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© 2009 Federation of European Psychophysiology Societies S. Rodríguez-Ruiz et al.: Effect Journal of Heart of Psychophysiology Rate Variability2009; in Cho Hogrefe Vol. colate 23(3):95–103 Publishing Cravers

Effect of Heart Rate Variability on Defensive Reaction and Eating Disorder Symptomatology in Chocolate Cravers Sonia Rodríguez-Ruiz1, Elisabeth Ruiz-Padial2, Nieves Vera1, Carmen Fernández1, Lourdes Anllo-Vento1, and Jaime Vila1 1

University of Granada, Spain, 2University of Jaén, Spain

Abstract. The study examines the effect of heart rate variability (HRV) on the cardiac defence response (CDR) and eating disorder symptomatology in chocolate cravers. Female chocolate cravers (n = 36) and noncravers (n = 36) underwent a psychophysiological test to assess their HRV during a 5-min rest period, followed by three trials to explore the CDR, elicited by an intense white noise, during the viewing of chocolate, neutral, and unpleasant pictures. After the test, participants completed a questionnaire to measure eating disorder symptomatology. The HRV was inversely related to the magnitude of the CDR and to eating disorder symptomatology in chocolate cravers. In addition, the HRV was inversely related to the magnitude of the CDR when viewing unpleasant pictures but not to neutral or chocolate ones, across all participants. These findings support the idea that poor autonomic regulation, indexed by low HRV, plays a relevant role in food craving and uncontrolled eating behavior. Keywords: chocolate craving, cardiac defence response, heart rate variability, eating disorder symptomatology

Introduction Food craving has been defined as a motivational state subjectively experienced as an irresistible desire to consume a certain type of food (Cepeda-Benito & Gleaves, 2001; Tiffany, 1995). This desire has been associated with eating disorder symptomatology such as compulsive ingestion, binge eating, and purging (Gendall, Joyce, Sullivan, & Bulik, 1998; Gendall, Sullivan, Joyce, & Bulik, 1997; Guertin, 1999). Food craving might be simultaneously triggered by positive (e.g., pleasant properties of food) and negative (e.g., unpleasant properties of food restriction or negative emotions) stimuli (Macht & Müller, 2007; Parker & Crawford, 2007; Parker, Parker, & Brotchie, 2006; Waters, Hill, & Waller, 2001a,b). This ambivalent character of food-related cues may explain the positive and negative emotional states frequently associated with excessive food consumption (Hetherington, 2001; Rogers & Smit, 2000). From this perspective, food craving can be considered an emotional regulatory mechanism (Cartwright & Stritzke, 2008; Müller, Dettmer, & Macht, 2008; Roger & Smit, 2000). Different methodologies have been applied to explore the physiological regulatory mechanisms underlying food craving. Cue reactivity studies have explored drug and food craving as a classical conditioned response (Drummond, Tiffany, Glautier, & Remington, 1995; Jansen, 1994, 1998). Hogrefe Publishing

Following the cue reactivity model, the physiological cephalic phase responses elicited during exposure to food cues (increase in heart rate, gastric activity and salivation), presumably acquired by Pavlovian association, prepare the body for the expected meal and are subjectively experienced as craving in normal subjects (Nederkoorn, Smulders, & Jansen, 2000). Nevertheless, in contrast to predictions, greater physiological reactivity was not found to be related to subjective craving in restrained eaters (Nederkoorn & Jansen, 2002). A different set of cue reactivity studies have used the startle probe paradigm (Lang, 1995) to examine whether the basic motivational system underlying food craving is appetitive or aversive. Drobes and colleagues (2001) found that food-deprived participants assessed food pictures as pleasant, but that their eye blink startle reflex, a defensive motor reaction, was enhanced during viewing of these images, suggesting the presence of an aversive motivational mechanism activated by food cues. In contrast, Hawk, Baschnagel, Ashare, and Epstein (2004) used a similar paradigm but observed attenuation of the startle reflex while deprived participants were exposed to in vivo food cues, supporting the involvement of an appetitive motivational mechanism in food craving. However, a third study using a similar methodology (Rodríguez, Fernández, Cepeda-Benito, & Vila, 2005) reported both augmentation and attenuation of defensive reflexes in Journal of Psychophysiology 2009; Vol. 23(3):95–103 DOI 10.1027/0269-8803.23.3.95

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S. Rodríguez-Ruiz et al.: Effect of Heart Rate Variability in Chocolate Cravers

chocolate cravers: During the viewing of chocolate images, the cardiac defence response (CDR) was attenuated and the startle reflex augmented, suggesting the presence of both appetitive and aversive mechanisms. Neuroimaging techniques have also been used to study the regulatory mechanisms underlying food craving. A large number of studies have identified a set of different regions (e.g., hippocampus, insula, caudate, amygdala, nucleus accumbens, anterior cingulate, and orbitofrontal cortices) that are activated or deactivated by drug and food cues (Arana, Parkinson, Hinton, Holland, & Owen, 2003; Garavan et al., 2000; Goldstein & Volkow, 2002; Kalivas & Volkow, 2005; LaBar et al., 2001; Lubman, Yücel, & Pantelis, 2004; Pelchat, Johnson, Chan, Valdez, & Ragland, 2004; Rolls & McCabe, 2007; Small, Zatorre, Dagher, Evans, & Jones-Gotman, 2001; Small, Gregory et al., 2003a; Small, Jones-Gotman, & Dagher, 2003b; Volkow et al., 2003; Wang et al., 2004). Thus, there have been reports of the simultaneous deactivation of prefrontal areas involved in emotion regulation via inhibitory control on the amygdala (Bechara, Damasio, & Damasio, 2000; LeDoux, 2000; Lubman et al., 2004) and activation of the opioid and mesolimbic dopaminergic regions involved in appetitive and reward motivation (Berridge, 1996; Robinson & Berridge, 2003). These findings suggest that both mechanisms (emotional dysregulation and appetitive sensitization) can act simultaneously and contribute to maintaining food craving and uncontrolled eating behaviors. These psychophysiological and neuroimaging studies on food or drug craving manipulated participants’ craving states in order to examine transient changes in the underlying neural mechanisms. In most of these studies, however, participants were also selected based on their past history with the substance, hence assuming that a stable trait in relation to the substance would be congruent with the transient physiological mechanisms activated by the substance. In the case of chocolate craving, there is some evidence that craving is both a stable trait and a transient state, having similar underlying mechanisms. In one of these studies, Small and colleagues (2001) examined changes in brain activity in volunteers who usually ate chocolate beyond satiation (stable trait). They observed different brain region activations depending on whether they ate chocolate when they were highly motivated to eat and rated the chocolate as pleasant, or when they were highly motivated to stop eating and rated the chocolate as unpleasant (transient state). Despite the above studies, further evidence is required to confirm the hypothesis that poor emotional regulation plays a role in food craving. Heart rate variability (HRV) has recently attracted the interest of scientists as an index of autonomic and emotional regulation. Thayer and Lane (2000) and Thayer and Siegel (2002) proposed a model of neurovisceral integration in which a network of neural structures associated with emotional and autonomic regulation is related to HRV via connections from the prefrontal cortex to the amygdala, and from the amygdala to the symJournal of Psychophysiology 2009; Vol. 23(3):95–103

pathetic and parasympathetic innervations of the heart. Numerous authors have found a negative association between vagally mediated HRV, measured at rest, and poor psychological and physiological functioning, including conditions characterized by a lack of impulse control (Allen, Matthews, & Kenyon, 2000; Ingjaldsson, Laberg, & Thayer, 2003; Thayer, Smith, Rossy, Sollers, & Friedman, 1998). Experimental data also support a relationship between HRV and emotional regulation. High vagally mediated HRV has been associated with larger orienting responses but faster habituation to nonthreat stimuli, whereas low HRV has been related to a failure to habituate (hypervigilance) and to greater defensive reactions (Ruiz-Padial, Sollers, Vila, & Thayer, 2003; Thayer, Friedman, Borkovec, Johnsen, & Molina, 2000). In this context, HRV is considered as a measure of a stable trait of emotional regulation The CDR has also been studied as an index of autonomic and emotional regulation (Cook & Turpin, 1997; Jung-Stalmann, 2003; Reyes, Godoy, & Vila, 1993; Vila et al., 2007). It is a complex pattern of heart-rate changes in response to intense aversive stimulation, lasting for 80 s, which is mediated by both parasympathetic and sympathetic mechanisms. It comprises two distinct accelerative components, a first acceleration of short latency (peak around second 3), vagally mediated; and a second one of long latency (peak around second 35), sympathetically mediated, with a decelerative component after each acceleration (Vila, Fernández, & Godoy, 1992). This response pattern, like the startle reflex, appears to show emotional modulation. Viewing unpleasant pictures (e.g., photographs of phobic animals or mutilated bodies) just before presentation of the noise, which constituted the defence stimulus, modifies the response pattern, increasing the magnitude and duration of a single accelerative component that lasts for around 40 s, followed by a final deceleration. Viewing pleasant (e.g., romantically engaged couples) and neutral (household objects) pictures just before presentation of the defence noise attenuates the response pattern, reducing the magnitude of the accelerative components (Sánchez et al., 2002). In this context, the CDR is considered as a measure of a transient state of emotional regulation. The above evidence suggests that food craving may be associated with eating disorder symptomatology that derives not only from appetitive sensitization, but also from a deficit in the regulatory mechanisms of emotions via a lack of inhibitory control by the prefrontal cortex. Vagally mediated HRV has been shown to be a reliable index of autonomic and emotional regulation and is probably related to the same inhibitory mechanism. We hypothesized that vagally mediated HRV in high food cravers would show an inverse association (1) with the magnitude of the cardiac defence response while viewing affective pictures and (2) with indices of eating disorder symptomatology. No such association was expected in low food cravers. Accordingly, it was anticipated that high food cravers with low HRV would show a higher CDR and greater eating disorder Hogrefe Publishing


symptomatology. With this background, the objective of the present study was to test the hypothesis that poor autonomic and emotional regulation plays a role in food craving and eating disorder symptomatology.

Method Participants A total of 72 female students with a mean age of 21.0 years (SD = 2.61) volunteered to participate. They were selected from an initial pool of 454 students who reported on their chocolate cravings using the Spanish adaptation of the Food Craving Questionnaire-Trait (Cepeda-Benito, Fernández, & Moreno, 2003; Rodríguez et al., 2007). Two groups of 36 students who scored, respectively, within the top and bottom tentiles of FCQ-T score distribution were assigned to the high and low chocolate craving groups (high craving: M = 150.72, SD = 21.21; low craving: M = 53.69, SD = 7.75). Their body mass index (BMI) was within the normal range (high cravers: M = 22.4; SD = 3.37; low cravers: M = 21.91; SD = 3.23; F(1, 70) = 0.40, p > .52). They were otherwise healthy without visual or auditory deficits.

Psychophysiological Measurements Participants attended a single laboratory session to measure HRV at rest and the magnitude of the CDR while viewing affective pictures. The test consisted of a 10-min baseline period with recording of HRV during the last 5 min, followed by three CDR trials. After the last CDR trial, participants had an additional series of trials to examine affective modulation of the eye-blink startle response. The data on eye-blink startle were reported elsewhere (Rodríguez et al., 2005) and are thus not included in the present paper. The pictures used in the three defence trials were selected according to the Spanish calibration of the International Affective Picture System (Moltó et al., 1999; Vila et al., 2001): a chocolate (code: 7340), an unpleasant (code: 6831), and a neutral (code: 7233) picture. Each CDR trial began with a 15-s baseline period followed by a 6 s picture presentation, with the order of presentation counterbalanced across participants within each group. The auditory stimulus (white noise of 105 dB intensity, 500 ms duration and instantaneous risetime) was presented at 3.5 s from picture onset and data collection continued for 80 s after the picture presentation ended. The length of the intertrial intervals varied randomly between 1 s and 4.5 s. A Grass polygraph (model Rps 7c8b, Grass Instrument Company, Astro-Med, West Warwick, RI, USA) was used to record the ECG (lead II) using a 7P4 preamplifier. Resting HRV was obtained by using the R-R intervals (time in Hogrefe Publishing

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ms between R waves of each beat from the heart) during the last 5 min of the 10-min rest period. Time domain analysis (nonspectral) provided estimates of mean HR and HRV (variation index) and included the mean R-R interval, the standard deviation of all normal R-R intervals and the root mean square of successive differences of R-R intervals (RMSSD) (Task Force of the European Society, 1996). In the present study, the RMSSD was obtained from the HR data, and the complete HR signal was carefully edited using visual checks and manual corrections of individual R-R intervals. The CDR was obtained following the procedure outlined by Vila and colleagues (1992) and used in previous studies. R-R intervals were transformed into mean HR/s. The 80 HR values after the onset of the defence-evoking stimulus were then expressed in terms of differential scores with respect to baseline level (15 s before stimulus) and reduced to the medians of 10 time intervals: two of 3 s, two of 5 s, three of 7 s, and three of 13 s. This procedure facilitates the statistical analysis without altering the response form. It also allows examination of changes in the response pattern during the 80-s period without focusing on any specific component. The sequence of stimulus presentations and the acquisition of physiological data were controlled by the VPM software program (Cook, 1994). Pictures were presented using a Kodak Ektapro slide projector (model 9020, Eastman Kodak Company, Rochester, NY, USA), which presented 145 cm × 95 cm images at 3-m distance from the participant. A Coulbourn Sound Stimulator (model V85-05, Coulbourn Instruments LLC, Allentown, PA, USA) was used to produce the defence stimulus, which was presented to the subject through earphones (model TDH49P, Telephonics, Farmingdale, NY, USA). Sound intensity was calibrated with a sonometer (model 2235, Brüel and Kjaer, Naerum, Denmark) and an artificial ear (model 4153, Brüel and Kjaer, Naerum, Denmark).

Self-Report Measurements Food Chocolate Craving Questionnaire-Trait (FCCQ-T) The FCCQ-T (39 items) measures the intensity of chocolate cravings using a 6-point scale. The instructions and items of the instruments ask respondents about cravings, urges, or desires for chocolate. Full-scale totals can be calculated by simply adding the corresponding item scores. In the present sample, the overall α for the FCCQ-T was 0.98. Evidence of the construct validity of the instrument includes findings of predictive, convergent, and discriminant validity in both Spanish- and English-speaking samples (Cepeda-Benito, Gleaves, Fernández et al., 2000; CepedaBenito, Gleaves, Williams, & Erath, 2000b; Rodríguez et al., 2007). Journal of Psychophysiology 2009; Vol. 23(3):95–103

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Eating Attitude Test (EAT)

Results

The EAT is a 40-item instrument designed to assess a broad range of eating disorder symptoms. It is useful as a clinical screening device (Garner & Garfinkel 1979). Respondents rate each item using a 6-point Likert scale ranging from never to always. The score can range from 0 to 120, with higher scores indicating higher symptom levels. Cutoffs of 30 and 50 characterize at risk and clinical populations (Mintz & O’Halloran 2000). In the present sample, the overall α for the EAT was 0.87. The EAT-40 has been validated and extensively used in Spanish-speaking populations (Castro, Toro, Salamero, & Guimera, 1991).

HRV No significant differences in HRV index classification (high or low) were found between the high- and low-craving groups, F(1, 70) = 0.31, p > .58 (see Table 1).

Table 1. Mean scores (M) and standard deviations (SD) of the heart rate variability index as a function of craving in the low and high heart rate variability groups Low HRV

Procedure Data were collected within a single session. Individual sessions could start at one of six times (9:30, 11:00, 12:30, 16:00, 17:30 or 19:00 hours), with the times equally balanced across the high and low chocolate craving groups. Participants received a brief description of the study before giving their written informed consent. After the specific instructions were read, the skin under the electrodes was cleaned and the electrodes, filled with electrolyte paste, were attached. The physiological recording was then checked, the earphones placed, and the participant was left alone in a semidarkened room. Participants were asked to breathe normally during the test and keep their eyes open looking at the screen in front of them. After the test, the electrodes were removed and participants completed the EAT.

Statistical Analysis Participants were classified as having high or low HRV according to the median split of the HRV index. Then, the modulation of HRV on the evocation of the CDR in the high-craving group was analyzed using a mixed 2 × 2 × 3 (× 10) between-group with repeated measures ANOVA. The between-group factors were HRV (high and low variability groups), Craving (high- and low-craving groups) and Picture Type (chocolate, neutral, and unpleasant). The repeated measures factor was Time (the 10 heart rate intervals representing the CDR). The Greenhouse-Geisser ε correction was applied for the repeated measure factor. Likewise, the modulation of HRV on eating attitudes in the high-craving group was analyzed by means of a 2 × 2 ANOVA with two between-group factors, HRV (high and low variability groups) and Craving (high- and low-craving groups). In addition, correlations between heart rate variability and cardiac defence and among heart rate variability, eating attitudes, and craving were analyzed using Pearson’s product moment coefficient. The level of significance was set at .05 for all analyses. Journal of Psychophysiology 2009; Vol. 23(3):95–103

High HRV

Craving groups

M

SD

M

SD

High craving (N)

2.66 (19)

0.43

5.39 (17)

1.63

Low craving (N)

3.01 (17)

0.53

5.21 (19)

1.65

Total (N)

2.82 (36)

0.51

5.30 (36)

1.62

Cardiac Defence The HRV (2) × Craving (2) × Picture (3) × Time (10) ANOVA yielded a significant main effect of Time (F(9, 540) = 26.18, p < .0001) and three significant interaction effects (Craving × Picture, F(1, 60) = 3.87, p < .03; Time × Craving × HRV, F(9, 540) = 2.07, p < .05; and Time × Picture × HRV, F(18, 540) = 2.08, p < .03). Results for the Craving × Picture interaction were presented elsewhere (Rodríguez et al., 2005) and are thus not reported here.

Cardiac Defence as a Function of HRV Results for the Time × Craving × HRV interaction are represented in Figure 1. As can be observed, only the low HRV participants in the high-craving group show a potentiated CDR (prolonged acceleration followed by a final deceleration). In the remaining groups the response is predominantly decelerative after the initial acceleration. Simple effects analysis of this interaction showed a significant Time × HRV effect only in the high-craving group (F(18, 270) = 2.56, p < .04). The same effect in the lowcraving group was not significant (F(18, 270) = .07, ns). Differences between the low and high HRV participants in the high-craving group were found in time intervals 3 (F(1, 34) = 7.82, p < .008), 4 (F(1, 34) = 10.83, p < .002), 5 (F(1, 34) = 4.44, p < .04), and 10 (F(1, 34) = 4.67, p < .04). In all these intervals, low HRV participants displayed a greater heart rate response than did high HRV participants. Hogrefe Publishing


Figure 1. Cardiac defence response as a function of the heart rate variability in the high (top) and low (bottom) craving groups.

Cardiac Defence as a Function of Picture Type Results for the Time × Picture × HRV interaction are displayed in Figure 2. No differences were found between high and low HRV groups (F(1, 60) = 1.376, p < .245). However, as can be observed, only the low HRV participants, across both craving groups, showed a potentiated CDR (prolonged acceleration followed by a final deceleration) when observing the unpleasant picture. When observing the neutral and the chocolate picture, the response is either more decelerative (neutral picture) or less accelerative (chocolate picture). No major differences were observed in the CDR when high HRV participants were viewing the pictures, when the response was predominantHogrefe Publishing

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Figure 2. Cardiac defence response as a function of the picture type (unpleasant, chocolate, and neutral) in the low (top) and high (bottom) heart rate variability groups.

ly decelerative after the initial acceleration. Simple effects analysis showed significant Time × Picture effects only in the low HRV group (F(18, 270) = 3.12, p < .003). The same analysis in the high HRV group was not significant (F(18, 270) = 1.1, ns). Differences between the three pictures in the low HRV group were found at time intervals 2 (F(2, 33) = 10.56, p < .0001) and 3 (F(2, 33) = 10.72, p < .0001). In both intervals, pairwise comparisons (Tukey test) showed that low HRV participants displayed a significantly greater heart rate accelerative response when observing the unpleasant picture than when observing the neutral (p < .0001) and chocolate (p < .05) ones. Journal of Psychophysiology 2009; Vol. 23(3):95–103

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higher eating disorder symptomatology. When the same analysis was performed for each craving group separately, the negative correlation remained significant in the highcraving group (–.230, p < .05), but not in the low-craving group (–.082, p > .60). Finally, a significant positive correlation was found between craving and eating attitudes across all participants (.326, p < .005). Participants with higher scores in the craving questionnaire reported higher eating disorder symptomatology. This positive correlation disappeared when each craving group was analyzed separately (p > .50).

Discussion

Figure 3. Mean scores in the Eating Attitude Test as a function of heart rate variability in the high and low craving groups.

Eating Attitudes The HRV (2) × Craving (2) ANOVA yielded significant effects of Craving (F(1, 68) = 9.38, p < .005) and Craving × HRV interaction (F(1, 68) = 6.59, p < .01). Figure 3 displays the Craving × HRV interaction. As can be observed, the low HRV participants in the high-craving group showed a greater score in the Eating Attitude Test versus the other three groups. Pairwise comparisons (Tukey test) revealed significant differences only between the low HRV/high-craving group and the three remaining groups: high HRV/high-craving group (p < .04), low HRV/lowcraving group (p < .001), and high HRV/low-craving group (p < .01).

Correlation Analysis Significant negative correlations were found, across all participants (N = 72), between HRV and cardiac defence at time intervals 3 (–.233, p < .05), 4 (–.309, p < .008), and 5 (–.230, p < .05). Participants with lower HRV showed higher accelerative heart rate response. When the same analysis was performed for each craving group separately (N = 36), significant negative correlations were observed in the high-craving group at time intervals 3 (–.368, p < .03), 4 (–.447, p < .006), and 10 (–.351, p < .04). In the low-craving group, none of the correlations were significant (p > .25). A significant negative correlation was also found between HRV and eating attitudes across all participants (–.229, p < .05). Participants with lower HRV reported Journal of Psychophysiology 2009; Vol. 23(3):95–103

HRV was significantly associated with the cardiac defence response that was especially marked in chocolate cravers. Only chocolate cravers with low HRV showed a potentiated accelerative response to the defence evoking stimulus, irrespective of picture content. The association between HRV and cardiac defence in chocolate cravers was also indicated by the negative correlations found between these two variables along the 10 time intervals of the cardiac response in the high-craving group. On the other hand, only low HRV participants, irrespective of craving group, showed the prolonged accelerative response while viewing the unpleasant picture. The potentiated response reproduces the pattern of heart rate changes reported in previous studies using unpleasant and phobic pictures (Sánchez et al., 2002; Vila et al., 2003), i.e., augmentation of a single accelerative component with no initial deceleration. An unexpected result was the absence of a stronger defence response when chocolate cravers with low HRV viewed the chocolate picture. Several explanations are possible. It can be argued that food cravers with poor emotion regulation (low HRV) poorly regulate their negative emotions, which may explain the stronger CDR to negative pictures alone. Alternatively, they might tend to regulate their negative feelings with overeating, which can in turn improve their mood (Hetherington, 2001; Parker & Crawford, 2007; Rogers & Smit, 2000). In this case, food itself is not coupled with negative emotions, and no defence reactions to food pictures would be expected. It is also possible that any participant who scores high on pathology (food craving, eating disorder, anxiety, drug use) in combination with poor emotional regulation has a stronger CDR to negative pictures. Thus, the stronger reactivity to negative pictures would not be specific to food cravers, but a mere indicator of psychopathology in individuals with poor emotion regulation. HRV was also associated with eating disorder symptomatology in chocolate cravers. Eating disorder symptomatology was found to be greater in chocolate cravers with low HRV than in those with high HRV or noncravers. The role of HRV in eating disorder symptomatology was also indicated by the negative correlation found between these Hogrefe Publishing


two variables in the high-craving group but not in the lowcraving group. The presence of more severe eating symptomatology in people with high food craving has been reported in several studies (Gendall et al., 1997, 1998; Rogers & Smit, 2000). A similar association has been described between food craving and some eating disorders, including obesity and bulimia nervosa (Guertin, 1999). Furthermore, it has been reported that high food cravers attempt to cope and regulate negative emotions derived from their ambivalence to food cues (Parker et al., 2006). These reports are consistent with the positive correlation found in our study between chocolate craving and eating disorder symptomatology and with the role that HRV plays in this relationship. In general, our finding that chocolate cravers with low vagally mediated HRV show a significant association with a greater defence response and eating disorder symptomatology supports the idea that food craving and uncontrolled eating behaviors are related to inadequate emotional regulation. Low HRV has been considered an index of poor autonomic and emotional regulation via a lower inhibitory control on the amygdala and other limbic structures by the prefrontal cortex (Thayer & Siegel, 2002). Recent neurobiological studies provide evidence on the role of the orbitofrontal cortex and anterior cingulate gyrus in craving experience and binging behaviors (Goldstein & Volkow, 2002; Lubman et al., 2004). These frontal cortical structures show substantial overlapping with the emotion circuit identified by Damasio and colleagues (Damasio, 1998) and with the central autonomic network proposed by Thayer and Siegle (2002). Functionally, both circuits regulate emotions and autonomic reactions via their projections to the amygdala and other limbic regions. The same circuits have been found to be involved in HRV. Lane, Reiman, Ahern, and Thayer (2001) performed neuroimaging and pharmacological blockade studies and reported an association between medial prefrontal activity and HRV. They correlated a spectrally derived index of vagally mediated HRV (high frequency HRV) with cerebral blood flow (rCBF) measured by positron emission tomography (PET), finding that emotional arousal was associated with a decrease in HRV and concomitant decreases in brain activation in the medial prefrontal cortex. The theoretical and practical implications of our results should take into consideration that our findings might be specific to chocolate craving, and that it might not be possible to extrapolate them to other foods. Chocolate is the type of food people most frequently crave, but its nutrient and sensory characteristics differ markedly from those of other types of food. Account must also be taken of the use of a methodology that did not consider personal preferences for the selected chocolate cue. There are more than 20 types of chocolate, and chocolate cravers usually have their own preferences (e.g., dark or milk chocolate). In addition, the noncausal nature of our study should be emphasized. Thus, the inverse relationship of HRV with eating symptomatology and defensive reactivity in chocolate cravers should not be interpreted as if low HRV is the cause of the Hogrefe Publishing

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eating symptomatology or the greater defence reaction. The opposite causal relationship is also possible. Keeping these limitations in mind, a practical implication of our findings is that HRV training, aimed at increasing vagal control, might be a useful method to increase emotional regulation strategies and reduce the irrational desire to consume food. A number of nonpharmacological techniques have been used to increase HRV, including thought field therapy (Callahan, 2001; Pignotti & Steinberg, 2001), aerobic training (Lazoglu, Glace, Gleim, & Coplan, 1996; Russoniello et al., 2002), breathing techniques (Lehrer, Sasaki, & Saito, 1999), and HRV biofeedback (McCraty & Tomasino 2004). HRV biofeedback has been proposed as a powerful tool to help individuals learn emotional self-regulation skills. Nolan et al. (2005) reported positive effects of HRV biofeedback as a complement to treatment programs for chronic stress, anxiety, depression, and physical disorders (e.g., fibromyalgia, hypertension, asthma, and cardiac arrhythmias). In summary, HRV was inversely associated with defensive reactions and eating disorder symptomatology in chocolate cravers. This finding supports the hypothesis that poor emotional regulation plays a relevant role in food craving and uncontrolled eating behavior.

Acknowledgments This research was supported by grants from the Spanish Ministry of Science and Technology (projects BSO20013015, SEJ2004-07956/PSI, and SEJ2005-06699/PSI) and the Junta de Andalucía (research group HUM-388).

References Allen, M.T., Matthews, K.A., & Kenyon, K.L. (2000). The relationships of resting baroreflex sensitivity, heart rate variability and measures of impulse control in children and adolescents. International Journal of Psychophysiology, 37, 185–194. Arana, F.S., Parkinson, J.A., Hinton, E., Holland, A.J., & Owen, A.M. (2003). Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection. Journal of Neuroscience, 23, 9632–9638. Berridge, K.C. (1996). Food reward: Brain substrates of wanting and linking. Neuroscience and Biobehavioral Reviews, 20, 1–25. Bechara, A., Damasio, H., & Damasio, A.R. (2000). Emotion, decision making and the orbitofrontal cortex. Cerebral Cortex, 10, 295–307. Callahan, R.J. (2001). The impact of thought field therapy on heart rate variability. Journal of Clinical Psychology, 57, 1153–1170. Cartwright, F., & Stritzke, W.G.K. (2008). A multidimensional ambivalence model of chocolate craving: Construct validity an associations with chocolate consumption and disordered eating. Eating Behaviors, 9, 1–12. Journal of Psychophysiology 2009; Vol. 23(3):95–103

102


Castro, J., Toro, J., Salamero, M., & Guimera, E. (1991). The eating attitude test: Validation of the Spanish version. Evaluación Psicológica, 7, 175–189. Cepeda-Benito, A., & Gleaves, D.H. (2001). A critique of food cravings research: Theory, measurement, food intake. In M.M. Hetherington (Ed.), Food cravings and addition. Surrey, UK: Leatherhead. Cepeda-Benito, A., Fernández, M.C., & Moreno, S. (2003). Relationship of gender and eating disorder symptoms to reported cravings for food: Construct validation of state and trait craving questionnaires in Spanish. Appetite, 40, 47–54. Cepeda-Benito, A., Gleaves, D.H., Fernández, M.C., Vila, J., Tara, L., & Reynoso, J. (2000). The development and validation of Spanish versions of the state and trait food cravings questionnaires. Behavior Research and Therapy, 38, 1125–1138. Cepeda-Benito, A., Gleaves, D.H., Williams, T.L., & Erath, S.T. (2000). The development and validation of the state and trait food cravings questionnaires. Behavior Therapy, 31, 151–173. Cook, E.W., III. (1994). VPM reference manual [Computer software]. Birmingham, AL: Author. Cook, E.W., III., & Turpin, G. (1997). Differentiating orienting, startle, and defence response: The role of affect and its implications for psychopathology. In P.J. Lang, R.F. Simons, & M.T. Balaban (Eds.), Attention and orienting (pp. 137–164). Hillsdale, NJ: Erlbaum. Damasio, A.R. (1998). Emotion in the perspective of an integrated nervous system. Brain Research Reviewers, 26, 83–86. Drobes, D.J., Miller, E.J., Hillman, C.H., Bradley, M.M., Cuthbert, B.N., & Lang, P.J. (2001). Food deprivation and emotional reactions to food cues: Implications for eating disorders. Biological Psychology, 57, 153–177. Drummond, D.C., Tiffany, S.T., Glautier, S., & Remington, B. (1995). Addictive behavior: Cue exposure theory and practice. Chichester: Wiley. Garavan, H., Pankiewicz, J., Bloom, A., Jung-Ki, C., Sperry, L., Ross, T.J. et al. (2000). Cue-induced cocaine craving: Neuroanatomical specificity for drug users and drug stimuli. American Journal of Psychiatry, 157, 1789–1798. Garner, D.M., & Garfinkel, P.E. (1979). The Eating Attitude Test: An index of the symptoms of anorexia nervosa. Psychological Medicine, 9, 273–279. Gendall, K.A., Joyce, P.R., Sullivan, P.F., & Bulik, C.M. (1998). Food cravers: Characteristics of those who binge. International Journal of Eating Disorders, 23, 353–360. Gendall, K.A., Sullivan, P.F., Joyce, P.R., & Bulik, C.M. (1997). Food cravings in women with a history of anorexia nervosa. International Journal of Eating Disorders, 22, 403–409. Goldstein, R.Z., & Volkow, N.D. (2002). Drug addiction and its underlying neurobiological basis: Neuroimaging evidence for the involvement of the frontal cortex. The American Journal of Psychiatry, 159, 1642–1652. Guertin, T.L. (1999). Eating behavior of bulimics, self-identified binge eaters and noneating disordered individuals: What differentiates these populations? Clinical Psychology Review, 19, 1–25. Hawk, L.W., Baschnagel, J.S., Ashare, R.L., & Epstein, L.H. (2004). Craving and startle modification during in vivo exposure to food cues. Appetite, 43, 285–294. Ingjaldsson, J.T., Laberg, J.C., & Thayer, J.F. (2003). Reduced heart rate variability in chronic alcohol abuse: Relationship Journal of Psychophysiology 2009; Vol. 23(3):95–103

with negative mood, chronic thought suppression, and compulsive drinking. Biological Psychiatry, 54, 1427–1436. Jansen, A. (1994). The learned nature of binge eating. Appetite, 8, 193–211. Jansen, A. (1998). A learning model of binge eating: Cue reactivity and cue exposure. Behavior Research and Therapy, 36, 257–272. Jung-Stalmann, B. (2003). The cardiac defence response, personality, stress management. Hamburg: Logos. Kalivas, P.W., & Volkow, N.D. (2005). The neural basis of addiction: A pathology of motivation and choice. The American Journal of Psychiatry, 162, 1403–1413. Keppel, G. (1991). Design and analysis. A researcher’s handbook. Upper Saddle River, NJ: Prentice Hall. LaBar, K.S., Gitelman, D.R., Parrish, T.B., Kim, Y.H., Nobre, A.C., & Mesulam, M.M. (2001). Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behavioral Neuroscience, 115, 493–500. Lane, R.D., Reiman, E.M., Ahern, G.L., & Thayer, J.F. (2001). Activity in medial prefrontal cortex correlates with vagal component of heart rate variability during emotion. Brain Cognition, 47, 97–100. Lazoglu, A.H., Glace, B., Gleim, G.W., & Coplan, N.L. (1996). Exercise and heart rate variability. American Heart Journal, 131, 825–827. LeDoux, J.E. (2000). Emotion circuits in the brain. Annual Review Neuroscience, 23, 155–184. Lehrer, P., Sasaki, Y., & Saito, Y. (1999). Zazen and cardiac variability. Psychosomatic Medicine, 61, 812–821. Lubman, D.I., Yücel, M., & Pantelis, C. (2004). Addiction, a condition of compulsive behavior? Neuroimaging and neuropsychological evidence of inhibitory dysregulation. Addiction, 99, 1491–1502. Macht, M., & Müller, J. (2007). Interactive effects of emotional and restrained eating on responses to chocolate and affect. The Journal of Nervous and Mental Disease, 12, 1024–1026. McCraty, R., & Tomasino, D. (2004). Heart rhythm coherence feedback: A new tool for stress reduction, rehabilitation, and performance enhancement. Proceeding of the First Baltic Forum on Neuronal Regulation and Biofeedback, Riga, Latvia. Mintz, L.B., & O’Halloram, M.S. (2000). The eating attitudes test: Validation with DSM-IV eating disorder criteria. Journal of Personality Assessment, 74, 489–503. Moltó, J., Montañés, S., Poy, R., Segarra, P., Pastor, M.C., Tormo, M.P. et al. (1999). Un nuevo método para el estudio experimental de las emociones: The International Affective Picture System (IAPS). Adaptación española. Revista de Psicología General y Aplicada, 52, 55–87. Müller, J., Dettmer, D., & Macht, M. (2008). The attitudes to chocolate questionnaire: Psychometric properties and relationship to dimensions of eating. Appetite, 50, 499–505. Nederkoorn, C., & Jansen, A. (2002). Cue reactivity and regulation of food intake. Eating Behaviors, 3, 61–72. Nederkoorn, C., Smulders, S., & Jansen, A. (2000). Cephalic phase responses, craving and food intake in normal subjects. Appetite, 35, 45–55. Nolan, R., Kamath, M.V., Floras, J.S., Stanley, J., Pang, C., Picton, P. et al. (2005). Heart rate variability of biofeedback as a behavioral neurocardiac intervention to enhance vagal heart rate control. American Heart Journal, 149, 1137. Parker, G., & Crawford, J. (2007). Chocolate craving when deHogrefe Publishing


pressed: A personality marker. British Journal of Psychiatry, 191, 351–352. Parker, G., Parker, I., & Brotchie, H. (2006). Mood state effects of chocolate. Journal of Affective Disorders, 92, 149–159. Pelchat, M.L., Johnson, A., Chan, R., Valdez, J., & Ragland, D.J. (2004). Images of desire: Food craving activation during fMRI. NeuroImage, 23, 1486–1493. Pignotti, M., & Steinberg, M. (2001). Heart rate variability as an outcome measure for thought field therapy in clinical practice. Journal of Clinical Psychology, 57, 1193–1206. Ramírez, I., Sánchez, M.B., Fernández, M.C., Lipp, O.V., & Vila, J. (2005). Differentiation between protective reflexes: Cardiac defence and startle. Psychophysiology, 42, 732. Reyes, G., Godoy, J., & Vila, J. (1993). Respiratory sinus arrhythmia as an index of parasympathetic cardiac control during the cardiac defence response. Biological Psychology, 35, 17–35. Robinson, T.E., & Berridge, K.C. (2003). Addiction. Annual Review of Psychology, 54, 25–53. Rodríguez, S., Fernández, M.C., Cepeda-Benito, A., & Vila, J. (2005). Subjective and physiological reactivity to chocolate images in high and low cravers. Biological Psychology, 70, 9–18. Rodríguez, S., Warren, C.S., Moreno, S., Cepeda-Benito, A., Gleaves, D.H., Fernández, M.C. et al. (2007). Adaptation of the Food Craving Questionnaire-Trait for the assessment of chocolate cravings: Validation across British and Spanish women. Appetite, 49, 245–250. Rogers, P.J., & Smit, H.J. (2000). Food craving and food “addiction”: A critical review of the evidence from a biopsychosocial perspective. Pharmacology, Biochemistry and Behavior, 66, 3–14. Rolls, E.T., & McCabe, C. (2007). Enhanced affective brain representations of chocolate in cravers vs. noncravers. European Journal of Neuroscience, 26, 1067–1076. Ruiz-Padial, E., Sollers, J.J. III., Vila, J., & Thayer, J.F. (2003). The rhythm of the heart in the blink of an eye: Emotion-modulated startle magnitude covaries with heart rate variability. Psychophysiology, 40, 306–313. Russoniello, C.V., Mahar, M.T., DiNallo, J.M., McCammon, M.R., Skalko, T.K., & Rowe, D.A. (2002). Effects of a physical activity program on heart rate variability in obese children. Applied Psychophysiology Biofeedback, 27, 299–320. Sánchez, M.B., Ruiz-Padial, E., Pérez, N., Fernández, M.C., Cobos, P., & Vila, J. (2002). Modulación emocional de los reflejos defensivos mediante visualización de imágenes afectivas. Psicothema, 14, 702–707. Small, D.M., Zatorre, R.J., Dagher, A., Evans, A.C., & Jones-Gotman, J. (2001). Changes in brain activity related to eating chocolate: From pleasure to aversion. Brain, 124, 1720–1733. Small, D.M., Gregory, M.D., Mak, Y.E, Gitelman, D.R, Mesulam, M., & Parrish, T.B. (2003). Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron, 39, 701–711. Small, D.M., Jones-Gotman, J., & Dagher, A. (2003). Feedinginduced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. NeuroImage, 19, 1709–1715. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. (1996). Heart rate variability: Standards of measurement, physiological interpretation, and clinical use. Circulation, 93, 1043–1065. Thayer, J.F., & Lane, R.D. (2000). A model of neurovisceral inHogrefe Publishing

103

tegration in emotion regulation and dysregulation. Journal of Affective Disorders, 61, 201–216. Thayer, J.F., & Siegle, G.J. (2002). Neurovisceral integration in cardiac and emotional regulation. IEEE Engineering in Medicine and Biology, 21, 24–29. Thayer, J.F., Friedman, B.H., Borkovec, T.D., Johnsen, B.H., & Molina, S. (2000). Phasic heart period reactions to cued threat and nonthreat stimuli in generalized anxiety disorder. Psychophysiology, 37, 361–368. Thayer, J.F., Smith, M., Rossy, L.A., Sollers, J.J. III., & Friedman, B.H. (1998). Heart period variability and depressive symptoms: Gender differences. Biological Psychiatry, 44, 304–306. Tiffany, S.T. (1990). A cognitive model of drug urges and drug use behavior: Role of automatic and nonautomatic processes. Psychological Review, 97, 147–168. Vila, J., Fernández, M.C., & Godoy, J. (1992). The cardiac defence response in humans: Effects of the stimulus modality and gender differences. Journal of Psychophysiology, 6, 140–154. Vila, J., Fernández, M.C., Pegalajar J., Vera, M.N, Robles, H., Pérez, N. et al. (2003). A new look at cardiac defense: Attention or emotion? Spanish Journal of Psychology, 6, 60–70. Vila, J., Guerra, P., Muñoz, M.A., Vico, C., Viedma-del Jesús, M., Delgado, L.C. et al. (2007). Cardiac defence: From attention to action. International Journal of Psychophysiology, 66, 169–182. Vila, J., Sánchez, M., Ramírez, I., Fernández, M.C., Cobos, P., Rodríguez, S. et al. (2001). El Sistema Internacional de Imágenes Afectivas (IAPS): Adaptación española. Segunda parte [The International Affective Picture System (IAPS): Spanish adaption. Second part]. Revista de Psicología General y Aplicada, 54, 635–657. Volkow, N.D., Wang, G.J., Maynard, L., Jayne, M., Fowler, J.S., Zhu, W. et al. (2003). Brain dopamine is associated with eating behaviors in humans. International Journal of Eating Disorders, 33, 136–142. Waters, A., Hill, A., & Waller, G. (2001a). Bulimics’ response to food cravings: Is binge-eating a product of hunger or emotional state? Behavior Research and Therapy, 39, 877–886. Waters, A., Hill, A., & Waller, G. (2001b). Internal and external antecedents of binge eating episodes in a group of women with bulimia nervosa. The International Journal of Eating Disorders, 29, 17–22. Wang, G.J., Volkow, N.D., Telang, F., Jayne, M., Ma, J., Rao, M. et al. (2004). Exposure to appetitive food stimuli markedly activates the human brain. Neuroimage, 21, 1790–1797.

Accepted for publication: June 2, 2009

Jaime Vila Departamento de Personalidad, Evaluación y Tratamiento Psicológico Facultad de Psicología Universidad de Granada Campus de la Cartuja s/n E-18071 Granada Spain Tel. +34 958 243753 Fax +34 958 243749 E-mail [email protected] Journal of Psychophysiology 2009; Vol. 23(3):95–103