Bedini, M., & Baldauf, D. (2021). Structure, function and connectivity fingerprints of the frontal eye field versus the inferior frontal junction: A comprehensive comparison. European Journal of Neuroscience, 54(4), 5462–5506. https://doi.org/10.1111/ejn.15393

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Bedini & Baldauf (2021)

The human prefrontal cortex contains two prominent areas, the frontal eye field and the inferior frontal junction, that are crucially involved in the orchestrating functions of attention, working memory and cognitive control.
In contrast to early visual areas, where all these cortical features are generally well aligned, and inter-individual differences are small, leading to a reliable way to parcel the underlying brain structures (Abdollahi et al., 2014; Sereno et al., 1995), in the PFC studies show that the alignment between cortical features becomes less apparent, and even the relative spatial arrangement of brain areas can sometimes vary substantially between individuals (Eickhoff, Yeo, & Genon, 2018). Thus, to understand the modular organization of the PFC, a multimodal approach capable of combining information about all the most relevant cortical properties becomes crucial (Glasser et al., 2016; Van Essen et al., 2019).

results:

We found remarkable differences in how these regions relate to sensory domains and visual topography, top-down and bottom-up spatial attention, spatial versus non-spatial (i.e., feature- and object-based) attention and working memory and, finally, the multipledemand system
The cytoarchitecture of the FEF is dysgranular. This region is part of BA6 and, to a lesser extent, of BA8. Its chemoarchitecture segregates it from the superior and the middle frontal gyrus. The cytoarchitecture of the IFJ is also dysgranular. This region lies in BA6, BA8 and BA44. Its receptor fingerprint segregates it from the ventral 44d. Receptorarchitecture also allows to segregate the IFJ in two distinct subregions.
The FEF is localized ventral to the junction of the sPCS and the SFS. The IFJ is localized dorsal to the junction of the iPCS with the IFS.
The FEF and IFJ are both primarily selective for visual information, but only the FEF contains a full topographic map of contralateral space.
The FEF is reached by the terminations of the SLF1 and SLF2. In contrast, we speculate that the IFJ may be reached by the terminations of the SLF2 and SLF3, thus suggesting partially segregated anatomical pathways from the plPFC to posterior parietal and temporoparietal cortices. The FEF is one of the core regions of the DAN, whereas the IFJ is part of the frontoparietal network. Meta-analytic connectivity modelling reveals three main co-activation patterns in the left IFJ, including a pattern related to attentional control. (SLF=superior longitudinal fasciculus)
according to the recent resting-state fMRI network partition by Ji et al. (2019; whose nodes are in turn based on the MMP1 parcellation), the FEF is part of the cingulo-opercular network, and the IFJp is part of the frontoparietal network, whereas the IFJa is part of a newly defined language network.
Although both areas are positioned near the output layer of the cognitive system, based on the involvement of the IFJ in encoding stimulus-response mappings according to novel task rules (Muhle-Karbe et al., 2017), and in a variety of other highlevel cognitive operations (Assem et al., 2020; Brass et al., 2005), it could be argued that the IFJ may encode information at a higher level of abstraction compared with the FEF (reviewed in Section 3.3). This would be consistent with the relatively recent emergence of the IFJ along the evolutionary path of the primate species compared with the more ancient dorsal pathway’s regions (Caminiti et al., 2015; Mars, Sotiropoulos, et al., 2018).
In their model, the FEF and IFJ show sensitivity to the stimulus context and sensory domain (spatial vs. verbal) and are hence hypothesized to be under the control of the cMFG and IFS, respectively (Nee & D’Esposito, 2016). In an updated version of this hierarchical model of cognitive control, Badre and Nee (2018) place the FEF and IFJ in the sensory-motor control areas that allow the maintenance of goal-related information to control movement in a domain-specific way; thus, although they are embedded in different information processing streams, they seem to be localized within the same gradient of the rostro-caudal axis. The authors also hypothesize that lateral areas could be similarly influenced by motivational factors that are propagated from the dorsomedial PFC at a comparable gradient in the PFC hierarchy (Badre & Nee, 2018). This suggestion parallels developments from the last decade in cognitive models of attention, which began to incorporate distinct forms of attentional biases stemming from learning processes and motivational factors (Anderson, 2019; Awh et al., 2012; Macaluso & Doricchi, 2013). It is however still unknown how these signals shape activity in the PFC (a possibility that we suggest should be investigated in future studies), and how the FEF and IFJ dynamically interact with subcortical and thalamic structures to achieve efficient control of behaviour (Halassa & Kastner, 2017; White et al., 2017).

attention:

attention The FEF and IFJ are both involved in top-down attention and show evidence of sustained activity in response to a cue. However, IFJ activity profile is more context dependent and influenced by bottom-up factors as well. The role of the IFJ could be of modulating DAN activity according to the current task demands and of toggling between DAN and VAN activities. (DAN=Dorsal Attention Network, VAN=Ventral Attention Network)

FEF

To date, the FEF has been the subject of hundreds of studies both in monkeys and in humans (reviewed in Petit & Pouget, 2019, Tehovnik et al., 2000, and Vernet et al., 2014). Despite the considerable efforts of the neuroscientific community to characterize the FEF, this region’s structure, function and connectivity in humans are often debated and are not yet fully understood.
They reported that several chemoarchitectonic features could segregate FEF from rostral regions in the middle frontal gyrus (MFG) and superior frontal gyrus. Their findings indicated that FEF is at a point of transition between the granular and agranular cortices in the vicinity of the superior PCS (sPCS).
In a single case ex vivo study, Schmitt et al. (2005) found that cytoarchitecture differentiates two aspects of the putative FEF localized in an area of 2 mm parallel to the lateral convexity and an area of 8 mm in the depth of the PCS. This study also reported that, according to cytoarchitectonic criteria, FEF is for the most part localized in BA6.
The FEF is predominantly involved in processing spatial information, mediating the set of overlapping functions of covert spatial attention, oculomotor control and spatial working memory.

IFJ:

The IFJ, in contrast, came under the spotlight of the neuroscientific community only much more recently. According to Sundermann and Pfleiderer (2012), although this region has been the object of many neuroimaging studies investigating various components of cognitive control, task-switching and working memory, researchers have often missed reporting the IFJ as a segregated brain region. The IFJ was first described with the current label in a series of influential studies by Brass, Derrfuss, von Cramon and colleagues (Brass & von Cramon, 2002, 2004; Derrfuss et al., 2004, 2005; see also Bunge et al., 2003, and Sylvester et al., 2003, for a converging characterization of the function of the IFJ; reviewed in Brass et al., 2005) and implicated in a cognitive control network (Cole & Schneider, 2007). In recent years, the IFJ has generated increased interest due to its involvement in a surprising variety of high-level cognitive functions, such as top-down visual attention (Baldauf & Desimone, 2014), working memory (Zanto et al., 2010) and the implementation of novel task instructions (Muhle-Karbe et al., 2017), thus firmly positioning it within the multiple-demand system of the brain (Assem et al., 2020; Duncan, 2010; Fedorenko et al., 2013).
Although the IFJ is not explicitly reported in their second study, we can speculate that this area corresponds to what the authors identify as BA6, BA44 and, to a lesser extent, area BA9/46v.
sharp change in cytoarchitecture and chemoarchitecture occurs in a region that corresponds to the functionally defined IFJ. The area analysed belongs to BA8, BA6 and BA44.
recent studies using MVPA revealed that the IFJ is involved in processing non-spatial information (i.e., in feature- and object-based attention and working memory tasks). The analysis of effective connectivity has also allowed to identify the IFJ as the source of modulation of feature-based attention and working memory encoding signals.
Several studies have now reported that the IFJ (and in particular, the IFJp) belongs to the core multipledemand system. There are also indications that the IFJa and FEF may display partial multipledemand characteristics, although this possibility needs to be further researched.

IFJa:

An additional analysis using contrasts with weaker cognitive demands in the working memory and relational reasoning tasks identified additional foci in the FEF and anterior IFJ (IFJa), among others. This suggests that these regions may display partial multiple-demand characteristics and that this possibility may need further scrutiny.

IFJp:

Interestingly, both the area IFJp (activated by the relational reasoning and the math task contrasts) and the area i6-8 (activated by all three task contrasts and preferentially by the working memory task) that lies immediately anterior to the FEF were included in the core multiple-demand system.

history:

In conclusion, several papers have now reported the involvement of the IFJ in the multiple-demand system, thus reinforcing the hypothesis that this area may have a broader role in cognition compared with the FEF. This idea is consistent with the view that the visuospatial attention system is evolutionarily older and its organization is well preserved in primates (Caminiti et al., 2015), whereas the vlPFC, and its projections to the temporooccipital cortex, might underlie the emergence of more complex human behaviours

VAN:

a right-lateralized ventral attention network (VAN), with inferior frontal gyrus (IFG) and the temporoparietal junction (TPJ) as primary nodes, was hypothesized to be involved in the automatic reorienting of attention to external (salient) stimulation (Corbetta & Shulman, 2002).

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Bedini & Baldauf (2021)

Bedini & Baldauf (2021)

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