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.     

Startle modulation before, during and after exposure to emotional stimuli.

Although affective modulation of the startle reflex is a highly replicable effect, the majority of studies have administered startle probes during exposure to affective stimuli. To examine more comprehensively the temporal course of startle potentiation, we assessed blink modulation before, during and immediately after exposure to positive, negative and neutral pictures. During each trial, cues about the affective content of pictures were presented, after which acoustic startle probes were delivered either before picture onset, during picture onset or immediately after picture offset. As expected, we observed a linear relation between picture valence and startle amplitude during picture viewing. Surprisingly, startle amplitude was larger while anticipating pleasant and unpleasant pictures relative to neutral pictures. No significant effects were observed during the offset phase. These results indicate that startle modulation is conditional upon temporal factors linked to stimulus onset and offset.     

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.     

Postauricular reflexes elicited by soft acoustic clicks and loud noise probes: Reliability,prepulse facilitation,and sensitivity to picture contents

The startle blink reflex is facilitated during early picture viewing, then inhibited by attention during pleasant and aversive pictures compared to neutral pictures, and finally potentiated during aversive pictures specifically. However, it is unclear whether the postauricular reflex, which is elicited by the same loud acoustic probe as the startle blink reflex but enhanced by appetitive instead of defensive emotion, has the same pattern and time course of emotional modulation. We examined this issue in a sample of 90 undergraduates using serially presented soft acoustic clicks that elicited postauricular (but not startle blink) reflexes in addition to standard startle probes. Postauricular reflexes elicited by both clicks and probes correlated during food and nurturant contents, during which they were potentiated compared to neutral pictures, suggesting clicks effectively elicit emotionally modulated postauricular reflexes. The postauricular reflex was initially facilitated during the first 500 ms of picture processing but was larger during pleasant than neutral pictures throughout picture processing, with larger effect sizes during the latter half of picture processing. Across reflexes and eliciting stimuli, measures of emotional modulation had higher coefficient alphas than magnitudes during specific picture contents within each valence, indicating that only emotional modulation measures assess higher‐order appetitive or defensive processing.     

Modulation of spinal reflexes: Arousal, pleasure, action

The human startle reflex is reliably modulated by the affective valence of foreground pictures, with larger reflexes elicited when viewing unpleasant relative to pleasant scenes. If this modulation is due to priming of the defensive startle reflex by an aversive foreground, a different pattern should occur for a reflex that is not inherently defensive in nature. In the current study, affective modulation was investigated using the spinal tendinous (T) reflex, which is well documented as sensitive to differences in arousal and is involved in actions that are both appetitively and defensively motivated. As such, T reflexes elicited during unpleasant pictures were not expected to be augmented relative to those elicited in the context of pleasant pictures. Results showed that T reflexes were facilitated during processing of arousing stimuli – either pleasant or unpleasant relative to low-arousal neutral materials. These effects of emotional stimuli on T-reflex amplitude are consistent with the hypothesis that motivational priming underlies affective reflex modulation.     

Independence of valence modulation and prepulse inhibition of startle

This study sought to determine whether prepulse inhibition and valence modulation of startle are independent, both within and across individuals. Acoustic probes (105 dB) were delivered as 68 undergraduate s viewed pleasant, neutral, and unpleasant pictures. Weak acoustic stimuli (8 dB above background) preceded half of the probes by 120 ms. As expected, startles were larger during unpleasant than during pleasant pictures, and smaller on prepulse than no-prepulse trials. In general, valence modulation and prepulse inhibition of startle were unrelated. That is, prepulse inhibition was consistent across affective states, valence modulation did not differ between no-prepulse and prepulse trials, and valence modulation and prepulse inhibition effects were uncorrelated across individuals. Analysis of raw and percent modification scores generally led to similar conclusions. It is concluded that valence modulation and prepulse inhibition are independent startle modulatory phenomena, although this conclusion is tempered by a finding of poor internal consistency reliability for valence modulation.     

Modulation of the acoustic startle reflex by emotionally-toned film-clips.

It has been widely reported that the eyeblink component of the acoustic startle reflex can be modulated by emotionally-toned slide stimuli; pleasant slides reduce eyeblink amplitudes whereas unpleasant slides enhance them. The present study examines the modulation of the acoustic startle reflex by short (2-min) film-clips classified as pleasant, unpleasant or neutral, on the basis of subjective ratings. These film-clips were also evaluated with respect to their test-retest reliability in producing affective states as well as modulating startle reflexes. Overall, results showed significant reduction of startle during pleasant clips and augmentation during unpleasant clips. However, on first showing, one of the two unpleasant clips (a medical demonstration film depicting details of toe surgery) actually inhibited the startle reflex rather than augmented it. This is discussed in terms of the proposition that only stimuli which arouse fear can be guaranteed to augment startle; stimuli that are repulsive may produce perceptual and emotional 'blunting' that reduces startle amplitude.     

Emotional response in patients with frontal brain damage: effects of affective valence and information content

The authors investigated the role of the frontal lobes in the emotional response in 19 patients with brain damage and 23 control subjects. They studied the modulation of the startle blink reflex by affective pictures, and other autonomic responses. Patients showed a dissociation between the startle reflex and the affective valence ratings of the pictures, as a result of a low inhibition of the startle reflex by pleasant pictures. Pictures elicited lower skin conductance responses (SCRs) in patients than in controls, whereas the groups did not differ in the SCRs prompted by less significant acoustic stimuli. The findings point to the frontal lobe as a structure involved in the emotional response and in the physiological emotional arousal related to the complexity of the stimuli.     

Pictures as prepulse: Attention and emotion in startle modification

The effects of an emotional stimulus prepulse on probe startle response were examined here. Pleasant, neutral, and unpleasant pictures were viewed for 6 s, and an acoustic startle probe was presented either 300, 800, 1,300, or 3,800 ms after slide onset, or 300 or 3,800 ms after slide offset. Blink magnitude and onset latency demonstrated (a) an early (prepulse) inhibition effect in which reflexes elicited immediately after slide onset were smaller than reflexes elicited later in the viewing interval, and (b) affective modulation, in which unpleasant stimuli prompted larger reflexes than pleasant. Interactive effects of probe time and picture valence indicated attention/arousal effects early and pleasantness effects late in the picture interval. Effects of both attention and emotion can be simultaneously measured using this startle-probe paradigm, encouraging its use in both basic and clinical contexts.     

Probing picture perception: Activation and emotion

When acoustic startle probes are presented during picture viewing, the blink reflex is augmented for unpleasant foreground stimuli and reduced during pleasant stimuli. The present experiment assessed the hypothesis that this affect-Startle effect increases as pictures are judged to be more arousing. Eyeblinks elicited by startle probes of three different intensities were recorded while subjects viewed pictures varying in both pleasure (pleasant, neutral, and unpleasant) and arousal (low, moderate, and high). Both blink potentiation during unpleasant content and blink diminution during pleasant content were clearly strongest for picture contents high in arousal. The effect was present for all probe intensities tested.     

Emotion and motivated behavior: postural adjustments to affective picture viewing

Thirty-six participants (18 female, 18 male) viewed affective pictures to investigate the coupling between emotional reactions and motivated behavior. Framed within the biphasic theory of emotion, the three systems approach was employed by collecting measures of subjective report, expressive physiology, and motivated behavior. Postural adjustments associated with viewing affective pictures were measured. Results indicated sex-differences for postural responses to unpleasant pictures; an effect not found for pleasant and neutral picture contents. Females exhibited increased postural movement in the posterior direction, and males exhibited increased movement in the anterior direction, for unpleasant pictures. Subjective report of valence and arousal using the self-assessment manikin (SAM), and the startle eye-blink reflex were collected during a separate session, which replicated previous picture-viewing research. Specifically, participants rated pleasant pictures higher in valence and exhibited smaller startle responses compared to unpleasant pictures. Females also reported lower valence ratings compared to males across all picture contents. These findings extend our knowledge of motivated engagement with affective stimuli and indicate that postural responses may provide insight into sex-related differences in withdrawal behavior.     

Affective modulation of tactile startle

Two studies were conducted to investigate affective modulation of startle responses to unilateral tactile probes and to determine whether such modulation is lateralized. Right-handed undergraduates received airpuffs to the left or right temple while viewing pleasant, neutral, and unpleasant pictures. Side of probe presentation was varied between the two trial blocks of the experiment in Study 1 (n= 48) but varied randomly within trial blocks in Study 2 (n= 48). Primary results were consistent across studies. Replicating and extending the findings for acoustic probes, eyeblink responses to tactile probes were larger during unpleasant than during pleasant pictures. However, affective modulation of startle did not differ reliably between the two sides of probe presentation (sensory laterality) or the two sides of the response (motor lateralily) in either study or in a combined analysis.     

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.     

Addressing the specificity of affective startle modulation: fear versus disgust.

Previous research is equivocal regarding whether startle reflex eyeblink is specifically sensitive to the emotion of fear, or is more generally influenced by the valence dimension of emotion. Thirty-five undergraduate participants (17 male) viewed 60 pictures from five affective categories (pleasant, neutral, fear, disgust-blood, and disgust-other). Bilateral eyeblink EMG responses to acoustic startle probes were assessed during 2/3 of picture presentations, and 1/3 of intertrial intervals. Left corrugator and levator EMG responses to no-startle pictures were also examined. Supporting an emotional valence model of affective startle modulation, the startle potentiation effect was not specific to fear materials. In fact, women, but not men, had larger startles during disgust compared with fear pictures. Both corrugator and levator EMG responses were greater to disgust than fear stimuli. These findings limit the generalizability of corrugator as an index of all negative emotions and extend evidence for the specificity of levator to disgust.     

Affective modulation of the startle response in depression: influence of the severity of depression, anhedonia, and anxiety

BACKGROUND: The amplitude of the startle reflex response is known to be influenced by the concomitant presentation of affect-toned material--if it is positive affect-toned, the reflex is inhibited, and if it is negative affect-toned, the reflex is augmented. Abundant evidence demonstrates the utility of the affect-startle paradigm as a significant tool for measuring both positive and negative emotions. We applied this paradigm to study emotional reactivity in depression, particularly in relation to symptoms of depression, anhedonia, and anxiety. METHODS: Depressed patients (22) and controls (22) were shown a series of film clips, consisting of two clips with positive valence, two with negative valence, and two with relatively neutral valence. The startle response was measured in reaction to the acoustic startle-eliciting stimuli presented three times binaurally during each clip. RESULTS: Highly depressed and anhedonic patients, relative to controls, showed a reduced mood (self-ratings) and a lack of startle modulation in response to affective film clips whereas patients relatively low on depression/anhedonia displayed a reduced mood only with pleasant clips and a normal pattern of affective startle modulation. Anhedonia and depression were highly positively correlated but neither correlated with anxiety. Anxious patients displayed larger reflexes across all clips and showed a reduced mood modulation with pleasant, but not unpleasant, clips. LIMITATIONS: The large majority of patients was medicated with antidepressants which may have influenced the results. CONCLUSIONS. Reactivity to pleasant stimuli is diminished in patients suffering from low levels of depression and/or anhedonia, but reactivity even to unpleasant stimuli seems compromised at high levels of depression and/or anhedonia. Anxiety is associated with hyperstartle responding.     

State anxiety and affective physiology: effects of sustained exposure to affective pictures

Effects of sustained exposure to emotional stimuli on affective reactions and their recovery were examined to determine whether increasing exposure to a specific emotional content (e.g., unpleasant) cumulatively affects physiological responses; and whether motivational activation persists following sustained exposure. Participants viewed pleasant, neutral, and unpleasant IAPS pictures, presented in blocks separated by an inter-block interval. With increasing exposure to unpleasant pictures, startle magnitude showed greater potentiation, and corrugator EMG activity increased. Both affective startle and corrugator modulation persisted following exposure to unpleasant pictures. The cumulative effects of sustained exposure to unpleasant pictures were enhanced for those reporting higher state anxiety, consistent with the hypothesis that sustained aversive exposure leads to increased defensive activation. These findings suggest sustained exposure to unpleasant pictures may induce a short-term mood state, and may be a useful paradigm to study individuals who vary in symptoms of anxiety.     

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 multi-process account of startle modulation during affective perception

Modulation of the startle reflex by sensory, attentional, and emotional processes was explored by presenting acoustic startle probes at various delays following picture onset. Within 500 ms of onset, blinks were first greatly facilitated and then inhibited, indicating prepulse facilitation and prepulse inhibition that did not vary with affect. Attention allocation to the picture continued across the viewing interval and was most pronounced for emotional pictures, as determined by attenuation of the P3 component to the startle probe. Startle potentiation for unpleasant pictures occurred later in the viewing interval and was strongest for highly arousing pictures. Taken together, the startle reflex during picture viewing is modulated by sequential and sometimes concurrent processes of prepulse facilitation, prepulse inhibition, attentional inhibition, and affective modulation, with reflex magnitude reflecting the net effect of multiple processes.     

Loss of emotional experience after traumatic brain injury: findings with the startle probe procedure

The authors used affective modulation of the eyeblink startle response to examine the impact of traumatic brain injury (TBI) on emotional reactions to pictures. Participants were 13 individuals with severe TBI and 24 controls. Participants were presented with pictures that differed in affective valence (e.g., mutilated bodies, erotic couples, and household objects) while the eyeblink startle response to an acoustic probe was measured. Startle amplitude was used to assess valence of emotional response, and startle latency was used to index interest in the pictures. Subjective ratings of the affect and arousal elicited by the various pictures were also obtained. TBI impaired startle potentiation to unpleasant pictures but not startle attenuation to pleasant pictures. Further, subjective ratings indicated that TBI participants found unpleasant pictures less arousing than did controls. The results are consistent with recent evidence of differential impairment in negative versus positive emotions after TBI and are discussed in relation to 2 competing explanations of startle modulation.     

Probe P3 and blinks: Two measures of affective startle modulation

Two concurrent measures of the evoked startlé response, the elicited blink reflex and the event-related potential, were measured while individuals viewed pictures that varied in pleasure and arousal. Replicating previous findings, the blink response was modulated by picture pleasantness, with larger reflexes elicited in the context of viewing unpleasant versus pleasant pictures. However, the probe P3 was primarily modulated by picture arousal, with smaller P3 responses elicited when viewing affective (pleasant or unpleasant) than when viewing neutral pictures. Both modulatory effects were sustained for probes presented in a subsequent picture imagery period. These data suggest that two measurable responses to the same startle probe are differentially modified by emotional context, with blink magnitude varying with pleasure and probe P3 varying with stimulus arousal.