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Emotion-Modulated Startle Magnitude Covaries with Heart Rate Variability

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Emotion-Modulated Startle Magnitude Covaries with Heart Rate Variability Psychophysiology, 40 (2003), 306–313. Blackwell Publishing Inc. Printed in the USA. Copyright r 2003 Society for Psychophysiological Research The rhythm of the heart in the blink of an eye: Emotion-modulated startle magnitude covaries with heart rate variability ELISABETH RUIZ-PADIAL,a JOHN J. SOLLERS, III,b JAIME VILA,c and JULIAN F. THAYERb aDepartment of Psychology, University of Jae´ n, Jae´ n, Spain bThe National Institute on Aging, Baltimore, Maryland, USA cDepartment of Clinical Psychology, University of Granada, Granada, Spain Abstract Emotion-modulated startle is a robust phenomenon that has been demonstrated in a wide range of experimental situations. Similarly, heart rate variability (HRV) has been associated with a diverse range of processes including affective and attentional regulation. The present study sought to examine the relationship between these two important measures of affective behavior. Ninety female participants viewed pleasant, neutral, and unpleasant pictures while exposed to acoustic startle stimuli. The eyeblink startle was recorded both during the affective foregrounds and during intertrial intervals. HRV was assessed during a resting baseline and relationships between HRVand startle magnitudes examined. Results indicated that resting HRVwas inversely related to startle magnitude during both intertrial intervals and affective foregrounds. In addition, the participants with the highest HRVshowed the most differentiated emotion- modulated startle effects, whereas those with the lowest HRV, compared to those with the highest HRV, showed significantly potentiated startle to neutral foregrounds and marginally potentiated startle to pleasant foregrounds. The findings are consistent with models that posit that prefrontal cortical activity modulates subcortical motivation circuits. These results have important implications for the use of startle probe methodology and for HRV in the study of emotional regulation and dysregulation. Descriptors: Startle, Heart rate variability, Emotion, Parasympathetic The startle probe methodology has revolutionized the study of context of viewing of films (Jansen & Frijda, 1994), listening to emotional processes. This technique can be used with both sounds (Bradley & Lang, 2000), and the smelling of odors human and nonhuman investigations of emotion as well as in (Miltner, 1994). In addition, a wide range of characteristics of the studies of information processing and attention. Importantly, an foreground stimuli and of the startle probe have been emotion-modulated startle effect has been demonstrated. Lang investigated. Affective modulation of the startle reflex has been and colleagues have developed a motivational priming model demonstrated using picture durations range from brief (150 ms) that proposes aversive and appetitive motivational systems that to relatively long (6 s) durations as well as during affective either match or mismatch with the defensive startle response imagery, and does not depend on the actual perceptual presence elicited by a sudden, intense stimulus. Relative to neutral of the foreground stimulus (Bradley & Lang, 2000). In addition, foreground stimuli, foreground stimuli that engage the aversive the affective modulation effect appears very rapidly after picture motivational system potentiate startle responses whereas fore- onset (within 300 ms; Codispoti, Bradley, & Lang, 2001). More- ground stimuli that engage the appetitive motivational system over, the affective modulation of the startle reflex has been used inhibit startle responses (Bradley, Cuthbert, & Lang, 1999). to investigate a wide range of individual difference variables The factors that influence the modulation of the startle reflex including persons with specific phobias, anxiety disorders, have been extensively investigated. Bradley et al. (1999) have schizophrenia, psychopathology, and depression (Allen, Trinder, recently summarized this vast literature. Affective modulation of & Brennan, 1999) as well as the personality of the participants the startle reflex has proven to be one of the most robust (Corr et al., 1995). Furthermore, stimulation of right hemisphere phenomena in psychophysiology. Whereas the affective modula- neural structures has been consistently associated with greater tion of the startle reflex has been most often demonstrated in the acoustic startle potentiation in the context of aversive compared context of picture viewing, it has also been demonstrated in the to appetitive stimuli (Bradley et al., 1999). In summary, the emotion- modulated startle effect has shown itself to be remarkably Address reprint requests to: Julian F. Thayer, NIA/GRC/LPC, 5600 consistent in a wide variety of research settings. Nathan Shock Drive, Baltimore, MD 21224, USA. E-mail: The detailed understanding of the neural circuitry underlying [email protected]. the affective modulation of the startle reflex helps to explain the 306 Startle and HRV 307 robustness of this phenomenon. Much of this knowledge has defensive reactions (HRacceleration) to the presentation of been gained in the investigation of animal models, but recent threat-related words (Thayer et al., 2000). In another study, brain lesion and neuroimaging studies in humans have also dental phobics with higher levels of vagally mediated HRV advanced our understanding of the affective modulation of the compared to those with lower levels of HRV showed greater startle reflex. The motivational model of Lang hypothesizes that inhibition of prepotent responses in a Stroop paradigm as the emotion-modulated startle effects are the result of emotional indexed by faster reaction times to color-incongruent and threat- priming of largely subcortical aversive and appetitive circuits. related words (Johnsen et al., in press). These results suggest that Davis and associates have investigated the acoustic startle reflex high levels of vagally mediated HRV are associated with better circuit in great detail in rats although less is known about humans affective and attentional regulation. (Davis, Walker, & Lee, 1997). Based on this rat model, they have The neural origins of cardiac autonomic modulation have also hypothesized that a primary, spinal circuit that shows habitua- been investigated. A set of neural structures termed the central tion and a secondary circuit that does not readily habituate autonomic network (CAN) has been identified. Structurally, the involving the central nucleus of the amygdala forms the basis of CAN includes the anterior cingulate, insular, and ventromedial the startle reflex circuitry. Importantly, this second circuit allows prefrontal cortices, the central nucleus of the amygdala, the the startle reflex to be repeatedly modulated (without habitua- paraventricular and related nuclei of the hypothalamus, the tion) by activity of the central nucleus of the amygdala. The periaquaductal gray matter, the parabrachial nucleus, the nucleus resistance to habituation of the affective modulation of the startle of the solitary tract (NTS), the nucleus ambiguus, the ventrolateral reflex in humans supports this model (see Bradley et al., 1999) medulla, the ventromedial medulla, and the medullary tegmental and highlights the importance of the central nucleus of the field. The primary output of the CAN is mediated through the amygdala in the affective modulation of the startle reflex. preganglionic sympathetic and parasympathetic neurons. Impor- Similarly, the report of a person with damage to the right tantly, these neurons innervate the heart via the stellate ganglia amygdala showing a reduced acoustic startle reflex and a failure and the vagus nerve. The interplay of these inputs to the sino-atrial to show affective startle modulation suggests that the neural node of the heart is the source of the complex variability that circuitry identified in rats may generalize to humans (Angrilli characterizes the heart rate time series (Saul, 1990). Thus, the et al., 1996). In summary, the neural circuitry of the startle reflex output of the CAN is directly linked to HRV. suggests that the affective modulation is achieved via a pathway Recent neuroimaging and pharmacological blockade studies involving the central nucleus of the amygdala. have investigated the neural origins of HRV. Lane, Reiman, The study of heart rate variability (HRV) has also demon- Ahern, and Thayer (2001) have presented evidence that medial strated a far-reaching utility in the study of emotional, prefrontal activity is associated with HRV. Vagally mediated attentional, and autonomic processes. Due to the differential HRV is considered to reflect antagonism of sympathoexcitatory frequency characteristics of the sympathetic and parasympa- influences (Uijtdehaage & Thayer, 2000). To explore its central thetic neural modulation of heart rate, spectral analysis of the neural substrates, a spectrally derived index of vagally mediated heart rate time series allows us to examine these neural influences. HRV (HF-HRV) was correlated with measures of cerebral blood Modulation at frequencies from 0.03 to 0.15 Hz corresponds flow (rCBF) derived from positron emission tomography (PET) primarily to baroreceptor-mediated regulation of blood pressure. in 12 healthy women during emotion and neutral conditions. This low frequency component involves modulation by both During the emotion minus neutral conditions, HF-HRV sympathetic and parasympathetic (vagal) influences. Modula- correlated with rCBF in the medial prefrontal cortex and the tion at frequencies greater than 0.15 Hz are respiration
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