7263

2. Brent C McPherson

   Department of Psychological and Brain Sciences, Indiana University, Bloomington, United States

   Contribution

   Data curation, Formal analysis, Methodology

   Competing interests

   No competing interests declared

3. Heiko Stemmann

   Institute for Brain Research and Center for Advanced Imaging, University of Bremen, Bremen, Germany

   Contribution

   Conceptualization, Formal analysis

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7492-1115

4. Franco Pestilli

   Department of Psychological and Brain Sciences, Indiana University, Bloomington, United States

   Contribution

   Conceptualization, Resources, Software, Supervision, Funding acquisition, Writing—review and editing

   Contributed equally with

   Winrich A Freiwald

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2469-0494

5. Winrich A Freiwald

   Laboratory of Neural Systems, The Rockefeller University, New York, United States

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Writing—review and editing

   Contributed equally with

   Franco Pestilli

   For correspondence

   wfreiwald@rockefeller.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8456-5030

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