Elsevier

Brain Research Bulletin

Volume 67, Issues 1–2, 30 September 2005, Pages 87-93
Brain Research Bulletin

Face perception is mediated by a distributed cortical network

https://doi.org/10.1016/j.brainresbull.2005.05.027Get rights and content

Abstract

The neural system associated with face perception in the human brain was investigated using functional magnetic resonance imaging (fMRI). In contrast to many studies that focused on discreet face-responsive regions, the objective of the current study was to demonstrate that regardless of stimulus format, emotional valence, or task demands, face perception evokes activation in a distributed cortical network. Subjects viewed various stimuli (line drawings of unfamiliar faces and photographs of unfamiliar, famous, and emotional faces) and their phase scrambled versions. A network of face-responsive regions was identified that included the inferior occipital gyrus, fusiform gyrus, superior temporal sulcus, hippocampus, amygdala, inferior frontal gyrus, and orbitofrontal cortex. Although bilateral activation was found in all regions, the response in the right hemisphere was stronger. This hemispheric asymmetry was manifested by larger and more significant clusters of activation and larger number of subjects who showed the effect. A region of interest analysis revealed that while all face stimuli evoked activation within all regions, viewing famous and emotional faces resulted in larger spatial extents of activation and higher amplitudes of the fMRI signal. These results indicate that a mere percept of a face is sufficient to localize activation within the distributed cortical network that mediates the visual analysis of facial identity and expression.

Introduction

Face perception is a highly developed visual skill in primates. Converging evidence from neuropsychology, neurophysiology, and cognitive development indicates that face perception may be mediated by a specialized neural system in the brain [9]. In the past decade, with the advent of functional brain imaging techniques, it has been shown that face perception consistently activates a region in the lateral fusiform gyrus [17], [30], [33], [46]. It has been proposed that the ‘fusiform face area’ is a module specialized for face perception [30]. This region, however, also responds significantly to other categories of objects (e.g., houses, chairs, and tools), thus ruling out its status as a face “module” [4], [21], [27], [28]. Furthermore, it has been shown that neural activation within the fusiform face-selective region is modulated by expertise [12], [13], attention [37], visual imagery [24], [26], [36], and emotion [51]. These findings suggest that the response to faces in extrastriate cortex is not the result of a mere hierarchical, bottom-up, ‘feature’ analysis, but is modulated by top-down effects, likely originating in parietal and frontal regions.

The recognition of identity is based on invariant facial features, while changeable aspects of the face, such as speech-related movement and expression, contribute to social communication. When looking at faces, we automatically perceive the gender, expression, and mood. Processing the information gleaned from the faces of others therefore requires the integration of activation within a network of cortical regions. Numerous face perception studies have reported activation not only in the fusiform gyrus, but also in other regions in the visual cortex, limbic system, and prefrontal cortex [24], [25]. Haxby et al. have suggested that face perception is mediated by a distributed neural network in the human brain and have proposed a new model that includes a ‘core’ system and an ‘extended’ system [20]. The core system is comprised of the inferior occipital gyrus (IOG), fusiform gyrus (FG), and the superior temporal sulcus (STS). The ventral regions (IOG and FG) mediate the recognition of individuals. The more dorsal regions (STS) participate in the perception of social signals such as the direction of gaze, speech-related lip movements, and facial expressions [22], [41]. The extended system includes the amygdala and the insula, which mediate the perception of emotional facial expressions, in particular fear, anger, and disgust [2], [25], [34], [39]. Additionally, it has been shown that assessment of facial attractiveness evoked activation in prefrontal cortex [35] and the reward circuitry, in particular the amygdala and nucleus accumbens [1]. It is important to note, however, that not a single study has shown activation within all regions of both the core and the extended systems.

The aim of this study was to test whether activation in regions of the distributed neural system associated with face perception could be localized with a simple task, namely passive viewing of various face stimuli. Previous studies focused on activation within the fusiform gyrus [16], or compared activation evoked by specific face stimuli, such as familiar versus unfamiliar faces [44]. We adopted a more general approach, instructing subjects to view different face stimuli (line drawings of unfamiliar faces and photographs of unfamiliar, famous, and emotional faces) and analyzing all face-responsive regions in the brain. Our results indicate that viewing faces evokes activation in a distributed network that includes multiple, bilateral regions in the visual cortex, limbic system, and prefrontal cortex. Within this network, the response to famous and emotional faces is stronger than the response to unfamiliar faces.

Section snippets

Subjects

Thirteen healthy, drug-free volunteers (eight males, five females, mean age 26 ± 4 years) with normal vision participated in the study. All subjects gave written informed consent prior to the examination.

Stimuli and task

Subjects were presented with four different types of face stimuli: black and white line drawings of unfamiliar faces, and gray scale photographs of unfamiliar, famous, and emotional faces. Phase scrambled versions of these faces were used as visual baseline. The scrambled pictures were generated

Activation evoked by visual perception of faces

Visual perception of faces, as compared with scrambled faces, significantly activated the IOG, FG, STS, amygdala, hippocampus, IFG, and the OFC (Fig. 1). Within these face-responsive regions, bilateral activation was found in all subjects (see Table 1 for cluster size and brain atlas coordinates), however stronger responses were observed in the right hemisphere. In the IOG, FG, STS, and IFG this hemispheric asymmetry was manifested by larger clusters of activation (P < 0.0001) and higher t-values

Discussion

The neural response evoked by passive viewing of faces was investigated using fMRI. Activation was found in a network of face-responsive regions, including the IOG, FG, STS, amygdala, hippocampus, IFG, and OFC. Within these regions, all stimuli (line drawings of unfamiliar faces and photographs of unfamiliar, famous, and emotional faces) evoked significant activation, with stronger responses in the right hemisphere. Furthermore, the response to famous and emotional faces was stronger than the

Acknowledgements

We thank Victor Candia, Daniel Kiper, Kevan Martin, and Elena Yago for their comments on previous drafts, Philips Medical systems for their continuous support, and the ETH Zurich program of Strategic Excellence Projects (TH 7/02-02).

References (52)

  • T. Landis et al.

    Are unilateral right posterior cerebral lesions sufficient to cause prosopagnosia? Clinical and radiological findings in six additional patients

    Cortex

    (1986)
  • C. Ranganath et al.

    Medial temporal lobe activity associated with active maintenance of novel information

    Neuron

    (2001)
  • E.T. Rolls

    The functions of the orbitofrontal cortex

    Brain Cogn.

    (2004)
  • P. Vuilleumier et al.

    Effects of attention and emotion on face processing in the human brain: an event-related fMRI study

    Neuron

    (2001)
  • A.D. Wagner et al.

    Recovering meaning: left prefrontal cortex guides controlled semantic retrieval

    Neuron

    (2001)
  • A. Aharon et al.

    Beautiful faces have variable reward value: fMRI and behavioral evidence

    Neuron

    (2001)
  • L.L. Chao et al.

    Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects

    Nat. Neurosci.

    (1999)
  • A.R. Damasio et al.

    Prosopagnosia: anatomic basis and behavioral mechanisms

    Neurology

    (1982)
  • De Renzi

    Prosopagnosia in two patients with CT scan evidence of damage confined to the right hemisphere

    Neuropsychologia

    (1986)
  • R.J. Dolan et al.

    Dissociating prefrontal and hippocampal function in episodic memory encoding

    Nature

    (1997)
  • K.J. Friston et al.

    Statistical parametric maps in functional imaging: a general linear approach

    Hum. Brain Mapp.

    (1995)
  • I. Gauthier et al.

    Expertise for cars and birds recruits brain areas involved in face recognition

    Nat. Neurosci.

    (2000)
  • I. Gauthier et al.

    Activation of the middle fusiform ‘face area’ increases with expertise in recognizing novel objects

    Nat. Neurosci.

    (1999)
  • M.L. Gorno-Tempini et al.

    Identification of famous faces and buildings: a functional neuroimaging study of semantically unique items

    Brain

    (2001)
  • M.L. Gorno-Tempini et al.

    The neural systems sustaining face and proper-name processing

    Brain

    (1998)
  • K. Grill-Spector et al.

    The fusiform face area subserves face perception, not generic within-category identification

    Nat. Neurosci.

    (2004)
  • Cited by (0)

    View full text