Startle modulation by affective faces

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.     

Affective startle modulation in anticipation and perception

Startle modulation was investigated as participants first anticipated and then viewed affective pictures in order to determine whether affective modulation of the startle reflex is similar in these different task contexts. During a 6-s anticipation period, a neutral light cue signaled whether the upcoming picture would portray snakes, erotica, or household objects; at the end of the anticipatory period, a picture in the signaled category was viewed for 6 s. Male participants highly fearful of snakes were recruited to maximize emotional arousal during anticipation and perception. Results indicated that the startle reflex was potentiated when anticipating either unpleasant (phobic) or pleasant (erotic) pictures, compared to neutral stimuli, whereas during perception, reflexes were potentiated when viewing unpleasant stimuli, and reduced when viewing pleasant pictures. The startle reflex is modulated by hedonic valence in picture perception, and by emotional arousal in a task context involving picture anticipation.     

Flashing a smile: Startle eyeblink modulation by masked affective faces

Affective faces are important stimuli with relevance to healthy and abnormal social and affective information processing. The aim of this study was to investigate the effect of brief presentations of affective faces on attention and emotional state across the time course of stimulus processing, as indexed by startle eyeblink response modulation. Healthy adults were presented with happy, neutral, and disgusted male and female faces that were backward masked by neutral faces. Startle responses were elicited at 300, 800, and 3,500 ms following stimulus presentation to probe early and late startle eyeblink modulation, indicative of attention allocation and emotional state, respectively. Results revealed that, at 300 ms, both face expression and face gender modulated startle eyeblink response, suggesting that more attention was allocated to masked happy compared to disgusted female faces, and masked disgusted compared to neutral male faces. There were no effects of either face expression or face gender on startle modulation at 800 ms. At 3,500 ms, target face expression did not modulate startle, but male faces elicited larger startle responses than female faces, indicative of a more negative emotional state. These findings provide a systematic investigation of attention and emotion modulation by brief affective faces across the time course of stimulus processing.     

The psychophysiology of social anxiety: Emotional modulation of the startle reflex during socially-relevant and -irrelevant pictures

The present study examined affective processes of social anxiety (SA) through emotional modulation of the startle reflex. Eighty-four high and low trait socially anxious undergraduates viewed socially-relevant and socially-irrelevant pleasant, neutral, and unpleasant pictures, and acoustic startle probes were presented during pictures and the inter-trial interval. Startle was potentiated during unpleasant compared to pleasant stimuli, but this valence modulation did not reliably vary between groups or socially-relevant and -irrelevant stimuli. However, when participants were categorized based on public-speaking fears rather than general SA symptoms, the high fear group demonstrated reliable valence modulation, whereas the low fear group did not. These findings are interpreted within the context of the broader literature suggesting that the specificity of fear in SA may influence psychophysiological reactivity.     

Sensation seeking and startle modulation by physically threatening images

The potential moderating effect of sensation seeking on anxious reactivity to threatening experiences was assessed using the affective modulation of startle-blink paradigm. Startle blinks, as measured by electromyographic (EMG) activity in response to loud (100 dB) white-noise stimuli, were elicited during the presentation of positive, neutral, and threatening visual images. Unlike participants low in sensation seeking who showed blink potentiation during threatening versus neutral images, participants high in sensation seeking showed equal magnitudes of startle to neutral and threatening images. The results suggest that individuals high compared with low on sensation seeking are less anxiously reactive to physically threatening visual stimuli. No attenuation in startle magnitude was elicited by positive images among low or high sensation seekers suggesting that the positive images employed in the current study were not arousing enough to activate the appetitive arousal system.     

The effects of contextual threat and anxiety on affective startle modulation

The startle reflex is attenuated and potentiated when participants are viewing pleasant and unpleasant images, respectively. Research demonstrates that threatening contexts also potentiate startle, but it remains unclear how a threatening context might impact startle modulation to emotional images, especially as a function of trait anxiety. The present study measured startle reactivity while 43 participants viewed pleasant, unpleasant, and neutral images across conditions of threat-of-shock and safety (i.e., no shock). Compared to neutral images, startle was potentiated during unpleasant images and attenuated during pleasant images. Threat-of-shock potentiated startle during all picture types, suggesting that threat-of-shock broadly sensitized the defensive system but did not change affective modulation of startle. Lastly, higher levels of trait anxiety were associated with less startle potentiation during unpleasant images across both conditions—a finding in line with previous research demonstrating deficient threat mobilization in response to unpleasant stimuli among highly anxious individuals.     

Startle reflex modulation during threat of shock and “threat” of reward

During threat of shock, the startle reflex is potentiated, suggesting modulation by defensive mobilization. To determine whether startle potentiation is specific to aversive anticipation, startle reflexes were measured in the context of either aversive or appetitive anticipation in a between‐subject study. Participants wore a device on the wrist that could deliver electrical shock (n = 49), or vibrotactile stimulation indicating monetary reward (n = 48). Cues signaling “threat” or “safe” periods were presented alone, or accompanied by presentation of affective and neutral pictures on half of the trials. Results indicated that the startle reflex was significantly potentiated when anticipating either shock or reward, compared to safe periods, both when no picture was presented, as well as during picture viewing. The difference between threat and safety in both reflex magnitude and skin conductance changes was larger for those anticipating shock, suggesting that the aversive context was more motivationally engaging. The pattern of reflex modulation as a function of picture valence varied under threat and safety, but was identical in the shock and reward groups, consistent with a hypothesis that anticipation of either aversive or appetitive events prompts heightened perceptual vigilance, potentiating the acoustic startle reflex.     

The effect of emotionally valenced eye region images on visuocortical processing of surprised faces

In this study, we presented pictorial representations of happy, neutral, and fearful expressions projected in the eye regions to determine whether the eye region alone is sufficient to produce a context effect. Participants were asked to judge the valence of surprised faces that had been preceded by a picture of an eye region. Behavioral results showed that affective ratings of surprised faces were context dependent. Prime‐related ERPs with presentation of happy eyes elicited a larger P1 than those for neutral and fearful eyes, likely due to the recognition advantage provided by a happy expression. Target‐related ERPs showed that surprised faces in the context of fearful and happy eyes elicited dramatically larger C1 than those in the neutral context, which reflected the modulation by predictions during the earliest stages of face processing. There were larger N170 with neutral and fearful eye contexts compared to the happy context, suggesting faces were being integrated with contextual threat information. The P3 component exhibited enhanced brain activity in response to faces preceded by happy and fearful eyes compared with neutral eyes, indicating motivated attention processing may be involved at this stage. Altogether, these results indicate for the first time that the influence of isolated eye regions on the perception of surprised faces involves preferential processing at the early stages and elaborate processing at the late stages. Moreover, higher cognitive processes such as predictions and attention can modulate face processing from the earliest stages in a top‐down manner.     

Fearfulness and Startle Potentiation during Aversive Visual Stimuli

Recent experimental research suggests an association between negative affect and potentiation of the human startle reflex, as well as enhancement of this effect among fearful compared to low fear subjects. In the present study, 32 undergraduates were selected for high or low total Fear Survey Schedule scores. Acoustic startle probes were presented while subjects received warned presentations of aversive and neutral photographic slides. High fear but not low fear subjects showed potentiated short-latency cardiac acceleration and blink magnitude, and reduced blink latency, during aversive compared to neutral slides. These results support the hypothesis that affective modulation of startle is enhanced among high fear compared to low fear subjects. Considered in the context of prior findings, the results suggest that this individual difference effect generalizes across psychophysiological components of the startle reflex and diverse procedures for manipulating affect.     

Startle potentiation in aversive anticipation: evidence for state but not trait effects

The present study was undertaken to determine whether aversiveness contributes to startle potentiation in anticipation of affective pictures above and beyond the effects of emotional arousal. Further, participants high in trait anxious apprehension, which is characterized by worry about the future, were expected to show especially pronounced anticipatory startle responses. Startle blink reflex was measured during warning stimuli that predicted the valence of ensuing aversive/unpleasant, pleasant, or neutral pictures. Startle magnitude was larger in anticipation of aversive than of pleasant pictures and smallest in anticipation of neutral pictures. Enhanced startle potentiation was not found in anxious apprehension subjects. These data suggest that the aversive nature of stimuli contribute to the potentiation of startle above and beyond the effects of emotional arousal, which may be a universal phenomenon not modulated by individual differences.     

A startle-probe methodology for investigating the effects of active avoidance on negative emotional reactivity

This study introduces a new methodology for investigating the impact of active avoidance and behavioral control on defensive emotional reactivity using the startle reflex. A between-groups yoked design was devised that permitted manipulation of participants’ perception of control over an aversive event (loud noise) while precisely controlling motor activity and noxious stimulation. Startle responses to tactile (airpuff) probes were compared during threat/performance trials and neutral trials. Results conclusively demonstrated cross-modal startle potentiation in the context of a continuous motor performance task. Also, consistent with prior research, heart rate increased with perceived control. However, behavioral control per se did not appear to mitigate defensive emotion as indexed by startle potentiation. These findings indicate that other parameters may mediate the efficacy of active coping in addition to control, and that the startle probe paradigm can provide a valuable tool for investigating these parameters in future research.     

Threat sensitivity as assessed by automatic amygdala response to fearful faces predicts speed of visual search for facial expression

It has been argued that the amygdala represents an integral component of a vigilance system that is primarily involved in the perception of ambiguous stimuli of biological relevance. The present investigation was conducted to examine the relationship between automatic amygdala responsivity to fearful faces which may be interpreted as an index of trait-like threat sensitivity and spatial processing characteristics of facial emotions. During 3T fMRI scanning, pictures of human faces bearing fearful, angry, and happy expressions were presented to 20 healthy volunteers using a backward masking procedure based on neutral facial expressions. Subsequently, a computer-based face-in-the-crowd task using schematic face stimuli was administered. The neural response of the (right) amygdala to masked fearful faces correlated consistently with response speed to negative and neutral faces. Neither amygdala activation during the masked presentation of angry faces nor amygdala activation during the presentation of happy faces was correlated with any of the response latencies in the face-in-the-crowd task. Our results suggest that amygdala responsivity to masked facial expression is differentially related to the general visual search speed for facial expression. Neurobiologically defined threat sensitivity seems to represent an important determinant of visual scanning behaviour.     

Effects of stress and shock anticipation on prepulse inhibition of the startle reflex

The effects of shock anticipation and attention to external stimuli on prepulse inhibition (PPI) were compared. In the threat-of-shock experiment, acoustic startle stimuli were presented with and without prepulses when aversive shocks were or were not anticipated. In the control experiment, startle and prepulse stimuli were delivered during periods with attended or ignored external stimuli. In the threat-of-shock experiment, startle was potentiated (fear-potentiated startle) and PPI was increased by shock anticipation. A gradual reduction in the overall PPI throughout the experiment was also found. In the control experiment, only PPI was increased in the attend condition. The PPI level remained constant throughout the experiment. The increase in PPI in the threat and attend conditions may have resulted from an increase in the general level of alertness that facilitated the processing of the prepulse. The gradual decrease in PPI in the threat experiment was hypothesized to result from a progressive deficit in sensory functioning due to the stressful nature of repeated shock anticipation.     

Startle effects on saccadic responses to emotional target stimuli

Startle stimuli elicit various physiological and cognitive responses. This study investigated whether acoustic startle stimuli affect saccadic reactions in an emotional pro‐ or antisaccade task. Startle probes were presented either 500 ms before or simultaneous with an imperative stimulus that indicated whether a saccade towards or away from positive, neutral, or negative peripheral target pictures had to be performed. Valence interacted with saccade direction according to an approach‐avoidance pattern of gaze behavior, with delayed prosaccades to negative targets and antisaccades away from positive targets. Acoustic startle stimuli preceding the presentation of peripheral target pictures speeded up the initiation saccades, irrespective of stimulus valence. Results indicate a speeding of cognitive‐motor processing by preceding startle stimuli.     

Defense reactions to interoceptive threats: A comparison between loaded breathing and aversive picture viewing

Human fear research has mostly applied exteroceptive stimuli to induce fear. Interoceptive sensations however can also be very threatening and play a major role in a number of anxiety disorders. In this study, we compared affective responses to inspiratory resistive loads with those to aversive pictures. During repeated administrations of two loads, a light and a moderate one, and five aversive pictures we measured electrodermal activity, startle blink responses, subjective fear and ratings on valence, arousal and dominance. Results indicate that loads evoke affective reactions comparable or stronger than those evoked by the pictures. Startle data did not follow this pattern with an absence of startle potentiation during the moderate load, suggesting that fear potentiated startle does not occur when the background aversive stimulus is of an interoceptive nature.     

Resting heart rate variability and the startle reflex to briefly presented affective pictures

We have previously shown that persons with low HRV showed potentiated startle responses to neutral stimuli. In the present study we replicated our prior findings and extended them to examine the effects of HRV on the startle magnitude to pictures that were presented outside of conscious awareness. A total of 85 male and female students were stratified via median split on their resting HRV. They were presented pictures for 6 s or for 30 ms. Results indicated that the high HRV group showed the context appropriate startle magnitude increase to unpleasant foreground. The low HRV group showed startle magnitude increase from pleasant to neutral pictures but no difference between the neutral and unpleasant pictures. This pattern of results was similar for the 30 ms and the 6 s conditions. These results suggest that having high HRV may allow persons to more efficiently process emotional stimuli and to better recognize threat and safety signals.     

Startle during backward evaluative conditioning is not modulated by instructions

Instructions highlighting that backward conditional stimuli (CSs) stop unconditional stimuli (USs) result in their acquiring valence opposite to that of the US on explicit measures of valence. We assessed whether such instructions would influence startle blink modulation in the same way. Two groups were presented with concurrent forward and backward evaluative conditioning (CS-US-CS) using cartoon aliens as CSs, and pleasant, neutral, and unpleasant sounds as USs. Startle magnitude was measured during conditioning and valence ratings were assessed after conditioning. Participants in the “start-stop” instructions group (n = 41) were instructed to learn whether CSs started or stopped US presentations, while participants in the “observe” instructions group (n = 41) were told to pay attention to the stimuli as they would be asked questions about them after the experiment. In the start-stop instructions group backward CSs paired with positive USs were rated as less pleasant than backward CSs paired with neutral and negative USs (contrast effect), whereas ratings of backward CSs did not differ in the observe instructions group. Startle magnitude was larger during backward CSs paired with positive USs in comparison to CSs paired with neutral or negative USs in both instruction groups. Startle blink modulation was unaffected by instructions, suggesting that startle indexes the emotional state at the time of probe presentation rather than CS valence based on propositional information about the function of the CS.     

Escaping aversive exposure

This research examined human defensive reactivity when exposure to an aversive event could be escaped but not entirely avoided. Prolonged visual cues indicated whether exposure to an upcoming aversive (i.e., disgusting) picture could be terminated after onset (escaped) or not, or that a neutral go signal would appear. Acoustically elicited startle reflexes were measured during each cue interval, as were cardiac and skin conductance activity. Early in the cuing interval, startle reflexes were potentiated during both escape and inescapable exposure trials, compared to the simple motor context. Later in the interval, reflexes remained potentiated for both escapable and inescapable trials, with potentiation further enhanced when aversive exposure could not be escaped compared to when exposure could be escaped. Heart rate deceleration in the cuing interval indicated increased vigilance when preparing any (escape or neutral) action, whereas skin conductance responding indicated enhanced sympathetic action mobilization particularly in an escape context. These data suggest that startle reflexes engaged in an escape context reflect both motor‐related response inhibition and aversive potentiation, and they indicate that defensive motivation is engaged whenever aversive exposure is guaranteed, regardless of whether it can be escaped or not.     

The persistence of socially instructed threat: Two threat‐of‐shock studies

Learning to anticipate threat is crucial in guiding protective behavior. In classical conditioning, single trial learning can result in long‐lasting fear associations. To examine whether threat learned through social communication is equally stable, an instructed fear paradigm was used with two repeated sessions on 1 day (Study 1; N = 43) and with separate sessions on 3 consecutive days (Study 2; N = 30). Startle EMG, skin conductance level (SCL), and self‐report data were recorded during alternating periods of instructed threat and safety. Within 1 day, threat‐potentiated startle was present across sessions but threat‐enhanced SCL decreased (Study 1). Across days, threat effects subsided with different timing for startle EMG, SCL, and self‐report (Study 2). The present findings are a laboratory analog for the persistence of socially transmitted fear, which can be amazingly resistant to extinction (e.g., in specific phobias) even in the absence of aversive experiences.     

The development of fear learning and generalization in 8-13 year-olds

The current study examined developmental changes in fear learning and generalization in 40 healthy 8–13 year‐olds using an aversive conditioning paradigm adapted from Lau et al. [Lau et al. [2008] Journal of the American Academy of Child and Adolescent Psychiatry 47:94–102]. In this task, the conditioned stimuli (CS+/CS?) are two neutral female faces, and the unconditioned stimulus is a fearful, screaming face. The second phase of the study also included a generalization stimulus (GS): a 50% blend of the CS± faces. The eye‐blink startle reflex was utilized to measure defensive responding. Patterns of fear learning and generalization were qualified by child age. Older children demonstrated greater fear learning (i.e., larger startle during CS+ than CS?) than younger children. In addition, older children exhibited the typical pattern of generalization observed in adults, whereas younger children did not. Finally, fear learning also related to contingency awareness; only children who correctly identified the CS+ demonstrated fear‐potentiated startle to the CS+. Clinical implications and future directions are discussed. © 2011 Wiley Periodicals,Inc. Dev Psychobiol 54: 675–684, 2012.