Dynamic Facial Expressions Evoke Distinct Activation in the Face Perception Network: a Connectivity Analysis Study
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Dynamic Facial Expressions Evoke Distinct Activation in the Face Perception Network: A Connectivity Analysis Study 1 1 2 Elaine Foley , Gina Rippon , Ngoc Jade Thai , Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/2/507/1777324/jocn_a_00120.pdf by MIT Libraries user on 17 May 2021 Olivia Longe1, and Carl Senior1 Abstract ■ Very little is known about the neural structures involved in the identified as insensitive to motion or affect but sensitive to the vi- perception of realistic dynamic facial expressions. In the present sual stimulus, the STS, identified as specifically sensitive to motion, study, a unique set of naturalistic dynamic facial emotional ex- and the amygdala, recruited to process affect. Measures of effec- pressions was created. Through fMRI and connectivity analysis, a tive connectivity between these regions revealed that dynamic fa- dynamic face perception network was identified, which is demon- cial stimuli were associated with specific increases in connectivity strated to extend Haxby et al.ʼs [Haxby, J. V., Hoffman, E. A., & between early visual regions, such as the inferior occipital gyrus Gobbini, M. I. The distributed human neural system for face per- and the STS, along with coupling between the STS and the amyg- ception. Trends in Cognitive Science, 4, 223–233, 2000] distrib- dala, as well as the inferior frontal gyrus. These findings support uted neural system for face perception. This network includes the presence of a distributed network of cortical regions that me- early visual regions, such as the inferior occipital gyrus, which is diate the perception of different dynamic facial expressions. ■ INTRODUCTION Real-life faces are dynamic by nature, particularly when Based largely on findings from behavioral observations, expressing emotion. However, much of the research on Bruce and Youngʼs(1986)influential“functional model face perception and emotion recognition to date has used of face recognition” has served as a general framework static stimuli of faces, such as stimuli from the Ekman and for the study of face perception for the last 30 years. Cen- Friesen (1976) collection. These posed static facial stimuli tral to this model is the notion that analysis of facial ex- do not reflect the unique temporal dynamics and infor- pression and identity proceed independently of each mation available from seeing a moving face in the real other. Further evidence to support the functional divi- world and thus do not allow a complete description of sion between facial expression and identity processing the neural correlates of natural face perception to be comes from neuropsychological studies of prosopagnosic made. Dynamic stimuli would offer a more suitable means patients, who can interpret facial expressions correctly but of examining the neural basis of realistic natural face per- are unable to correctly identify familiar faces (Humphreys, ception. Behavioral studies using dynamic facial stimuli Donnelly, & Riddoch, 1993). Haxby, Hoffman, and Gobbini have shown that motion plays an important role in facili- (2000) later modified this model to provide a neurologi- tating judgments of gender (Hill & Johnston, 2001) and cal description of face perception, wherein they describe also contributes to identity judgments (Christie & Bruce, a “distributed human neural system for face perception.” 1998; Pike, Kemp, Towell, & Phillips, 1997). In addition, This model, like the earlier Bruce and Young (1986) model, judgments of facial affect are influenced by changing the proposes distinct pathways for the visual analysis of fa- velocity of an expressing face, suggesting that the dynamic cial identity and expression. The perception of identity, display of facial expressions provides unique temporal in- the invariant aspect of a face, occurs in a ventral pathway formation about the expressions, which is not available in that involves the lateral fusiform gyrus (FG), whereas the static displays (Kamachi et al., 2001). Dynamic facial ex- STS is part of the dorsal pathway that is implicated in pressions of emotion have been shown to facilitate emo- the processing and representation of changeable facial tion recognition compared with their static counterparts features. The extended system then incorporates addi- (Sato, Kochiyama, Yoshikawa, Naito, & Matsumara, 2004; tional brain regions to support further face processing, LaBar, Crupain, Voyvodic, & McCarthy, 2003), possibly be- such as emotion recognition. cause of additional information encoded in facial action patterns, which is not present in static stimuli (Wehrle, 1Aston University, 2University of Bristol Kaiser, Schmidt, & Scherer, 2000). © 2011 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 24:2, pp. 507–520 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00120 by guest on 26 September 2021 However, very little is known about the neural struc- before projecting to the STS. This implies that the STS tures involved in the perception of realistic dynamic facial may play a role in facial identification when identification expressions, as Haxby et al.ʼs (2000) distributed face per- can be gleaned from dynamic facial signatures. They also ception model was mainly defined using evidence de- suggest that the STS and FG may be connected via the rived from static images of faces, with the exception of middle temporal visual area MT, thus facilitating recognition Puce, Allison, Bentin, Gore, and McCarthy (1998). These through structure-from-motion processes. This is consis- static stimuli obviously represent impoverished displays tent with Sato et al. (2004), who report increased activa- lacking natural facial motion, which do not facilitate a tion in MTG to dynamic faces. In addition, Calder and Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/2/507/1777324/jocn_a_00120.pdf by MIT Libraries user on 17 May 2021 complete interrogation of the face perception network, Young (2005) recently used principle component analy- particularly the dorsal pathway which is implicated in sis to investigate the degree of separation between these the processing of facial dynamics. Although perception two pathways and found that facial expressions and identity of static face stimuli does elicit activation in the dorsal canbecodedwithinasinglemultidimensional framework STS region, it is believed to result from implied rather than rather than relying on separate independent codes. From overt biological motion (Fairhall & Ishai, 2007; Haxby, this, it would appear that the roles of the FG and STS may Hoffman, & Gobbini, 2002). Naturally, dynamic stimuli not be as dissociable and distinct as previously thought. should therefore be considered to understand the com- One way to examine the degree of separation and func- plete neurology of ecologically valid face perception. tional interplay between the FG and STS, and the other Recent brain imaging studies have investigated the neu- neural structures involved in face processing, is to use con- ral network underlying the processing of dynamic face stim- nectivity analysis. Rather than looking solely at isolated uli. For example, Kilts, Egan, Gideon, Ely, and Hoffman regional effects, connectivity analysis examines the interac- (2003) carried out a PET study using dynamic and static tions between brain regions. It also provides a means of face stimuli and found increased activation in STS in re- assessing the extent to which the same brain regions sup- sponse to dynamic compared with static face stimuli, along port different operations depending on task-dependent with greater activation in the amygdala and hippocampus. network connections (Friston et al., 1997). Recently, Fairhall In an fMRI study LaBar et al. (2003) reported increased and Ishai (2007) used fMRI and connectivity analysis activation in FG, ventromedial pFC, and STS to dynamic (dynamic causal modeling) to examine the interactions expressions of emotion compared with neutral. Addition- between the different regions of the face perception net- ally, Sato et al. (2004) carried out an fMRI study using work with static face stimuli. They presented photographs dynamic gray-scaled morphed stimuli of fearful and happy of unfamiliar, famous, and emotional faces in a passive faces, dynamic mosaics of scrambled faces, and static con- viewing task and found that all faces exerted a strong trols. They found increased activation in the inferior oc- and significant influence on the effective connectivity be- cipital gyrus (IOG), middle temporal gyrus (MTG), STS, tween IOG and both FG and STS. Emotional and famous and FG to dynamic facial expressions compared with the faces significantly modulated the coupling between IOG dynamic and static controls. These findings are generally and FG, but not between IOG and STS. They also found consistent with Haxby et al.ʼs (2000) distributed model that the FG exerted influences on the amygdala, inferior of face perception and show considerable overlap in acti- frontal gyrus (IFG), and OFC. They concluded from this vation patterns in response to different face processing that the extraction of the changeable aspects of face stim- tasks. However many of these studies (Sato et al., 2004; uli, within limbic and prefrontal regions, is enabled via the LaBar et al., 2003) have used morphed stimuli, which were FG in the ventral pathway rather than the STS. However, constructed from static stimuli and may represent artificial this may be because of the fact that static images of faces motion.