Elsevier

Biological Psychology

Volume 83, Issue 1, January 2010, Pages 37-40
Biological Psychology

Startle modulation by affective faces

https://doi.org/10.1016/j.biopsycho.2009.10.001Get rights and content

Abstract

Startle reflex modulation by affective pictures is a well-established effect in human emotion research. However, much less is known about startle modulation by affective faces, despite the growing evidence that facial expressions robustly activate emotion-related brain circuits. In this study, acoustic startle probes were administered to 37 young adult participants (20 women) during the viewing of slides from the Pictures of Facial Affect set including neutral, happy, angry, and fearful faces. The effect of expression valence (happy, neutral, and negative) on startle magnitude was highly significant (p < .001). Startle reflex was strongly potentiated by negative expressions (fearful and angry), however, no attenuation by happy faces was observed. A significant valence by gender interaction suggests stronger startle potentiation effects in females. These results demonstrate that affective facial expressions can produce significant modulation of the startle reflex.

Introduction

Startle reflex modulation by an affective foreground is a well-established experimental phenomenon in human emotion research. Acoustic startle reflex is an automatic, obligatory defensive response triggered by abrupt and loud noise. Studies of animals (Davis, 1989) and humans (Grillon, 2002) have shown that the startle reflex is potentiated in the presence of a conditioned fear stimulus. Converging evidence suggests that the intensity of the startle reflex depends on the ongoing motivational and affective state of the subject, such that the reflex is facilitated by aversive/defensive motivational states and attenuated by appetitive states (Grillon and Baas, 2003, Lang et al., 1998, Vrana et al., 1988).

The neurobiological substrates of startle modulation by emotion have been extensively studied in animals using fear-potentiated startle paradigms (reviewed in Koch and Schnitzler, 1997). These studies showed that the primary acoustic startle pathway in the brain stem is modulated through direct projections by the secondary pathway, in which the amygdala plays the central role. Thus, the degree of startle reflex modulation by various stimuli can serve as an objective measure of the extent to which particular stimuli activate (or suppress) the neural circuitry underlying the two basic motivational systems, aversive and appetitive, and two emotional states, pleasant and unpleasant (Koch and Schnitzler, 1997, Lang et al., 1998).

Human startle experiments have largely relied on affective pictures as stimulus material for emotion induction, particularly images from the International Affective Picture System (IAPS) (Lang et al., 1999). The IAPS pictures have been shown to produce a robust modulation of the startle reflex, such that reflex magnitude was the largest during unpleasant, intermediate during neutral, and smallest during pleasant pictures (Cuthbert et al., 1996, Lang et al., 1998, Vrana et al., 1988). This valence effect has been replicated using other kinds of stimuli such as emotional sounds (Bradley and Lang, 2000) as well as conditioned stimuli in fear conditioning paradigms (Grillon, 2002). Individual differences in affective modulation of startle have been associated with personality characteristics and psychopathology (Corr et al., 1996, Grillon and Baas, 2003, Vaidyanathan et al., 2009). In contrast to the extant literature on startle modulation by affective pictures, affective facial expressions have been little used in startle experiments, although several important features of facial images such as structural homogeneity and uniform perceptual complexity over a range of emotional expression, as well as low novelty can provide a more rigorous control for picture characteristics that are unrelated to emotional content.

The neural mechanisms of face perception are being increasingly understood (reviewed in Haxby et al., 2002, Posamentier and Abdi, 2003). Studies of amygdala lesions (Adolphs et al., 2005, Adolphs et al., 1995) and direct electrical stimulation of the amygdala suggest that this structure plays an important role in the processing of facial emotional expressions by humans and non-human primates. Neuroimaging studies have demonstrated a robust activation of the amygdala by emotional facial expressions, especially by fearful faces (Breiter et al., 1996, Morris et al., 1996). Two functional neuroimaging studies directly compared brain activation patterns induced by facial expressions and affective pictures from the IAPS. Hariri et al. (2002) found that fearful and angry facial expressions produce a significantly stronger response in the amygdala compared to the IAPS pictures. Moreover, facial stimuli also produced a greater autonomic (skin conductance) response than affective pictures in the same study. Another study found that both affective faces and IAPS pictures recruit similar brain regions but also noted a greater activation of some regions by affective faces (Britton et al., 2006).

It should be noted, however, that the relation between threatening facial expressions and amygdala activation is not universal: amygdala activation has also been reported for other facial expressions and by faces in general (Breiter et al., 1996), and reduced amygdala responses were observed in tasks requiring explicit emotion recognition, in contrast to increased amygdala activation in tasks involving implicit processing of facial expressions (Critchley et al., 2000). These exceptions notwithstanding, available evidence indicates that affective facial expressions, particularly fearful expressions produce a robust activation of the amygdala during passive viewing (i.e., in the absence of explicit processing demands).

The few studies that have examined the effects of the valence of facial expressions on startle modulation have reported mixed results. In a study by Balaban (1995), a startle probe was administered while 5-month-old infants were shown photographic slides of unfamiliar adult faces with happy, neutral, and angry expressions. There was a linear relationship between startle response magnitude and slide valence: the response was augmented during exposure to the angry faces and was reduced during exposure to the happy faces relative to neutral faces. However, a study of 4–8-year-old children did not find differences in startle responses during viewing of angry and neutral faces (Waters et al., 2008). The few studies that used adult samples have also provided mixed findings. One abstract (Alpers and Adolph, 2006) reported no effect of expression valence (i.e., angry and happy vs. neutral) on startle modulation. In another study, pictures of smiling and crying infants failed to produce startle modulation in young adults (Spangler et al., 2001). A recent study by Hess et al. (2007) in which happy, neutral, and angry faces were administered to a group of young adults, also produced mixed results. No main effect of facial expression was found, but there was a significant interaction between expression and the actor's sex. However, possible effects of viewer's gender were not reported.

We are aware of only one published startle reflex study in which both angry and fearful faces were administered (Springer et al., 2007). In one experiment, the authors found a significant effect of facial expression on startle magnitude, where angry but not fearful faces produced an increased eyeblink response compared to all other expressions. A replication experiment using the same paradigm with different facial material failed to show a significant main effect of facial expression on startle, but in pairwise comparisons, angry faces still showed significant differences from other expressions. It should be noted, however, that the startle stimuli were administered on every trial and thus were fully predictable to the subjects, which is not typical for startle modulation studies (Springer et al., 2007).

Taken together, the available evidence does not seem to support the notion that affective facial expression can modulate the startle response in adults as consistently as affective pictures. However, it is important to note that only one study included faces with fearful expression.

The goal of this study was to examine startle reflex modulation by affective faces in a community-based sample of young adults. We hypothesized that affective facial expression would influence the startle magnitude in the direction predicted by the theory of motivation and emotion proposed by Lang et al. (1993), i.e., that the startle response will be potentiated by expressions with negative emotional valence (fearful and angry) and attenuated by positively valenced (happy) faces. In addition, we intended to examine possible effects of the observer's sex on startle modulation by affective faces.

Section snippets

Participants

Thirty-nine individuals including 18 men (18–22 years; M age ± SD: 19.4 ± 1.2 years) and 21 woman (18–21 years; M age ± SD: 19.0 ± 1.3 years) participated in the study. Participants were recruited through state birth records as part of a larger population-based epidemiological study of twins and families and were included in the present study after screening for exclusion criteria. The criteria included a history of head trauma with loss of consciousness for more than 5 min, known history of epilepsy,

Results

Grand-averaged startle EMG responses, as well as average startle magnitudes for different expression conditions are shown in Fig. 1. RM ANOVA indicated that the main effect of Valence was highly significant (F(2,70) = 11.6, p < .001, effects size η2 = .249, Greenhouse–Geisser epsilon (ɛ) =0.97; here and in the following analyses p-values are Greenhouse–Geisser corrected.

There was no significant main effect of Gender on the magnitude of startle responses (F(1,35) = 1.22, η2 = .03, p = .28). However, there

Discussion

The results of the present study demonstrate that affective facial expressions can modulate the startle reflex in young adults. However, the data only partially support our original hypothesis, because modulation effects were limited to startle potentiation by emotionally negative expressions, and startle was not suppressed by positive emotional expression. Furthermore, this effect was significant in female participants only.

The present finding differs from previous studies that did not find a

Acknowledgements

This work was supported by the grants DA00421 and DA018899 from the National Institute on Drug Abuse. The authors thank Dr. Sean Kristjansson and two anonymous reviewers for their helpful comments on the manuscript.

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