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The Visual Analysis of Emotional Actions

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SOCIAL NEUROSCIENCE, 2006, 1(1) 63Á/74 The visual analysis of emotional actions Arieta Chouchourelou Rutgers University Á/ Newark Campus, Newark, NJ, USA Toshihiko Matsuka Stevens Institute of Technology, W.J. Howe School of Technology Management, Hoboken, NJ, USA Kent Harber and Maggie Shiffrar Rutgers University Á/ Newark Campus, Newark, NJ, USA Is the visual analysis of human actions modulated by the emotional content of those actions? This question is motivated by a consideration of the neuroanatomical connections between visual and emotional areas. Specifically, the superior temporal sulcus (STS), known to play a critical role in the visual detection of action, is extensively interconnected with the amygdala, a center for emotion processing. To the extent that amygdala activity influences STS activity, one would expect to find systematic differences in the visual detection of emotional actions. A series of psychophysical studies tested this prediction. Experiment 1 identified point-light walker movies that convincingly depicted five different emotional states: happiness, sadness, neutral, anger, and fear. In Experiment 2, participants performed a walker detection task with these movies. Detection performance was systematically modulated by the emotional content of the gaits. Participants demonstrated the greatest visual sensitivity to angry walkers. The results of Experiment 3 suggest that local velocity cues to anger may account for high false alarm rates to the presence of angry gaits. These results support the hypothesis that the visual analysis of human action depends upon emotion processes. Human observers demonstrate impressive visual 1988), emotional state (Atkinson, Dittrich, Gem- sensitivity to the actions of other people. This was mell, & Young, 2004) and gender (Troje, 2002). first documented in the classic studies of Johans- Psychophysical studies have identified two son (1973) in which he showed that the move- factors that define visual sensitivity to point-light ments of a few points were sufficient to readily displays of human action. One of these is motor generate compelling percepts of human action. experience. Visual sensitivity to human action Such point-light displays are traditionally con- varies as a function of the observer’s own motor structed by attaching luminous points to the main experience with those actions (Knoblich & Flach, joints of a moving actor. The actor’s movements 2001; Jacobs, Pinto, & Shiffrar, 2004). For exam- are filmed so that only the moving points are ple, observers demonstrate greater visual sensi- visible. While such displays are highly degraded, tivity to point-light displays of their own actions observers are able to rapidly and accurately than to the actions of their friends. Because perceive a point-light actor’s action (Johansson, people have the most motor experience, and little 1973), intent (Runeson & Frykolm, 1983), social visual experience, with their own actions, this dominance (Montepare & Zebrowitz-McArthur, heightened capacity for self-recognition indicates Correspondence should be addressed to: Arieta Chouchourelou, Department of Psychology, Rutgers University, Newark, NJ 07102, USA. E-mail: [email protected] This work was funded by NIH grant NEI12300. # 2006 Psychology Press Ltd www.psypress.com/socialneuroscience DOI:10.1080/17470910600630599 64 CHOUCHOURELOU ET AL. that motor processes contribute to action percep- significant anatomical abnormalities have been tion (Loula, Prasad, Harber, & Shiffrar, 2005). found in the STS of autistic children (Boddaert A second important contributor to the recog- et al., 2004; Waiter, Williams, Murray, Gilchrist, nition of human movement is visual experience. Perrett, & Whiten, 2005). Finally, observation of The more one sees a particular action, the greater static images of fearful whole-body expressions is one’s visual sensitivity to point-light depictions of associated with enhanced activity in the STS and that action (Jacobs & Shiffrar, 2005). Indeed, in other action representation and preparation sensory experience is key to the perception of the areas (De Gelder, Snyder, Greve, Gerard, Hadji- self as a social entity (Decety & Chaminade, khani, 2004). 2003). Neurophysiological data support the im- The hypothesis that the visual analysis of portance of visual experience in action percep- human action within the STS may be modulated tion. Single-cell recordings in nonhuman primates by the emotional content of that action is and functional neuroimaging studies with humans consistent with the numerous feedback and indicate that the superior temporal sulcus feed-forward connections between the STS and (STS) is selectively responsive to human motion the amygdala (Adolphs, 1999; Baron-Cohen, (Beauchamp, Lee, Haxby, & Martin, 2002; 1995; Brothers, 1997). For example, the amygda- Perrett, Rolls, & Caan, 1982; Puce & Perrett, loid nuclei are an important part of the limbic 2003). STS activity is strongly associated with the system (Felleman & Van Essen, 1991; Jones & perception of point-light displays of human action Powell, 1970) and play a critical role in the but not moving objects or random motion assessment of the emotional content of percep- (Bonda, Petrides, Ostry, & Evans, 1996; Gross- tual stimuli (Adolphs, 1999; Brothers, 1997). STS man et al., 2000; Oram & Perrett, 1996). Im- projections account for a significant proportion of portantly, STS activity is modulated by the visual the visual input to the amygdala (Amaral, experience that observers gain from watching Behniea, & Kelly, 2003; Iwai & Yukie, 1987; point-light actions (Grossman, Blake, & Kim, Iwai, Yukie, Wantanabe, Hikosaka, Suyama, & 2004). Thus, both perceptual sensitivity and STS Ishikawa, 1990). Furthermore, projections from activity to human motion are influenced by visual the amygdala to the STS are considerable experience. (Amaral et al., 2003). The goal of the current research is to examine Increasingly, amygdala function is understood whether an additional factor, namely, emotional as an appraiser of the potential threat or danger processes, also shape visual sensitivity to human posed by ‘‘incoming’’ stimuli (Amaral et al., 2003; action. Behavioral findings indicate that human Sato, Yoshikawa, Kochiyama, & Matsumura, observers can accurately recognize distinct emo- 2004). Such a position is consistent with observed tions portrayed in the whole body movements of deficits in ‘‘emotional reactivity’’ (Amaral, 2003). point-light actors (Atkinson et al., 2004; Clarke, For example, rhesus monkeys sustaining bilateral Bradshaw, Field, Hampson, & Rose, 2005; amygdaloid lesions do not react appropriately to Dittrich, Troscianko, Lea, & Morgan, 1996). potentially dangerous social situations (Amaral, Moreover, emotion recognition is best when 2003). Extensive work on rodents (LeDoux, 1995; point-light actors are presented as naturally Davis & Whalen, 2001) and some sporadic interacting couples (Clarke et al., 2005). This primate work (Kalin, 1993; Kluver & Bucy, suggests that social and emotional processes 1938) further highlight the role of the amygdala may significantly influence the visual analysis of (and their removal) in fear, fear conditioning and human movement. phobia development. Human data from lesion The potential impact of emotional processes and functional imaging studies strongly confirm on action perception is further suggested by amygdala function in perceiving and reacting to several neurophysiological findings. First, STS fear (Whalen, Shin, McInerney, Fischer, Wright, activity appears to be heightened for potentially & Rauch, 2001; Whalen et al., 2004). The threatening, and thus fear-inducing, actions amygdala has also been implicated in the percep- (Wheaton, Pipingas, Silberstein, & Puce, 2001). tion of other emotions (e.g., Adolphs & Tranel, Furthermore, STS activity is modulated by an 2004; Breiter et al., 1996; Yang et al., 2002). observed actor’s intent in normal observers (Jel- Broader amygdaloid activation may be asso- lema & Perrett, 2003; Saxe, Xiao, Kovacs, Perrett, ciated with the processing of potential threat & Kanwisher, 2004) but not in autistic observers during conditions of reduced attention at the (Pelphrey, Morris, & McCarthy, 2005). Indeed, expense of response specificity (Anderson, VISUAL ANALYSIS OF EMOTIONAL ACTIONS 65 Christoff, Panitz, De Rosa, & Gabrieli, 2003). this and all of the studies reported here were This idea ties in well with the view of reviewed and approved by the Rutgers University the amygdala as an orchestrating factor in the IRB. organization of withdrawal-related behaviors (Adolphs, 2002; Adolphs & Tranel, 2004; Apparatus. All stimuli were displayed on a 14- Anderson, Spencer, Fulbright, & Phelps, 2000). inch DellTM screen with a refresh rate of 60 Hz TM Consistent with this, amygdala activation in and a 1024/768 pixel resolution. A Dell response to emotional stimuli is rapid (Oya, Pentium computer controlled monitor output. Kawasaki, Howard, & Adolphs, 2002) and may Experimental design and control were pro- not require conscious awareness of or attention to grammed in MicrosoftTM Visual Basic 6.0. Motion a stimulus (Whalen, Rauch, Etcoff, McInerney, Builder 5.0 by KaydaraTM was used in all stages of Lee, & Jenike, 1998; Vuilleumier, Armony, movie processing and editing. Gaits were tracked Driver, & Dolan, 2001). with a ReActor motion capture system from Taken together, neurophysiological data sup- Ascension Technology Corporation. This appara- port the existence of tight connections
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