General Discussion - Effects of Anticipatory Anxiety on Emotion Processing

General Discussion

Both emotional picture viewing and threat-of-shock are well-established research paradigms. Exposed to pictorial stimuli varying in emotional valence and arousal has been shown to be associated with multifaceted perceptual, physiological, and behavioral changes. Starting with the stimulus onset, sensory-motor response programs facilitate optimal information uptake (e.g., orienting response; Bradley, 2009; Öhman, 1979). In addition, mediated by means of distributed cortical networks involved in the visual processing stream, attentional processes provide an information selection. To this end, emotional-motivational significance has been suggested to guide stimulus processing in providing preferential access to processing resources (Lang et al., 1997; Öhman et al., 2000; Schupp et al., 2006). As supported by a large number of studies utilizing neuroscientific methods (e.g., ERP, fMRI), this “natural selective attention” enables detailed processing of significant over non-significant information in the visual processing stream (e.g., Bradley et al., 2003; Junghöfer, Sabatinelli et al., 2006; Lang et al., 1998;

Pessoa & Ungerleider, 2004; Sabatinelli et al., 2005; Schupp et al., 2006; Vuilleumier, 2005). Building upon this stimulus extraction, the fundament is provided to adequately respond within a given situation. Accordingly, as soon as relevant information is detected, physiological systems involved in related response repertoire are prepared. This motivational priming account is supported by numerous studies demonstrating psychophysiological changes in favor of action (e.g., Bradley et al., 2001; Hamm et al., 2003; Lang et al., 1997; Öhman et al., 2001).

Within a context of potential threat, perceptual and response systems are more vigilant and prepared for action than while being in a relaxed atmosphere. Accordingly, environmental information related to real-world danger has been suggested to play a superior role in organizing immediate responses to sustain life and organism’s integrity

(Cacioppo & Berntson, 1994; Mogg & Bradley, 1999; Ito, Larsen, Smith, & Cacioppo, 1998). In this context, recent research utilized the threat-of-shock paradigm as providing a powerful tool to induce fear/anxiety by means of verbal communication. As revealed by several studies, instructed threat-cues are related to physiological changes facilitating fast responses (e.g., Bradley et al., 2005; Funayama et al., 2001; Grillon et al., 1991, 2004, 2006; Grillon & Davis, 1995). Moreover, few first studies focused on perceptual and attentional modulation during the anticipation of threat (e.g., Baas et al., 2002, 2006;

Böcker et al., 2001, 2004; Cornwell et al., 2007; Hasler et al., 2007), and still less studies referred to similarities and differences of emotion processing and anticipatory anxiety (Bradley et al., 2005; Funayama et al., 2001; Lissek et al., 2007). Thus, to date little is known about the interplay of emotion processing and the anticipation of threat.

To investigate this research question, the present thesis pursued two major avenues to examine reciprocal interactions and the mutual impact of anticipatory anxiety and emotion processing. (1) Anticipating aversive events may modulate emotion processing depending on whether picture materials are related or unrelated to threat-of-shock. In other words, the predictive value of environmental information regarding threat-of-shock may be crucial in determining threat effects on perceptual processing and responding. To this end, Study I and II examined emotional and neutral picture processing when these stimuli were unrelated (i.e. not predictive) to threat-of-shock. Conversely, in Study III picture categories were instructed to cue threat-of-shock (cf. Bradley et al., 2005). (2) The mutual impact of anticipatory anxiety and hedonic picture valence may vary across different processing and response stages (e.g., perceptual-evaluative vs. motor-behavioral; cf. Cacioppo &

Berntson, 1994). That is, the notion of different processing stages states an information processing stream ranging from perceptual/evaluative processing levels (Study II and III), to physiological response preparation and final motor output (Study I; cf. Bradley et al.,

2005). Thus, a state of aversive anticipation may critically modulate the perception and physiological responses to environmental stimuli.

Focusing on the Interaction of Anticipatory Anxiety and Emotion Processing Threat-of-shock and Affective Picture Viewing: Replications

Key findings regarding both picture viewing and threat-of-shock paradigms were replicated. The defensive eyeblink reflex was observed to vary as a function of hedonic picture valence (i.e., inhibited/potentiated during pleasant/unpleasant picture viewing; cf.

Bradley, 2000; Lang et al., 1997), and verbally instructed threat contingencies (threat potentiated startle; cf. Grillon et al., 1991; Lissek et al., 2007). Furthermore, enhanced skin conductance levels indicated the activation of the sympathetic nervous system under threatening conditions (cf. Bradley et al. 2005; Phelps et al., 2001). Thus, Study I provided basal evidence for the mutual activation of motivational systems by means of verbally instructed threat-of-shock and affective picture media in the present protocol. With regard to perceptual-evaluative processes, Study II and III replicated emotion-sensitive ERP components (i.e., enhanced EPN and LPP amplitudes for emotional as compared to neutral pictures), which are suggested to reflect preferential processing of emotional/motivational significant stimuli (cf. Junghöfer et al., 2001; Schupp et al., 2006). Overall, self-report data supported the notion of the high aversiveness of threat-of-shock conditions (cf. Grillon et al., 1991; Mol et al., 2007). Taken together, these replications provide the fundament to meaningfully interpret the interaction of both experimental manipulations.

(1) Predictive Value: Picture Materials Cueing or Unrelated to Threat-of-shock

Pictures Unrelated to Threat-of-shock: The present Studies I and II operationalized anticipatory anxiety by means of sustained presented picture frames instructed to signal

threat-of-shock. These background frames established the context in which pictures unrelated to threat-of-shock were presented phasically. Thus, exposed to environmental conditions including rather unpredictable events (i.e., threat-of-shock sustained for a long period of time), aversive anticipatory processes were triggered irrespective of hedonic picture valence.

With regard to perceptual-evaluative modulations, Study II revealed a valence-specific effect for pleasant picture materials incongruent to the current state of aversive anticipation. Specifically, under threat-of-shock pleasant picture processing was associated with a relative negativity developing early over visual processing areas and sustaining for several hundred ms (80 - 580 ms). Furthermore, neither unpleasant nor neutral stimuli exhibited comparable threat effects. Accordingly, alternative hypotheses predicting a general sensitization effect irrespective of picture valence, or specifically enhanced processing of unpleasant pictures under threat-of-shock were not supported in this protocol. In contrast, these findings may rather reflect enhanced attentional engagement towards stimuli mismatching environmental conditions (Study II). This emotional mismatch hypothesis was suggested in reference to research on the impact of physical and semantic incongruity (MMN and N400; Kutas & Federmeier, 2000; Näätänen, 1995).

Thus, the detection of an environmental deviance/change may direct attentional resources to trigger situational update processes (Cornwell et al., 2007).

Furthermore, indicating primed physiological response systems exerting final motor output, Study I revealed that contextual threat signals prompted overall potentiated reflex activity and enhanced skin conductance level. Of main interest, under threat-of-shock defensive reflex activity remained sensitive to the hedonic picture content. This was suggested to reflect an additive but independent effect of aversive anticipation and picture valence on defense system activation (Study I). Considering previous research, results

support an arousal-based impact of aversive anticipation on startle reflex modulation. For instance, recent research examining defensive reactivity during the anticipation of pictures found startle potentiation when anticipating emotionally arousing images (pleasant and unpleasant), in contrast to neutral stimuli (Lipp, Cox, & Siddle, 2001; Sabatinelli, Bradley,

& Lang, 2001). Analogously, the anticipation of aversive events while viewing task irrelevant pictures might reflect emotional arousal rather than the hedonic valence of the anticipated event. Consistent with this hypothesis, a recent study by Löw and colleagues (2008) obtained similar physiological mobilization patterns during the anticipation of appetitive (monetary reward) and aversive (threat-of-loss) outcomes. Taken together, these findings support the notion of highly flexible motivational systems that dynamically adjust to foreground and contextual environmental conditions.

Pictures Predictive for Threat-of-shock: Study III and a similar study by Bradley and colleagues (2005) provided complementary findings about cue-specific or rather predictable of-shock (i.e., possible shock administration was limited to brief threat-cue presentation time). Thus, by means of verbal instructions, the implicit hedonic picture valence was learned to be associated with threat-contingencies.

Regarding perceptual/evaluative modulations, Study III examined electrocortical processing of pictures explicitly instructed as threat-, safe-, or control cues, respectively.

Threat-cue processing revealed modulated P1, P2, and LPP components irrespective of the hedonic picture valence. However, there was no interaction of threat-of-shock and hedonic picture valence on the EPN or LPP components. According to the general sensitization hypothesis, threat-cue processing was suggested to operate independently from the extraction of implicit hedonic picture valence.

With respect to motor/behavioral output stages, Bradley and colleagues (2005) observed that both pleasant and unpleasant pictures prompted similarly potentiated startle

reflex, heart rate deceleration and enhanced skin conductance responses when serving as instructed threat-cues. Interestingly, threat-of-shock potentiated startle responses were observed only for pleasant pictures cueing threat, whereas startle blink magnitudes during unpleasant pictures remained on a similar level for threat as compared to safety conditions.

However, effectively both ‘pleasant’ threat cues and passively viewing unpleasant pictures exhibited similarly potentiated startle magnitudes, and therefore indicated alike enhanced defensive activation by pleasant and unpleasant threat-cues (Bradley et al., 2005).

To summarize and integrate these result patterns (Study I, II, III, Bradley et al., 2005), the importance of the instructed predictive value of picture media needs to be highlighted. Viewing pictures that were predictive for threat-of-shock revealed clear ERP effects indicating initially unspecific vigilance and subsequently more elaborate stimulus processing as compared to safety and control conditions (Study III). In addition, response-related physiological parameter indicated enhanced defensive activation in order to prepare and execute appropriate actions (Bradley et al., 2005). On the other side, the perceptual processing of threat-irrelevant picture stimuli revealed processing patterns rather related to an emotional mismatch between foreground picture and aversive background information (Study II). However, physiological response systems indicated defensive activation due to the threatening context, and nevertheless, the defensive reflex circuitry remained sensitive to irrelevant picture media (Study I). Taken together, these findings support the notion that verbally instructed threat-contingencies direct attentional processing resources and prime defensive responses in order to cope with both unpredictable or rather predictable real-world dangers (Grillon et al., 2004; Hasler et al., 2007; Mol et al., 2007).

(2) Processing Stages: From Perception to Response

The interplay of anticipatory anxiety and hedonic picture valence varied across processing stages (perceptual/evaluative vs. motor/behavioral stages; cf. Cacioppo &

Berntson, 1994). Whereas viewing pictures unrelated to contextual threat signals exhibited valence-specific ERP modulations on perceptual stages (Study II), the motor-behavioral output revealed startle modulations irrespective of hedonic picture valence (Study I).

Somewhat contrary, instructed threat-cues revealed valence-unspecific ERP effects (Study III) and prompted similar defensive activation regardless of implicit hedonic picture valence (Bradley et al., 2005). As previously discussed, these differences may tightly relate to the different predictive value of the picture contents, and therefore exert differential impact on perceptual processing and response preparation. Thus, with regard to clinical research, distinct findings among rather predictable and unpredictable threat-of-shock on emotion processing may refer to differences of cue-specific fear and more generalized anxiety (Barlow et al., 1996; Davis, 2002; Grillon et al., 2004).

Furthermore, Study III provided insights about sub-processes within the perceptual-evaluative processing stream as modulated by threat-of-shock. Specifically, early stimulus processing as reflected by the P1 component rather roughly discriminated among experimental runs comprising threat-of-shock and no-threat. Subsequently, the P2 component reflected a more elaborate distinction between threat-cue and safe-cue within threat-of-shock runs as compared to control condition. Finally, as indicated by the LPP component later stimulus processing reflected highly accurate differentiation between threat-of-shock cues as compared to both safe conditions (safe-cues and control cues).

These changes in differential processing patterns over time may reflect successive processing stages ranging from large-capacity sensory encoding to capacity-limited higher-order evaluations (Öhman, 1979, 1986; Schupp et al., 2006; Schupp, Stockburger,

Schmälzle et al., 2008). Thus, building on each other, consecutive perceptual/evaluative sub-processes progressively gained more detailed information about environmental conditions.

In addition, Study II indicated enhanced perceptual processing of situational incongruent stimuli. Thus, as long as pictures were irrelevant to the anticipation of threat, an environmental deviance may preferentially direct attentional resources triggering situational update processes (Cornwell et al., 2007). However, it has to be noted that the ERP extraction in Study II was locked to the picture onset (i.e., not related to the onset of contextual threat-of-shock signals), and therefore may have hindered more general unspecific threat effects indicative for enhanced alertness and vigilance (cf. Study III;

Michalowski et al., 2009). To clarify this hypothesis, a non-continuous presentation of contextual threat signals would be informative (e.g., separated by intertrial intervals; cf.

Pastor et al., 2007).

Focusing on the motor-behavioral output stage, results clearly showed the modulation of defensive reflex circuitry by means of contextual threat signals (Study I), and instructed threat-cues (Bradley et al., 2005). Furthermore, beyond reflexive motor stages, first studies observed behavioral avoidance and modulated choice behavior in order to avoid unpredictable threat (Grillon et al., 2006; Berns et al., 2006). However, few is known about the execution of overt and goal directed behavior under threat of aversive events (e.g., by giving the chance to actively avoid or cope with aversive outcomes;

Delgado, Jou, LeDoux, & Phelps, 2009; Lissek et al., 2007). In addition, enhanced electrodermal activity has been observed for threat-of-shock, compared with safety conditions (Study I; Bradley et al., 2005). These data are consistent with previous conditioning studies (cf. Öhman, Hamm, & Hugdahl, 2000) in which elevated skin conductance was found for cues signaling either aversive (electric shock) or non-aversive

(reaction time task) outcomes. Thus, the sympathetically mediated skin conductance may more broadly reflect predictive properties of the cueing stimulus (Bradley et al., 2005;

Öhman et al., 2000). Taken together, building upon facilitated stimulus processing, related physiological systems are prepared to easily respond under aversive conditions of verbally instructed threat-of-shock. These effects vary as a function of predictive stimulus value and distinct processing stages.

Threat-of-shock and Affective Picture Processing: Emotion-sensitive ERP Components With regard to ERP findings, the present Studies II and III provided little evidence that threat-of-shock interactively modulated selective emotion processing as indicated by the early posterior negativity and the late positive potential. Although Study II revealed enhanced negativity for pleasant pictures during threat-of-shock within the EPN time window (140-280 ms), this modulation appeared to reflect the sustained posterior negativity effect spanning a much longer period of time (80-580 ms) rather than the specific enhancement of the EPN component. Furthermore, during threat-of-shock periods neither EPN modulations for unpleasant pictures were observed, nor the emotional LPP varied as a function of sustained threat or safety conditions. Thus, Study II provided no support for a motivational priming account, which would predict that sustained defensive activation specifically sensitizes unpleasant picture processing.

In addition, threat-of-shock cued by hedonic picture content revealed no effect on the EPN component, but exhibited a pronounced late positive potential for threat-cues as opposed to the same pictures cueing safety or presented under control conditions (Study III). However, this threat induced LPP modulation revealed a more parieto-occipital topography than the LPP elicited by affective picture media (centro-parietal). Although LPP effects for threat-of-shock and picture category were significant over both scalp-topographies, neither of the clusters revealed a significant interaction. However, more

importantly, enhanced LPP amplitudes for threat-cues as compared to safe-cues may reflect a general sensitization effect (i.e., irrespective of implicit hedonic picture valence) facilitating elaborate stimulus processing in favor of real-world danger cues (Study III).

Thus, considering the EPN and LPP as measures of stimulus significance and selective attention to emotional/motivational relevant picture contents (Schupp et al., 2006), the present studies revealed similarities and differences in the processing of emotional picture media and threat-related environmental information. With regard to the topography, effects for emotional pictures and threat-of-shock were partly similar distributed over occipital (~80-300 ms) and parietal (~300-800 ms) sensor regions. These effects were suggested to indicate early perceptual processing over modality-specific brain regions and later high-level elaborative processing including distributed brain-networks in parietal association regions (Study II and III; Junghöfer, Sabatinelli et al., 2006;

Nieuwenhuis et al., 2005; Picton, 1992; Schupp et al., 2006).

Referring to the time course, threat-of-shock effects revealed considerably shorter onset-latencies than emotional picture content (Study II and III; cf. Baas et al., 2002, 2006). These findings may relate to the higher global impact of real-world danger conditions as compared to pictorial information mediating rather vicarious affective meaning. However, future research is needed to outline the underlying processes and neural networks fostering fast detection and categorization of stimulus significance under threatening conditions (cf. Codispoti, Ferrari, DeCesarei, & Cardinale, 2006; Schupp et al., 2006).

Threat-of-shock and Affective Picture Processing: Novelty and Habituation

Focusing on IAPS picture processing, several studies observed that enlarged EPN and LPP amplitudes elicited by emotional as compared to neutral pictures are maintained,

even when picture materials were repeated as often as 100 times (Codispoti et al., 2006, 2007; Schupp et al., 2005, 2006). These findings were fully confirmed in the present Study II. Thus, selective attention to affective pictures seems to be a robust phenomenon, even when presented concurrently to stimuli signaling threat of real-world danger (Study II and III; cf., Schupp, Stockburger, Bublatzky et al., 2007, 2008). With regard to motor-behavioral responding, the finding of reduced affective startle modulation in the end of Study I contrast with recent research reporting affective reflex modulation as relatively stable over time (Bradley, Lang, & Cuthbert, 1993; Bradley, Cuthbert, & Lang, 1996).

However, various methodological differences may account for this finding (e.g., continuous picture presentation, number of trials).

Referring to threat-of-shock manipulation, habituation effects have not been systematically investigated yet. Some studies reported that threat-of-shock effects were relatively sustained across blocks of few trials (e.g., for startle potentiation and self-reported data; Grillon et al., 1991; Grillon et al., 1993; Cornwell et al., 2007; Mol et al., 2007). However, a recent fMRI study reported significant within block habituation, i.e., attenuated amygdala activation (Phelps et al., 2001). Thus, the available evidence points to the direction that threat-of-shock effects are relatively robust, but differ across measurement time and dependent variables. Extending these findings, Study I explicitly addressed this topic. Although startle blink magnitude habituated along the experiment, differences between threat and safety conditions remained significant even at the end of the experiment. In addition, enhanced skin conductance level was observed to be stable within and across threat-of-shock conditions. That is, despite repeated ‘false’ shock announcements (i.e., no shock application), verbally instructed threat of aversive events prompted intense and sustained activation of defensive response systems.

With regard to the perceptual/evaluative processing stage, Study II revealed marginal modulation of the threat-of-shock effect among the first as compared to the second experimental session (each ~10 min). Furthermore, self-report data revealed somewhat attenuated threat effects at the end of the second session, but the difference between threat-of-shock and safety conditions was still highly significant. Thus, Study I and II support the notion of robust effects on perceptual processing and motor output parameters under conditions of contextually signaled threat-of-shock, but nevertheless unpredictable aversive events. These findings are in line with recent research affirming unpredictability as an important factor mediating habituation of neural activity (e.g., in the amygdala) and emotional behavior (Grillon et al., 2006; Herry et al., 2007). Accordingly, aversive stimuli produce more fear/anxiety if presented in a temporally unpredictable rather than reliably cued manner (Grillon et al., 2004; Mineka & Kihlstrom, 1978). Seen from an evolutionary perspective, the persistence of defensive activation under threatening conditions appears functional in natural environment, as response priming while viewing

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