Perception of emotional expressions is independent of face selectivity in monkey inferior temporal cortex

Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 05/2008; 105(14):5591-6. DOI: 10.1073/pnas.0800489105
Source: PubMed


The ability to perceive and differentiate facial expressions is vital for social communication. Numerous functional MRI (fMRI) studies in humans have shown enhanced responses to faces with different emotional valence, in both the amygdala and the visual cortex. However, relatively few studies have examined how valence influences neural responses in monkeys, thereby limiting the ability to draw comparisons across species and thus understand the underlying neural mechanisms. Here we tested the effects of macaque facial expressions on neural activation within these two regions using fMRI in three awake, behaving monkeys. Monkeys maintained central fixation while blocks of different monkey facial expressions were presented. Four different facial expressions were tested: (i) neutral, (ii) aggressive (open-mouthed threat), (iii) fearful (fear grin), and (iv) submissive (lip smack). Our results confirmed that both the amygdala and the inferior temporal cortex in monkeys are modulated by facial expressions. As in human fMRI, fearful expressions evoked the greatest response in monkeys-even though fearful expressions are physically dissimilar in humans and macaques. Furthermore, we found that valence effects were not uniformly distributed over the inferior temporal cortex. Surprisingly, these valence maps were independent of two related functional maps: (i) the map of "face-selective" regions (faces versus non-face objects) and (ii) the map of "face-responsive" regions (faces versus scrambled images). Thus, the neural mechanisms underlying face perception and valence perception appear to be distinct.

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Available from: Roger B Tootell, May 22, 2014
    • "In contrast, a recent study has shown that intranasal administration of oxytocin in monkeys reduced the activity in face-responsive ROIs to fearful and threatening faces, but not to neutral or appeasing faces, suggesting a selective effect of oxytocin on the perception of negative, but not positive, facial expressions (Liu et al. 2015). Our findings, in terms of both the differential valence effects and the differential modulation of the effective connectivity, suggest a modulation in macaques based not on the dichotomy of positive (neutral and appeasing) versus negative (fearful and threatening) facial expressions, but rather on the classification of facial expression along 3 axes: dominance (threatening), avoidance (fearful), and affiliation (appeasing) (Hadj-Bouziane et al. 2008). Thus, our study provides empirical evidence for dynamic alterations in neural coupling during the perception of behaviorally relevant facial expressions that are vital for social communication and interaction. "
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    ABSTRACT: In humans and monkeys, face perception activates a distributed cortical network that includes extrastriate, limbic, and prefrontal regions. Within face-responsive regions, emotional faces evoke stronger responses than neutral faces ("valence effect"). We used fMRI and Dynamic Causal Modeling (DCM) to test the hypothesis that emotional faces differentially alter the functional coupling among face-responsive regions. Three monkeys viewed conspecific faces with neutral, threatening, fearful, and appeasing expressions. Using Bayesian model selection, various models of neural interactions between the posterior (TEO) and anterior (TE) portions of inferior temporal (IT) cortex, the amygdala, the orbitofrontal (OFC), and ventrolateral prefrontal cortex (VLPFC) were tested. The valence effect was mediated by feedback connections from the amygdala to TE and TEO, and feedback connections from VLPFC to the amygdala and TE. Emotional faces were associated with differential effective connectivity: Fearful faces evoked stronger modulations in the connections from the amygdala to TE and TEO; threatening faces evoked weaker modulations in the connections from the amygdala and VLPFC to TE; and appeasing faces evoked weaker modulations in the connection from VLPFC to the amygdala. Our results suggest dynamic alterations in neural coupling during the perception of behaviorally relevant facial expressions that are vital for social communication.
    No preview · Article · Jan 2016 · Cerebral Cortex
    • "Quite surprisingly, when using dynamic facial expressions, Zhu et al. (2012) observed an additional face-responsive region lateral to the face patches (Figure 2). Although significant progress has been made in understanding the neuronal response characteristics of monkey face patches (Freiwald & Tsao, 2010; Freiwald et al., 2009; Hadj-Bouziane et al., 2008; Issa & DiCarlo, 2012; Pinsk et al., 2009; Tsao et al., 2006), little is known about their topographic organizations. Relating face patches to retinotopic areas, however , has implications for the neural computations they perform (Freiwald & Tsao, 2010; Halgren et al., 1999). "
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    ABSTRACT: We review recent phase-encoded retinotopic mapping data and discuss the spatial relationship between the retinotopically organized monkey cortex and feature- and category-selective clusters. Four areas sharing a foveal representation, V4t, FST, MT, and MSTv, constitute the MT field map cluster. Rostral to V4, areas V4A, OTd, PITv, and PITd also share a foveal representation, again forming a cluster. Concerning the retinotopic organization of face patches, we observed a gradual shift from posterior patches that are retinotopically organized to anterior, nonretinotopic patches. Feature- and category-selective regions in the nonretinotopic IT cortex form repetitive supermodules, each containing face, body, and color patches.
    No preview · Chapter · Dec 2015
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    • "The present study showed that emotional expressions could be decoded from the pattern of activity in the FFA. Contrary to many models of face processing (Haxby et al., 2000; O'Toole et al., 2002; Winston et al., 2004), these findings support claims that the FFA is involved in processing emotional expressions (Ganel et al., 2005; Tsuchiya et al., 2008; Fox et al., 2009a; Xu and Biederman, 2010; Kawasaki et al., 2012) and is consistent with evidence that emotion selective neurons are distributed throughout the ventral temporal lobes (Hadj-Bouziane et al., 2008; Morin et al., 2010). Although classification accuracy in the FFA was low, the present findings are similar with previous studies examining the patterns evoked by other within-category distinctions with MVPA (Eger et al., 2008; Op de Beeck et al., 2010). "
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    ABSTRACT: It is widely assumed that the fusiform face area (FFA), a brain region specialized for face perception, is not involved in processing emotional expressions. This assumption is based on the proposition that the FFA is involved in face identification and only processes features that are invariant across changes due to head movements, speaking and expressing emotions. The present study tested this proposition by examining whether the response in the human FFA varies across emotional expressions with functional magnetic resonance imaging and brain decoding analysis techniques (n = 11). A one vs. all classification analysis showed that most emotional expressions that participants perceived could be reliably predicted from the neural pattern of activity in left and the right FFA, suggesting that the perception of different emotional expressions recruit partially non-overlapping neural mechanisms. In addition, emotional expressions could also be decoded from the pattern of activity in the early visual cortex (EVC), indicating that retinotopic cortex also shows a differential response to emotional expressions. These results cast doubt on the idea that the FFA is involved in expression invariant face processing, and instead indicate that emotional expressions evoke partially de-correlated signals throughout occipital and posterior temporal cortex.
    Full-text · Article · Oct 2013 · Frontiers in Human Neuroscience
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