The improbable simplicity of the fusiform face area

doi:10.1016/j.tics.2012.03.003

Trends in Cognitive Sciences

Volume 16, Issue 5, May 2012, Pages 251-254

https://doi.org/10.1016/j.tics.2012.03.003 Get rights and content

The fusiform face area (FFA) is described as an easily identifiable module on the fusiform gyrus. However, the organization of face-selective regions in ventral temporal cortex (VTC) is more complex than this prevailing view. We highlight methodological factors contributing to these complexities and the extensive variability in how the FFA is identified. We suggest a series of constraints to aid researchers when defining any functionally specialized region with a pleasing realization: anatomy matters.

Introduction

Nearly a decade ago, Semir Zeki discussed improbable visual areas in the primate brain [1] (see also [2]). In his critique, Zeki questioned the accuracy and theoretical logic of defining extrastriate cortical areas based on partial retinotopic maps as well as the variable parcellation criteria used across research groups. However, his discussion stopped at human V4 and did not extend into VTC where high-level visual representations for faces, body parts, objects, and places are located (Figure 1a). We apply Zeki's concerns of accuracy and parcellation criteria to the FFA and ask: Does the FFA exist in the way it is depicted in journals, textbooks, and everyday media – as a ‘blueberry-sized’ module on the fusiform gyrus [3]? To address this question, we first discuss various depictions of the FFA and highlight factors contributing to this variability. We then summarize a recent organizational framework developed to reconcile the many faces of the FFA and to accommodate complexities of VTC organization more generally.

Section snippets

Functional localizer approach identifies the FFA but is it time for an update?

The classic work by Kanwisher and colleagues has been highly influential – ushering in nearly 2500 citations in the past 15 years – for introducing the elegant functional localizer method to the field of functional magnetic resonance imaging (fMRI) and for convincingly demonstrating the existence of face-selective regions in the human brain [4]. The localizer approach first identifies a region of interest in individual subjects with one set of data (e.g. comparing fMRI responses to images of

FFA: multiple and discontinuous, smoothed and simplified, or hindered by artifacts

The complexity begins when experimenters run an FFA localizer only to find approximately eight face-selective clusters across ventral and lateral aspects of the temporal lobe depending on the scanning parameters used 4, 6, 7, 10 (VTC shown in Figure 1b–d). Often, more than one face-selective region is detected on the fusiform gyrus (Figure 1b–d) 4, 6, 7, 8, 9, 10, 11. Aligning with the influential theoretical model, researchers commonly combine all fusiform face-selective regions into the FFA (

Solution: anatomy matters

Improved scanning methods enable consistent localization of several face-selective regions in VTC when considering their spatial organization relative to surrounding regions and neuroanatomical landmarks 8, 9 (Figure 2a). Such an approach reveals that face-selective regions are discontinuous and organized within and across subjects as opposed to discontinuous and variable as commonly reported. Specifically, face-selective regions have a periodic nature where each region is approximately 10 mm in

Concluding remarks

It is not improbable that neural responses specific to faces cluster in the human brain. However, it is unlikely that face-selective responses cluster in a fashion consistent with the present description of the FFA. Instead, methodological factors such as spatial smoothing and fMRI artifacts contribute to the complexity and changing presence of face-selective responses. Zeki [1] concluded his paper with the notion that traditional and even conservative criteria have considerable merit when

Acknowledgments

This work was supported by NSF BCS grant 0920865 and Round 4 Bio-X IIP award. We thank Melina Uncapher, Nick Davidenko, Alina Liberman, and three anonymous reviewers for helpful comments on prior versions of this manuscript.

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Neuroimaging and intracranial electrophysiological studies have consistently shown the largest and most consistent face-selective neural activity in the middle portion of the human right lateral fusiform gyrus (‘fusiform face area(s)’, FFA). Yet, direct evidence for the critical role of this region in face identity recognition (FIR) is still lacking. Here we report the first evidence of transient behavioral impairment of FIR during focal electrical stimulation of the right FFA. Upon stimulation of an electrode contact within this region, subject CJ, who shows typical FIR ability outside of stimulation, was transiently unable to point to pictures of famous faces among strangers and to match pictures of famous or unfamiliar faces presented simultaneously for their identity. Her performance at comparable tasks with other visual materials (written names, pictures of buildings) remained unaffected by stimulation at the same location. During right FFA stimulation, CJ consistently reported that simultaneously presented faces appeared as being the same identity, with little or no distortion of the spatial face configuration. Independent electrophysiological recordings showed the largest neural face-selective and face identity activity at the critical electrode contacts. Altogether, this extensive multimodal case report supports the causal role of the right FFA in FIR.
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Functionally and structurally distinct fusiform face area(s) in over 1000 participants
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The fusiform face area (FFA) is a widely studied region causally involved in face perception. Even though cognitive neuroscientists have been studying the FFA for over two decades, answers to foundational questions regarding the function, architecture, and connectivity of the FFA from a large (N>1000) group of participants are still lacking. To fill this gap in knowledge, we quantified these multimodal features of fusiform face-selective regions in 1053 participants in the Human Connectome Project. After manually defining over 4,000 fusiform face-selective regions, we report five main findings. First, 68.76% of hemispheres have two cortically separate regions (pFus-faces/FFA-1 and mFus-faces/FFA-2). Second, in 26.69% of hemispheres, pFus-faces/FFA-1 and mFus-faces/FFA-2 are spatially contiguous, yet are distinct based on functional, architectural, and connectivity metrics. Third, pFus-faces/FFA-1 is more face-selective than mFus-faces/FFA-2, and the two regions have distinct functional connectivity fingerprints. Fourth, pFus-faces/FFA-1 is cortically thinner and more heavily myelinated than mFus-faces/FFA-2. Fifth, face-selective patterns and functional connectivity fingerprints of each region are more similar in monozygotic than dizygotic twins and more so than architectural gradients. As we share our areal definitions with the field, future studies can explore how structural and functional features of these regions will inform theories regarding how visual categories are represented in the brain.
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The neural face perception network is distributed across both hemispheres. However, the dominant role in humans is virtually unanimously attributed to the right hemisphere. Interestingly, there are, to our knowledge, no imaging studies that systematically describe the distribution of hemispheric lateralization in the core system of face perception across subjects in large cohorts so far. To address this, we determined the hemispheric lateralization of all core system regions (i.e., occipital face area - OFA, fusiform face area - FFA, posterior superior temporal sulcus - pSTS) in 108 healthy subjects using functional magnetic resonance imaging (fMRI). We were particularly interested in the variability of hemispheric lateralization across subjects and explored how many subjects can be classified as right-dominant based on the fMRI activation pattern. We further assessed lateralization differences between different regions of the core system and analyzed the influence of handedness and sex on the lateralization with a generalized mixed effects regression model. As expected, brain activity was on average stronger in right-hemispheric brain regions than in their left-hemispheric homologues. This asymmetry was, however, only weakly pronounced in comparison to other lateralized brain functions (such as language and spatial attention) and strongly varied between individuals. Only half of the subjects in the present study could be classified as right-hemispheric dominant. Additionally, we did not detect significant lateralization differences between core system regions. Our data did also not support a general leftward shift of hemispheric lateralization in left-handers. Only the interaction of handedness and sex in the FFA revealed that specifically left-handed men were significantly more left-lateralized compared to right-handed males. In essence, our fMRI data did not support a clear right-hemispheric dominance of the face perception network. Our findings thus ultimately question the dogma that the face perception network – as measured with fMRI – can be characterized as “typically right lateralized”.
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Citation Excerpt :
In all these studies, connections are less dense – or reduced in connection strength/connectivity probability - between EVC and the FFA than between EVC and the spatially closer OFA (Gschwind et al., 2012; Wang et al., 2020). This appears to be the case also in the most recent study of Finzi et al.(2021), in which the FFA complex is divided in two clusters (pFus and mFus, after Weiner and Grill-Spector, 2010; or pFus-faces and mFus-faces; after Weiner and Grill-Spector, 2012, Fig.10) and the EVC holds direct connections with each of these clusters (in all participants in which these regions are successfully localized (Fig.6 in Finzi et al., 2021; see Fig.11&B here). Thus, despite the longer spatial distance between EVC and FFA than EVC and OFA, and the dominance of short-range fibers in the cortical face network overall (Wang et al., 2020), DTI studies considered together overwhelmingly support the early hypothesis of direct connections from EVC to the FFA complex (Rossion et al., 2003; Rossion, 2008, Figs.6 and 7), against a strict hierarchical view of the cortical face network.
Patient PS sustained her dramatic brain injury thirty years ago, in 1992, the same year as the first report of a neuroimaging study of human face recognition.The present paper complements the review on the functional nature of PS's prosopagnosia (part I), illustrating how her case study directly, i.e., through neuroimaging investigations of her brain structure and activity, but also indirectly, through neural studies performed on other clinical cases and neurotypical individuals, inspired and constrained neural models of human face recognition.In the dominant right hemisphere for face recognition in humans, PS's main lesion concerns (inputs to) the inferior occipital gyrus (IOG), in a region where face-selective activity is typically found in normal individuals (‘Occipital Face Area’, OFA).Her case study initially supported the criticality of this region for face identity recognition (FIR) and provided the impetus for transcranial magnetic stimulation (TMS), intracerebral electrical stimulation, and cortical surgery studies that have generally supported this view.Despite PS's right IOG lesion, typical face-selectivity is found anteriorly in the middle portion of the fusiform gyrus, a hominoid structure.This face-selective right ‘Fusiform Face Area’ (FFA) has been widely considered as the most important region for human face recognition.This finding led to the original proposal of direct anatomico-functional connections from early visual cortices to the FFA, bypassing the IOG/OFA , a hypothesis supported by further neuroimaging studies of PS, other neurological cases and neuro-typical individuals with original visual stimulation paradigms, data recordings and analyses.The proposal of a lack of sensitivity to face identity in PS's right FFA due to defective reentrant inputs from the IOG/FFA has also been supported by other cases, functional connectivity and cortical surgery studies.Overall, neural studies of, and based on, the case of prosopagnosia PS strongly question the hierarchical organization of the human neural face recognition system, supporting a more flexible and dynamic view of this key social brain function in our species.

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Trends in Cognitive Sciences

ForumThe improbable simplicity of the fusiform face area

Introduction

Section snippets

Functional localizer approach identifies the FFA but is it time for an update?

FFA: multiple and discontinuous, smoothed and simplified, or hindered by artifacts

Solution: anatomy matters

Concluding remarks

Acknowledgments

Trends Neurosci.

Neuroimage

Neuroimage

Neuron

Neuroscience. What's in a face?

Science

The fusiform face area: a module in human extrastriate cortex specialized for face perception

J. Neurosci.

Forum
The improbable simplicity of the fusiform face area