Emotion, motivation, and anxiety: brain mechanisms and psychophysiology.

The organization of response systems in emotion is founded on two basic motive systems, appetitive and defensive. The subcortical and deep cortical structures that determine primary motivated behavior are similar across mammalian species. Animal research has illuminated these neural systems and defined their reflex outputs. Although motivated behavior is more complex and varied in humans, the simpler underlying response patterns persist in affective expression. These basic phenomena are elucidated here in the context of affective perception. Thus, the research examines human beings watching uniquely human stimuli--primarily picture media (but also words and sounds) that prompt emotional arousal--showing how the underlying motivational structure is apparent in the organization of visceral and behavioral responses, in the priming of simple reflexes, and in the reentrant processing of these symbolic representations in the sensory cortex. Implications of the work for understanding pathological emotional states are discussed, emphasizing research on psychopathy and the anxiety disorders.

Emotion, attention, and the startle reflex.

This theoretical model of emotion is based on research using the startle-probe methodology. It explains inconsistencies in probe studies of attention and fear conditioning and provides a new approach to emotional perception, imagery, and memory. Emotions are organized biphasically, as appetitive or aversive (defensive). Reflexes with the same valence as an ongoing emotional state are augmented; mismatched reflexes are inhibited. Thus, the startle response (an aversive reflex) is enhanced during a fear state and is diminished in a pleasant emotional context. This affect-startle effect is not determined by general arousal, simple attention, or probe modality. The effect is found when affects are prompted by pictures or memory images, changes appropriately with aversive conditioning, and may be dependent on right-hemisphere processing. Implications for clinical, neurophysiological, and basic research in emotion are outlined.

Emotion, novelty, and the startle reflex: habituation in humans.

Previous research with both animal and human subjects has shown that startle reflex magnitude is potentiated in an aversive stimulus context, relative to responses elicited in a neutral or appetitive context. In the present experiment, the same pleasant, unpleasant, and neutral picture stimuli were repeatedly presented to human subjects. Startle reflex habituation was assessed in each stimulus context and was compared with the habituation patterns of heart rate, electrodermal, and facial corrugator muscle responses. All systems showed initial differentiation among affective picture contents and general habituation over trials. The startle reflex alone, however, continued to differentiate among pleasant, neutral, and unpleasant pictures throughout the presentation series. These results suggest that (a) the startle probe reflex is relatively uninfluenced by stimulus novelty, (b) the startle modulatory circuit (identified with amygdala-reticular connections in animals) varies systematically with affective valence, and (c) the modulatory influence is less subject to habituation than is the obligatory startle pathway or responses in other somatic and autonomic systems.

Startle potentiation: shock sensitization, aversive learning, and affective picture modulation.

This study investigated the size of, and relationship between, different modulatory effects of aversive stimulation on the acoustic startle reflex. This reflex is potentiated by shock exposure and associative shock conditioning (in animals and human volunteers) and unpleasant pictures (in human volunteers). In this study, dramatic sensitization of the probe-startle response was observed after shock exposure but not after a control task. Magnitude of sensitization was significantly larger than associative shock conditioning and picture modulation effects (also significant). Sensitization and conditioning scores showed modest, significant correlations with one another but not with picture modulation scores, consistent with animal data showing that partially overlapping brain mechanisms (i.e., amygdaloid-reticular projections) mediate these effects. The present results also indicate that sensitization of startle in human volunteers is a relatively more robust defensive response to aversive stimulation.

Intravenous beta-endorphin: behavioral and physiological effects in conscious monkeys.

Beta-endorphin (0.7 and 2.8 mg/kg) and morphine (0.15 and 0.60 mg/kg) were administered intravenously to rhesus monkeys responding on an operant schedule. Beta-endorphin injections resulted in dose-dependent effects which included marked, but relatively brief disruptions in behavioral responding, decreases in systolic blood pressure, and more protracted increases in heart rate. Morphine injections were followed by much longer duration decreases in response rates and systolic blood pressure, and an irregular but largely deceleratory heart rate response. On a molar basis, beta-endorphin was approximately twice as potent as morphine. It was concluded that intravenously administered beta-endorphin exerts behavioral and physiological effects in the unanesthetized primate.

Emotion in the criminal psychopath: fear image processing.

We tested the hypothesis that the response mobilization that normally accompanies imagery of emotional situations is deficient in psychopaths. Cardiac, electrodermal, and facial muscle responses of 54 prisoners, assigned to low- and high-psychopathy groups using R. D. Hare's (1991) Psychopathy Checklist--Revised, were recorded while subjects imagined fearful and neutral scenes in a cued sentence-processing task. Groups did not differ on self-ratings of fearfulness, imagery ability, or imagery experience. Low-psychopathy subjects showed larger physiological reactions during fearful imagery than high-psychopathy subjects. Extreme scores on the antisocial behavior factor of psychopathy predicted imagery response deficits. Results are consistent with the idea that semantic and emotional processes are dissociated in psychopaths.

Emotional imagery in simple and social phobia: fear versus anxiety.

In a first study, phobic volunteer subjects (N = 60) reacted psychophysiologically with greater vigor to imagery of their own phobic content than to other fearful or nonaffective images. Imagery heart rate responses were largest in subjects with multiple phobias. For simple (dental) phobics, cardiac reactivity was positively correlated with reports of imagery vividness and concordant with reports of affective distress; these relationships were not observed for social (speech) phobics. In a second study, these phobic volunteers were shown to be similar on most measures to an outpatient clinically phobic sample. In an analysis of the combined samples, fearful and socially anxious subtypes were defined by questionnaires. Only the fearful subtype showed a significant covariation among physiological responses, imagery vividness, and severity of phobic disorder. This fearful-anxious distinction seems to cut across diagnostic categories, providing a heuristic perspective from which to view anxiety disorders.

Brain potentials in affective picture processing: covariation with autonomic arousal and affective report.

Emotionally arousing picture stimuli evoked scalp-recorded event-related potentials. A late, slow positive voltage change was observed, which was significantly larger for affective than neutral stimuli. This positive shift began 200-300 ms after picture onset, reached its maximum amplitude approximately 1 s after picture onset, and was sustained for most of a 6-s picture presentation period. The positive increase was not related to local probability of content type, but was accentuated for pictures that prompted increased autonomic responses and reports of greater affective arousal (e.g. erotic or violent content). These results suggest that the late positive wave indicates a selective processing of emotional stimuli, reflecting the activation of motivational systems in the brain.

Food deprivation and emotional reactions to food cues: implications for eating disorders.

Two studies examined emotional responding to food cues. In experiment 1, normal college students were assigned to 0-, 6- or 24-h of food deprivation prior to presentations of standard emotional and food-related pictures. Food deprivation had no impact on responses elicited by standard emotional pictures. However, subjective and psychophysiological reactions to food pictures were affected significantly by deprivation. Importantly, food-deprived subjects viewing food pictures showed an enhanced startle reflex and increased heart rate. Experiment 2 replicated the food deprivation effects from experiment 1, and examined participants reporting either a habitual pattern of restrained (anorexia-like) or binge (bulimia-like) eating. Food-deprived and binge eater groups showed startle potentiation to food cues, and rated these stimuli as more pleasant, relative to restrained eaters and control subjects. The results are interpreted from the perspective that startle modulation reflects activation of defensive or appetitive motivation. Implications of the data for understanding eating disorders are considered.

Emotion and motivation I: defensive and appetitive reactions in picture processing.

Emotional reactions are organized by underlying motivational states--defensive and appetitive--that have evolved to promote the survival of individuals and species. Affective responses were measured while participants viewed pictures with varied emotional and neutral content. Consistent with the motivational hypothesis, reports of the strongest emotional arousal, largest skin conductance responses, most pronounced cardiac deceleration, and greatest modulation of the startle reflex occurred when participants viewed pictures depicting threat, violent death, and erotica. Moreover, reflex modulation and conductance change varied with arousal, whereas facial patterns were content specific. The findings suggest that affective responses serve different functions-mobilization for action, attention, and social communication-and reflect the motivational system that is engaged, its intensity of activation, and the specific emotional context.

The fear potentiated startle effect. Blink reflex modulation as a result of classical aversive conditioning.

A differential conditioning study examined whether an acoustic startle probe, presented during extinction of an aversively conditioned visual stimulus, potentiated the reflex eyeblink response in humans and whether this potentiation varied with the change in affective valence of the conditioned stimulus. Sixty college students were randomly assigned to view a series of two slides, depicting either unpleasant/highly arousing, unpleasant/moderate arousing, neutral/calm, pleasant/moderate arousing or pleasant/highly arousing scenes and objects (duration: 8 sec). During preconditioning (8 trials) and extinction (24 trials) acoustic startle probes (white noise bursts [50 ms; 95 dBA] were administered during and between slide presentation). During acquisition (16 trials) CS+ was reinforced by an electric shock. Startle response magnitudes significantly increased from preconditioning to extinction and were substantially larger to CS+. Conditioned startle reflex augmentation linearly increased with the pleasantness of the slides. Furthermore, subjects showed a greater post-conditioning increase of judged aversiveness to slides that they had previously reported to be more pleasant, exactly paralleling the startle reflex results.

Affective information processing and the assessment of anxiety.

A conceptualization of anxiety as comprising three loosely coupled response systems of overt behavior, verbal report, and physiological activation has proven useful in clinical and theoretical work. With this framework as a starting point, an information-processing approach to the study of emotion is described. Emotions are conceived as affective programs within the brain, with information coded as propositions organized into associative networks. Affective expression results when such a network is accessed and processed, which can occur when a sufficient number of propositions are activated by environment stimuli and/or internal associations. It is hypothesized that information about the expressive physiology is an integral component of the associative structure, and that processing of the network accordingly results in measurable psychophysiological response. Data from studies of emotional imagery, as well as other areas of research, are reviewed in support in these theories. The utility of this approach for the assessment of anxiety disorders is discussed, and results of clinical studies are presented to suggest that individual differences in accessing and processing emotional information may bear significant implications for prognosis and treatment selection. It is speculated that differences among the anxiety disorders could be interpreted in terms of the degree of cognitive organization of the network, leading to potential refinement of current diagnostic categories. In conclusion, cognitive psychology paradigms are discussed in terms of their application to the assessment and treatment of anxiety disorders.

Picture media and emotion: effects of a sustained affective context.

Pleasant, neutral, or unpleasant pictures were presented in a continuous series, and the effects of repetitive exposure to pictures of the same affective valence were assessed in somatic (corrugator electromyographic [EMG] activity) and visceral (heart rate and skin conductance) systems. Probe stimuli (startle or reaction time probes) were presented to index emotional and attentional concomitants of processing. Affective discrimination was maintained across time in all response systems, and sensitization was found for the corrugator EMG response. Responses to reaction time probes indexed differences in attentional allocation as a function of cognitive and affective variables in this paradigm. Taken together, the data suggest that presentation of a series of affective pictures of similar valence produces emotional reactions that are either maintained or sensitized across the temporal intervals used here but that do not habituate.

Startle reflex modification: emotion or attention?

Alternative interpretations of startle probe modulation by a pictorial foreground were tested: Either reflex amplitude varies as a function of modality-determined attention allocation, or, regardless of probe modality, reflex amplitude varies with the emotional valence of the foreground content. Thirty-six subjects viewed a series of 54 slides, divided into two 27-slide blocks. Each block consisted of nine exemplars of three independently rated emotional content categories--pleasant, neutral, and unpleasant. Startle probes, half visual (flashgun) and half acoustic (white noise), were presented unpredictably during and between slide presentations. Eyeblink reflexes, corrugator and orbicularis oculi muscle tension, heart rate, and skin conductance were recorded during a 6-s slide interval. Subjects subsequently rated the slides for emotional valence and arousal, and interest value. Free-viewing times were also recorded. Analysis of reflex response and all ancillary measures supported the hypothesis that the primary determinant of startle modulation was the emotional valence of foreground content.

Startle and emotion: lateral acoustic probes and the bilateral blink.

The affect-startle effect describes the modulation of the reflexive eyeblink response to a probe startle stimulus as a function of foreground emotional valence. Larger blinks occur during viewing of unpleasant slide foregrounds, relative to positive foregrounds. This effect has been obtained repeatedly using binaural acoustic startle probes. The current study examines this phenomenon for monaural probes administered to the left and right ears in separate blocks. Startle probes were presented during and between exposures to pleasant, neutral, and unpleasant slides, with the ear of presentation counterbalanced across subjects. Left monaural probes produced blink magnitudes that increased linearly from pleasant to unpleasant slide foregrounds, and appeared to be independent of attention or interest. Right monaural probes did not vary with foreground valence. These findings suggest that the startle probe indexes emotional processing that is lateralized in the central nervous system.

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.

Lateralized startle probes in the study of emotion.

Two experiments are reported in which affective modulation of the startle reflex elicited by monaurally presented acoustic probes was further examined. An earlier study in our laboratory obtained significant modulation by affect for probes presented to the left ear, but no significant effect for probes presented to the right ear. Experiment 1 replicated the procedures used in that experiment and obtained the same pattern of effects. Experiment 2 changed the presentation of monaural probes from a blocked to a mixed presentation and again obtained a similar pattern. Modulatory differences in reflex magnitude between pleasant and unpleasant stimuli were consistently large and reliable for reflexes elicited by left ear probes but weak and unreliable for reflexes elicited by right ear probes.