The Reflex Physiology of Defense

For humans, the threat of painful shock greatly potentiates the reflexive startle blink. Moreover, viewing unpleasant, compared with pleasant, pictures also prompts heightened startle reflexes, suggesting that the startle reflex indexes general defensive activation. In this study, pleasant or unpleasant pictures were used to signal shock threat in order to explore how previous affective associations modulate new defensive reactions. When cuing threat of shock, pleasant and unpleasant pictures prompted physiological profiles consistent with defensive activation, indicating that threat of shock renders previously pleasant cues aversive. For unpleasant pictures only, defensive startle was potentiated even when these cues signaled safety. Taken together, the data indicate that (a) regardless of their intrinsic affective meaning, cues signaling shock threat prompt somatic and autonomic reactions consistent with defense, and that (b) intrinsically unpleasant cues continue to prompt defensive activation even when the context of their presentation is specifically nonthreatening. When confronting cues that predict an imminent painful shock, both people (Hamm, Greenwald, Bradley, & Lang, 1993) and rats (Davis, 1989) show an enhanced startle reflex. Furthermore, Grillon and Davis (e.g., Grillon, Ameli, Woods, Merikangas, & Davis, 1991; Grillon & Davis, 1995) have shown repeatedly that for humans, the mere verbal threat of electric shock is enough to produce the same effect. That is, the reflexive blink response is potentiated when startle probes are presented in the context of a cue (e.g., a red light—‘‘threat’’) that signals the possibility of electric shock relative to when they are presented in the context of a cue (e.g., a green light—‘‘safe’’) signaling that no shocks will be delivered. In humans, the startle reflex is similarly potentiated when people look at unpleasant pictures (see Bradley, Cuthbert, & Lang, 1999, for a review). Moreover, the startle reflex is inhibited when people view pleasant scenes, compared with affectively neutral pictures. In effect, the hedonic valence of stimuli—that is, how pleasant or unpleasant they are—can be determined by the magnitude of concurrently elicited startle blinks. We have interpreted affective modulation of the startle reflex as an instance of motivational priming. In this view (see Konorski, 1967; Lang, Bradley, & Cuthbert, 1990, 1997), emotions are organized motivationally—by a defensive motivational system, activated in contexts involving threat, and an appetitive system, activated in contexts that sustain the organism, promoting survival. These systems are implemented through neural circuits in the brain that are old in evolution and shared across mammalian species. According to the motivational-priming view, activation of the defense system by an unpleasant cue (i.e., a shock or unpleasant picture) primes related defensive reflexes such as the startle response; conversely, when the appetitive system is predominant, defensive reflexes are inhibited. Thus, threat of shock activates the defensive motivational system, potentiating the startle reflex. In the absence of shock threat, pleasant and unpleasant cues are presumed to intrinsically activate the appetitive and defensive motivational systems, prompting startle enhancement or inhibition, respectively. In the current study, we used pleasant or unpleasant pictures to cue threat of shock (or safety) in order to investigate how existing hedonic associations modify reactions to upcoming aversive events. In the classical threat-of-shock paradigm (e.g., Grillon et al., 1991), the critical comparison is between the magnitude of startle reflexes elicited during cues that signal threat of shock (threat period) and the magnitude of startle reflexes elicited during cues that signal a period that is free of shock threat (safe period). In the present experiment, we examined these startle effects as a function of the hedonic valence of the cue and, in addition to startle, assessed other concurrent defensive reactions (e.g., in heart rate, facial muscle action) that are prompted by threat. One hypothesis is that when pleasant pictures cue shock, concurrent appetitive activation will lead these cues to prompt Brad Moulder is now at Educational Testing Service, Princeton, NJ. Address correspondence to Margaret Bradley, Box 100165 HSC, Gainesville, FL 32610; e-mail: [email protected]. PSYCHOLOGICAL SCIENCE 468 Volume 16—Number 6 Copyright r 2005 American Psychological Society weaker defensive reactions than occur when unpleasant cues signal shock threat. This reciprocal-activation hypothesis is somewhat supported by counterconditioning studies suggesting that it is difficult to change associations from aversive to appetitive (e.g., Bromage & Scavio, 1978; Scavio, 1974) or vice versa. However, it is also possible that cues signaling threat of shock will potentiate the startle reflex, compared with cues that signal safety, regardless of the a priori hedonic valence of the cues. According to this defensive-activation hypothesis, once a cue signals an aversive event (such as the possibility of painful shock), the defense system is activated, regardless of prior hedonic associations. This hypothesis predicts that picture cues threatening shock, regardless of whether they are pleasant or unpleasant, will elicit larger somatic and autonomic reflexes than do cues signaling safety. Both hypotheses predict that in the absence of shock threat, reflexes should be potentiated when people view unpleasant, compared with pleasant, pictures, as these aversive stimuli should continue to activate the defense system. In the present study, threat and safety cues consisted of a variety of different pictures, selected from the International Affective Picture System (IAPS; Lang, Bradley, & Cuthbert, 2001), that are rated either as highly pleasant and arousing or as highly unpleasant and arousing; people reliably react to these pictures with affective differentiation (e.g., Bradley, Codispoti, Cuthbert, & Lang, 2001; Lang, Greenwald, Bradley, & Hamm, 1993). Half of the participants were told that if any pleasant picture was presented, presentation of an electric shock was possible (i.e., threat), whereas if any unpleasant picture was presented, there was no shock threat (i.e., safe). For the other half of the participants, unpleasant pictures cued threat of shock, and pleasant pictures were safe. PHYSIOLOGICAL MEASURES OF DEFENSIVE ACTIVATION Fear-potentiated startle is one index of defensive activation. In a normal picture-viewing context, unpleasant (compared with pleasant) pictures also prompt increased cardiac deceleration (similar to the fear bradycardia observed in animals; see Campbell, Wood, & McBride, 1997) and heightened activity over the corrugator facial (‘‘frown’’) muscle (Bradley et al., 2001; Lang et al., 1993; Winton, Putman, & Krauss, 1984). To the extent that threat of shock prompts defensive activation (as opposed to sheer anticipatory processing, e.g.), cues signaling threat of shock are expected to prompt enhanced cardiac deceleration and increased corrugator electromyographic (EMG) activity. To date, there is limited understanding of the pattern of autonomic and somatic physiological changes that might accompany startle modulation under threat of shock. Unlike cardiac and facial EMG measures, skin conductance activity does not discriminate between defensive and appetitive activation in a normal picture-viewing context. Rather, both unpleasant and pleasant pictures prompt greater electrodermal reactions than neutral pictures (Lang et al., 1993), suggesting that sympathetic activity increases during viewing of emotional pictures. Moreover, Öhman, Hamm, and Hugdahl (2000) noted that skin conductance activity increases for signaling stimuli, regardless of whether they cue aversive (e.g., shock) or nonaversive (reaction time task) events, suggesting that this measure also reflects the signal value of the cue. In the case of the present study, skin conductance would be heightened for cues that threaten shock, compared with cues that signal safety, regardless of their a priori hedonic valence.