The shared signal hypothesis and neural responses to expressions and gaze in infants and adults

Abstract

Event-related potentials were recorded from adults and 4-month-old infants while they watched pictures of faces that varied in emotional expression (happy and fearful) and in gaze direction (direct or averted). Results indicate that emotional expression is temporally independent of gaze direction processing at early stages of processing, and only become integrated at later latencies. Facial expressions affected the face-sensitive ERP components in both adults (N170) and infants (N290 and P400), while gaze direction and the interaction between facial expression and gaze affected the posterior channels in adults and the frontocentral channels in infants. Specifically, in adults, this interaction reflected a greater responsiveness to fearful expressions with averted gaze (avoidance-oriented emotion), and to happy faces with direct gaze (approach-oriented emotions). In infants, a larger activation to a happy expression at the frontocentral negative component (Nc) was found, and planned comparisons showed that it was due to the direct gaze condition. Taken together, these results support the shared signal hypothesis in adults, but only to a lesser extent in infants, suggesting that experience could play an important role.

Early Binding of Gaze, Gesture, and Emotion: Neural Time Course and Correlates

“…The activation of the amygdala while observers perceived bodily expressions of anger replicates previous studies (Pichon et al, 2009) and supports its proposed role in the automatic detection of threat (Emery and Amaral, 2000;LeDoux, 2000;Amaral et al, 2003;Feinstein et al, 2011). Amygdala damage diminishes the brain's response to threatening faces at both the ϳ100 -150 and ϳ500 -600 ms time ranges (Rotshtein et al, 2010), and, in both infants and adults, the interaction between gaze direction and emotion takes place at ϳ200 -300 ms (Klucharev and Sams, 2004;Rigato et al, 2010). Furthermore, previous fMRI studies manipulating self-involvement during face perception revealed that facial expression and gaze direction are integrated in the medial temporal poles (Schilbach et al, 2006;Conty and Grèzes, 2012) or in amygdala (Adams and Kleck, 2003;Hadjikhani et al, 2008;NЈDiaye et al, 2009;Sato et al, 2010).…”

“…We confirm that activity within motorrelated cortical areas arises 150 -200 ms after the onset of a perceived action (Nishitani and Hari, 2002;Caetano et al, 2007;Tkach et al, 2007;Catmur et al, 2010) and that the interaction between gaze direction and emotion takes place at ϳ200 -300 ms (Klucharev and Sams, 2004;Rigato et al, 2010). However, in contrast to recent accounts of human amygdala function in social cue integration (Sander et al, 2007;NЈDiaye et al, 2009;Cristinzio et al, 2010;Sato et al, 2010), we found that emotional content is processed earlier within the amygdala and independently of other cues.…”

“…We thus confirmed that not only gaze direction and emotion but also body gesture are independently processed at early stages (Rigato et al, 2010) (Fig. 2).…”

“…The amygdala may thus sustain early binding of visually presented social signals. Electroencephalography (EEG) studies suggest that the interaction between emotion and gaze direction occurs at ϳ200 -300 ms (Klucharev and Sams, 2004;Rigato et al, 2010), but direct implication of the amygdala in such a mechanism has yet to be provided.…”

“…First, we analyzed the ERPs to identify the time course of early binding of social cues. We expected a temporal marker of their integration at ϳ200 ms (Klucharev and Sams, 2004;Rigato et al, 2010). Then, we quantified the parametric variation of self-involvement on the neural sources of the ERPs by combining the ERPs with fMRI data.…”