Affect Regulation and Food Intake in Bulimia Nervosa: Emotional

advertisement
Journal of Abnormal Psychology
2006, Vol. 115, No. 3, 567–579
Copyright 2006 by the American Psychological Association
0021-843X/06/$12.00 DOI: 10.1037/0021-843X.115.3.567
Affect Regulation and Food Intake in Bulimia Nervosa: Emotional
Responding to Food Cues After Deprivation and Subsequent Eating
Birgit I. Mauler
Alfons O. Hamm and Almut I. Weike
Christoph-Dornier-Foundation for Clinical
Psychology Muenster, Germany
University of Greifswald, Germany
Brunna Tuschen-Caffier
University of Bielefeld, Germany
Emotional responding to salient food cues and effects of food deprivation and consumption were
investigated in 32 women with bulimia and 32 control women. One half of each group was food deprived
before viewing unpleasant, neutral, pleasant, and food-related pictures. Then participants could eat from
a buffet before viewing a parallel picture set. Women with bulimia showed a substantial potentiation of
startle responses during viewing of food cues relative to control women. This startle potentiation was
attenuated by food deprivation and augmented by increased food consumption. These data support the
affective regulation model suggesting that food cues prompt negative affective states in women with
bulimia, who are overwhelmed by fasting. The resulting deprivation increases the incentive value of food
cues and may thus trigger binge eating.
Keywords: bulimia nervosa, startle response, deprivation, affect regulation, binge eating
From the perspective of self-regulation (see Mann & Ward,
2004, for a recent discussion), dieting is the attempt of persons
with bulimia to reduce the negative affect elicited by cues that are
associated with food intake and the fear of gaining weight. Such an
idea seems to be nonintuitive, because food cues normally have
reinforcing, appetitive qualities in healthy volunteers. Indeed, external food cues potentiate appetitive reflexes (e.g., salivation;
Konorski, 1967; Wooley & Wooley, 1981) and slightly inhibit
protective reflexes such as the startle response, a cranial to caudal
spreading wave of flexor movements elicited by abruptly occurring sensory events (Bradley, Codispoti, Cuthbert, & Lang, 2001).
Deprivation even seems to increase the appetitive motivational
state that can be triggered by food cues. Food cues are rated as
more pleasant by deprived relative to nondeprived persons (e.g.,
Lavy & van den Hout, 1993) and are rated as being more attractive
than other reinforcers (Bulik & Brinded, 1994; Raynor & Epstein,
2003). In addition, deprivation leads to increased salivation during
confrontation with food cues (Staats & Hammond, 1972) as well as
to increased blood flow in the amygdala and the associated inferotemporal cortical regions (LaBar et al., 2001).
On the other hand, emotional responses of women with bulimia
nervosa to food cues seem to differ from those of control subjects
without bulimia, although data in this area of research are scarce.
In controlled studies, when purging was rendered impossible,
women with bulimia reported negative affect and anxiety after
eating (Buree, Papageorgis, & Hare, 1990; Leitenberg, Gross,
Peterson, & Rosen, 1984). Additionally, they reported fear of
gaining weight, tenseness, or being irritated and depressed (e.g.,
Staiger, Dawe, & McCarthy, 2000), supporting the idea that dieting might be used by the women with bulimia to avoid the negative
affect associated with food exposure and eating. Studies, in which
attempts were made to relate these verbal report data to physiological responses elicited by food cues (e.g., salivation, heart rate,
The most salient aspect of bulimia nervosa is an abnormal eating
pattern. Arguably, the cardinal feature of this disordered eating is
bouts of uncontrolled food intake (binges). During bingeing large
amounts of food are usually ingested while the person experiences
an irresistible food craving and lack of control over his or her
eating behavior. Additionally, there is recurrent inappropriate behavior to prevent weight gain including purging behavior directly
after bingeing (e.g., vomiting or use of laxatives), excessive exercise, and restrained eating or fasting between periods of binge
eating. There seems to be general consensus in the literature that
such dieting is a key factor in the development and maintenance of
bulimic psychopathology for the majority of the patients (Brewerton, Dansky, Kilpatrick, & O’Neal, 2000; Bulik, Sullivan,
Carter, & Joyce, 1997; Polivy & Herman, 2002; Stice, 2002). Food
restriction can trigger binge eating (Davis, Freeman, & Garner,
1988; Rosen, Tacy, & Howell, 1990) and maintains the bulimic
eating pattern (Fairburn, Stice, et al., 2003; Leon, Fulkerson, Perry,
& Early-Zald, 1995; Patton, Johnson-Sabine, Wood, Mann, &
Wakeling, 1990).
Birgit I. Mauler, Christoph-Dornier-Foundation for Clinical Psychology, Muenster, Germany; Alfons O. Hamm and Almut I. Weike, Department of Psychology, University of Greifswald, Germany; Brunna TuschenCaffier, Department of Clinical Psychology, University of Bielefeld,
Germany.
This research was supported by the Christoph-Dornier-Foundation for
Clinical Psychology and by grants from the Deutsche Forschungsgemeinschaft (German Research Foundation) to Alfons O. Hamm (Ha 1593/6-2
and Ha 1593/10-2). We thank Dr. Carmen Hamm for taking the blood
samples of all participants.
Correspondence concerning this article should be addressed to Alfons
O. Hamm, Department of Psychology, University of Greifswald, FranzMehring-Strasse 47, 17487, Greifswald, Germany. E-mail: hamm@unigreifswald.de
567
568
MAULER, HAMM, WEIKE, AND TUSCHEN-CAFFIER
and electrodermal responses), though, showed discouraging results. In most studies no reliable relationships between measures of
autonomic arousal and verbal report were obtained (Buree et al.,
1990; Carter & Bulik, 1996; Leitenberg et al., 1984; Williamson,
Kelley, Davis, Ruggiero, & Veitia, 1985). This does not come as
a surprise, because discordance and desynchrony between different
response systems are often observed during emotional responding
(Cacioppo, Klein, Berntson, & Hartfield, 1993; Lang, 1985). One
reason for this modest correlation is that different indices of
emotions, of course, serve different functions. Verbal report is
used to communicate affective experiences to others and is therefore biased by intentions of self-presentation or by specific situational demands. Autonomic measures (such as heart rate and skin
conductance) are primarily linked to the intensity of affective
stimulation (see Lang, Greenwald, Bradley, & Hamm, 1993), and
these measures of autonomic arousal alone might not be the best
choice to investigate the emotional impact of food cues for individuals with bulimia.
In contrast, the modulation of the acoustic startle reflex seems to
specifically index the motivational potency of a cue. The magnitude of the startle eyeblink response elicited by a brief acoustic
probe stimulus is augmented during viewing of unpleasant and
specifically threatening pictures and is reduced while viewing
pleasant images (Vrana, Spence, & Lang, 1988; see Bradley, 2000,
for review). This effect has been replicated several times (e.g.,
Cook, Davis, Hawk, Spence, & Gautier, 1992; Hamm, Cuthbert,
Globisch, & Vaitl, 1997; Patrick, Bradley, & Lang, 1993). The
phenomenon has been explained by the emotional priming model
(Lang, Bradley, & Cuthbert, 1998), stating that independently
evoked defensive and protective reflexes are augmented if the
organism is in a defensive motivational state and reduced if the
organism is in an appetitive state. Emotional priming of the startle
reflex operates on a very fundamental level outside of subjects’
awareness and is mediated by the amygdala, a subcortical limbic
structure located in the anterior medial temporal lobe (see Davis,
2000).
Drobes et al. (2001) used the startle probe methodology for the
first time to investigate the motivational impact of salient food
cues in participants who report habitually deviant eating patterns.
As expected, food cues prompted comparable startle response
magnitudes relative to other pleasant, food unrelated visual cues in
control participants. By contrast, those participants who have
experienced eating binges in the past showed a relative potentiation of their startle response magnitudes during viewing of food
cues (compared with other pleasant nonfood cues), suggesting that
these usually appetitive cues did not activate positive affect in this
group of subjects. However, the same effect was found in the
deprived control group. This finding is surprising, because food
cues normally should have a positive incentive value in deprived
participants. Accordingly, Hawk, Baschnagl, Ashare, and Epstein
(2004) found a stronger reduction of the startle reflex magnitude in
deprived participants during viewing of their favorite food cues. In
contrast to the study of Drobes et al. (2001), participants in the
study of Hawk et al. (2004) were given access to their favorite food
after the experiment. The experimental context of the study of
Drobes et al. (2001) did not allow for immediate food consumption. Therefore, these authors interpreted the relative startle potentiation as indexing a negative affective state of frustrative nonreward; that is, hungry participants viewed food pictures without
getting the opportunity to eat. Deviant eating patterns coupled with
deprivation status, however, were not a focus of that study.
In the current study, therefore, we focused on affective responses to food cues in women with bulimia nervosa, comparing
their physiological, behavioral, and verbal response patterns with
those of control women without bulimia. Additionally, standard
affective materials (unpleasant, neutral, and pleasant pictures)
were presented to investigate the specificity of the emotional
responding to food cues in these women with an eating disorder.
Moreover, we investigated whether prior food deprivation would
influence the motivational relevance of food cues and whether this
effect would be modulated by psychopathology. Thus, half of the
women with bulimia and half of the control women were food
deprived for 24 hours before the experiment. Compliance with the
deprivation condition was controlled by the assessment of
␤-hydroxybutyric acid taken from the serum. A second aim of the
study was to investigate the modulation of affective responding to
food cues by prior food consumption. To this end, all participants
were allowed to eat as much as they wanted from a breakfast buffet
during a recreational break between the first and second psychophysiological assessment.
It was expected that food cues would serve as appetitive stimuli
in the control subjects and would consequently elicit an appetitive
motivational response pattern, including startle response inhibition. Moreover, if the hypothesis of frustrative nonreward is correct, participants should exhibit increased startle magnitudes during viewing of food cues after 24 hours of food deprivation. If food
cues elicit a negative affect in those with bulimia, as predicted by
the affect regulation hypotheses, these stimuli should elicit a
relative potentiation of the startle reflex in these participants. On
the other hand, food cues might also elicit a stronger appetitive
response disposition in these participants and might therefore be
more potent in eliciting binge eating. If this were the case, those
with bulimia should show a stronger reduction in startle magnitudes evoked during viewing of food pictures relative to the
control women. Deprivation might increase the incentive value of
the food cues and should then increase appetitive motivation and
further reduce startle magnitudes during viewing of food cues in
the women with bulimia.
Method
Participants
One hundred fifty-six individuals responded to two different advertisements on the university campus and in local newspapers asking for subjects
with and without disturbed eating habits. After a short telephone screening
of these individuals, asking for symptoms of bulimia, including restrained
eating, body weight, height, pregnancy, thyroid malfunctions, and age, 87
of them were invited for a further diagnostic session. After this clinical
interview, 66 women agreed to participate in the experiment. Control
participants had no history of eating disorders and were not on a weight
loss diet at the moment. Bulimia nervosa was diagnosed in 34 participants
on the basis of the Diagnostic and Statistical Manual of Mental Disorders
(4th ed.) criteria (American Psychiatric Association, 1994) using a standardized clinical interview (Fairburn & Cooper, 1993). The binge frequency of the women with bulimia was 8.06 (⫾ 4.2) per week. Thirty-three
of the 34 women with bulimia purged by vomiting. Their mean frequency
of self-induced vomiting was 7.34 (⫾ 4.1) times per week. On average, the
participants with bulimia reported durations of bulimia nervosa of 6.4 (⫾
AFFECT REGULATION AND BULIMIA NERVOSA
3.7) years. Ten of them showed comorbidity with anxiety or affective
disorder.1
All participants completed the German versions of the Restraint Scale
(Polivy, Herman, & Howard, 1988) and the Three-Factor Eating Questionnaire (Stunkard & Messick, 1985). Because the general fear level affects
the overall startle response amplitudes (Cook et al., 1992), all participants
completed the German version of the State Anxiety Questionnaire (Spielberger, Gorsuch, & Lushene, 1970). There were no significant differences
in the overall state anxiety level between women with bulimia and control
women. Group means of all questionnaire scores are presented in Table 1.
Furthermore, body mass index and the age range of each group are also
shown in Table 1.
Because individuals in a normal weight range were sought (most individuals with bulimia are of normal weight), all subjects were selected on
the basis of an average body mass index (ranging from 19 to 24 kg/m2).
Additionally, they were not taking any medication and did not report
pregnancy or thyroid malfunctions. Participants included in the control
group (N ⫽ 32) did not report any history of eating disorders and were not
currently dieting or identified as restraint eaters (ⱕ9 in the Restraint Scale
and ⱕ6 in Scale 1 of the Three-Factor Eating Questionnaire).
Participants in each diagnostic group were randomly assigned to the
deprivation condition, whereas the remaining participants were instructed
to proceed with their normal diet. Participants obtained a small monetary
reward for their participation. This investigation was approved by the
ethics committee of the Christoph-Dornier-Foundation for Clinical
Psychology.
Procedure and Stimulus Materials
Food deprivation. In the deprivation condition subjects were asked to
refrain from eating for 24 hours beginning at 10:00 a.m. on the day before
the study. On the following day, blood samples were taken at 9:00 a.m.
from all participants. ␤-hydroxybutyric acid was analyzed from the serum
to assess whether participants followed the instruction.2 As expected,
concentrations of this metabolite increased from 84.4 and 86.6 ␮mol/L to
605.8 and 522.7 ␮mol/L after fasting for deprived women with bulimia and
control women, respectively. Although participants were informed that the
blood test would show whether or not they had eaten during the deprivation
interval, two participants with bulimia had to be excluded after the blood
test, because the concentration of the metabolite clearly revealed that they
had not followed the food deprivation instruction (values were 82.5 and
90.3 ␮mol/L). All control subjects followed the food deprivation instruction. Thus, 16 subjects in each of the 4 groups participated in the experimental sessions.
Table 1
Scores in the Three-Factor Eating Questionnaire (TEFQ), the
Restraint Scale (RS), the State Anxiety Questionnaire (STAI),
and the Mean Body Mass Index (BMI) of the Deprived and
Nondeprived Participants With Bulimia and Control
Participants
Bulimia
Control
Deprived Nondeprived Deprived Nondeprived
(n ⫽ 16)
(n ⫽ 16)
(n ⫽ 16)
(n ⫽ 16)
TFEQ (Scale I)
RS
STAI
BMI (kg/m2)
Age (range) (years)
Note.
12.8 (1.2)
22.8 (1.2)
47.0 (0.6)
21.9 (0.4)
25–35
13.5 (1.2)
21.6 (1.0)
47.5 (0.6)
20.6 (0.4)
21–33
2.4 (0.4)
6.3 (0.6)
47.6 (0.4)
20.9 (0.4)
20–28
Scores are presented as means and (standard errors).
2.3 (0.4)
6.4 (0.5)
45.9 (0.6)
21.3 (0.3)
20–30
569
First experimental session. The first experimental session in the laboratory began at 10:00 a.m., that is, 1 hour after the blood sample was
taken. Participants in the nondeprived groups were instructed to eat breakfast (about 450 kcal) before coming to the laboratory. Those who had not
complied with this instruction (n ⫽ 2) were asked to consume a standard
breakfast (450 kcal) before starting the experiment. Physiological sensors
were attached while the participant reclined in a comfortable chair in a
sound-attenuated and dimly lit room. At the beginning of the session, four
acoustic startle eliciting stimuli [a 50-ms burst of broadband 105 dB(A)
white noise with instantaneous rise/fall time; S81-02, Coulbourn] were
presented binaurally through headphones (MDR-CD 170; Sony). Two
probes were administered while participants viewed pictures of landscapes,
and two probes were presented without visual foreground. Afterward the
signals were checked, and all participants were instructed that a series of
pictures would be presented and that each picture should be viewed for the
entire time it appeared on the screen. In addition, they were told that
occasional noises heard over headphones could be ignored. Then each
participant viewed one of two sets of 32 color pictures,3 8 pictures
containing explicit food cues and 8 pictures each selected from the three
standard valence categories (i.e., pleasant, neutral, and unpleasant) based
on normative ratings (Hamm & Vaitl, 1993). Forty-nine of the 64 pictures
were selected from the International Affective Picture System4 (Center for
the Study of Emotion and Attention, 1995). Fifteen of the 16 food pictures
were created for that study and were rated for valence, arousal, and
dominance in a pilot study. Picture contents were presented in perceptually
random order, counterbalanced across participants. Each picture was presented for 6 s. On 6 of the 8 picture presentations per picture category, the
acoustic startle probe was administered either 4.0, 4.5, or 5.0 s after picture
1
Because affective startle reflex modulation is impaired in patients with
affective disorders (Allen, Trinder, & Brennan, 1999), Mann–Whitney U
tests were performed to test whether emotional responses of the 6 women
with bulimia with comorbid affective disorder differed from those of the
other women with bulimia. Emotional responses to the affective stimuli did
not differ in this comparison; Mann–Whitney U (N ⫽ 32) ⫽ 92.00, ns,
82.00, ns, for Sessions 1 and 2, respectively. One has to keep in mind that
Allen et al. (1999) investigated medicated inpatients with severe major
depression, and deviant affective startle modulation was only obtained for
patients with a Beck Depression Inventory score ⬎30.
2
The normal range of ␤-hydroxybutyric acid, a metabolite of the fatty
acids that can pass the blood– brain barrier, varies between 30 and 120
␮mol/L. During fasting the level of this metabolite increases substantially
up to 500 –700 ␮mol/L but rapidly returns to the baseline level after food
intake. Thus, ␤-hydroxybutyric acid is a good biological index for assessing compliance with a deprivation instruction (Webber & Macdonald,
1994). The secretion of ␤-hydroxybutyric acid also follows a definite
circadian rhythm. Therefore, the blood samples were always taken at the
same time in the morning. Moreover, to control for interindividual differences a second baseline measurement of ␤-hydroxybutyric acid level was
taken either 1 week before or after the experiment. No deprivation instructions were given this time, and blood samples were again taken at 9:00 a.m.
3
Stimulus materials were arranged in two sets (A and B) of 32 slides
each, which were similar for picture contents and normative valence and
arousal ratings. Half of the subjects viewed Set A in the first and Set B in
the second experimental session and vice versa.
4
Numbers of the International Affective Picture System pictures are as
follows: Set A neutral, 2200, 5500, 7050, 7010, 7100, 7550, 7820, 7130,
pleasant, 1710, 2040, 2080, 4430, 4608, 4680, 8030, 8200, unpleasant,
1120, 3000, 3100, 3120, 6210, 6230, 9250, 6312, food, 7330; Set B neutral,
2210, 5510, 7020, 7090, 7170, 9070, 7830, 7500, pleasant, 1750, 2050,
2250, 4490, 4660, 4690, 8490, 8080, unpleasant, 1300, 3010, 3130, 3150,
6190, 6200, 9050, 6313.
570
MAULER, HAMM, WEIKE, AND TUSCHEN-CAFFIER
onset. In addition, 8 startle probes were presented during the intertrial
intervals, which varied between 8 and 21 s.
After each picture was presented once, sensors and headphones were
removed. The participant was instructed that she could now view the same
pictures as long as desired using a button press to terminate picture
presentation. Viewing times were recorded in milliseconds as a behavioral
measure of interest. After picture offset, each participant rated her subjective experience of valence and arousal, using the computerized version of
the Self-Assessment–Manikin (Hodes, Cook, & Lang, 1985). Participants
then rated their interest in each picture and, only after watching food
pictures, their general desire to eat using a 20-point computerized line
rating.
Food consumption. After the picture rating task, participants were
taken to another room, where they were allowed to eat as much as desired
from a breakfast buffet consisting of various rolls, cereals, and so forth.
Participants were alone in the room but could be observed through a
one-way mirror. A radio and newspapers were available to create a pleasant
atmosphere. A total amount of 20 min of food access was given. Any food
remaining after this period of time was removed, weighted, and counted.
The amount of calories consumed was calculated using a computer program (PRODI, Version 4).
Second experimental session. After food consumption, participants
were led back to the laboratory, physiological sensors were attached again,
and the same procedure was applied as in the first experimental session.
Now each participant viewed the other of the two sets of 32 color pictures.
Acoustic startle probes were administered in the same order during and
between picture viewing as in the first session. After the pictures were
viewed once and physiological responses were recorded, the same pictures
were presented again and free viewing times and subjective ratings were
obtained.
Apparatus
The eyeblink component of the startle response was measured by recording the electromyographic (EMG) activity over the left orbicularis
oculi muscle beneath the eye using Ag/AgCl miniature surface electrodes
(Sensormedics, Yorbahinda, CA) filled with electrolyte (Marquette,
Hellige, Freiburg, Germany). The raw EMG signal was amplified and
filtered through a 30 –1,000 Hz bandpass using a Coulbourn S75-01
bioamplifier. The signal was then rectified and integrated on line by a
Coulbourn S76-01 contour-following integrator with a time constant of 10
ms. Digital sampling with a rate of 1000 Hz started 100 ms before and
lasted until 400 ms after the onset of the acoustic startle stimulus.
Corrugator EMG activity was recorded above the left eye with Ag/AgCl
miniature surface electrodes (Sensormedics) filled with electrolyte, using
the placement recommended by Fridlund and Cacioppo (1986). Amplification and filtering of the raw signal were identical to those described for
the orbicularis oculi. The signal was then rectified and integrated on line
using a Coulbourn S76-01 contour-following integrator with a time constant set at 500 ms. Digital sampling at 10 Hz began 3 s before picture onset
and ended 3 s after picture offset.
Skin conductance was recorded with Ag/AgCl standard electrodes (8
mm diameter; Marquette Hellige) filled with a 0.05 M sodium chloride
electrolyte medium. Electrodes were placed adjacently on the hypothenar
eminence of the palmar surface of the participant’s nondominant hand. A
Coulbourn S71-22 skin conductance coupler provided a constant voltage of
0.5 V across electrodes and processed the signal with a resolution of 0.01
␮S. Digital sampling at 10 Hz started 3 s before picture onset and
continued until 3 s after picture offset.
A lead II electrocardiogram was obtained using Ag/AgCl standard
electrodes (Marquette Hellige) filled with Hellige electrolyte. The signal
was amplified and filtered with a Coulbourn S75-01 bioamplifier. The
analogue signal was digitized with a sampling rate of 1000 Hz starting 3 s
before picture onset and continuing until 3 s after picture offset. A peak
trigger served for online registration of the R-wave within the analogue
electrocardiogram signal. Interbeat intervals were converted to heart rate in
beats per minute in half-second bins, following the recommendations of
Graham (1978).
Visual stimuli were presented using a Kodak Ektagraph slide projector
situated in the room adjacent to the experimental chamber. The pictures
were presented on a white wall 1.5 m in front of the participant. The size
of the visible picture was 120 ⫻ 80 cm.
After completion of the study, all participants were debriefed, and those
with bulimia were offered treatment in the outpatient facility of the
Christoph-Dornier-Foundation.
Data Reduction and Analysis
The reflex eyeblink data were reduced and scored off line using a
computer program (Globisch, Hamm, Schneider, & Vaitl, 1993) that identified latency of blink onset (in milliseconds) and peak amplitude (in
microvolts). Responses starting 20 –100 ms after startle probe onset and
reaching peak amplitude within 150 ms after probe onset were identified as
startle eyeblinks. Trials with clear movement artifacts or excessive baseline
activity were rejected (1.81%), and trials in which no response could be
detected were scored as zero magnitude. The results of various distribution
analyses (assessment of skewness and kurtosis and the Kolmogorov–
Smirnoff test of normal distribution) suggested that startle response magnitudes should be standardized to correct for individual differences. There
were no significant differences between the four groups in the overall raw
startle magnitude, F(1, 60) ⬍ 1. Therefore, responses from each participant
were transformed to z scores and converted to T scores (i.e., 50 ⫹ [z ⫻
10]). All picture and intertrial interval startle responses were used as the
reference distribution for these computations.
Skin conductance responses to the pictures were scored according to the
recommendations of Prokasy and Kumpfer (1973). The first interval response was defined as the largest increase in conductance occurring between 0.9 and 4 s after stimulus onset. Because the earliest probe was
administered 4 s after picture onset, the first interval response was not
confounded by the acoustic probe stimulus. Logarithms of these values
were computed before statistical analyses to normalize the distribution
(Venables & Christie, 1980). Again, to reduce interindividual variability
and to facilitate comparisons of different picture contents, the log values
were range corrected by dividing each individual score by the participant’s
maximum response (Lykken & Venables, 1971). One nondeprived control
participant was excluded from further analyses because of electrodermal
nonresponding (i.e., maximum response ⫽ 0).
Digital values of corrugator EMG activity were converted to microvolts,
and corrugator responses were scored by subtracting the 1-s prestimulus
level from the average change in the 6-s picture viewing interval. Corrugator responding of one nondeprived control participant was lost because
of equipment malfunction. Baseline heart rate (1 s before picture onset)
was subtracted from average heart rate for every half-second during the 6-s
picture viewing period, and these phasic heart rate changes were averaged
for statistical analyses. Cardiac responses to food cues showed an overall
deceleration. Accordingly, component scores did not reveal any additional
information and therefore are not reported. Five control participants (three
deprived and two nondeprived) had to be excluded from heart rate analyses
because of excessive artifact recordings during one of the experimental
sessions.
Following prior research with this paradigm, a first step in the analysis
was to replicate responses to the three standard affective categories and
verify that the overall response pattern did not vary across the different
groups. A mixed model analysis of variance (ANOVA) for each measure
involved Pathology (participants with bulimia vs. control participants) and
Deprivation (deprived vs. nondeprived participants) as between-subjects
variables and Category (unpleasant vs. neutral vs. pleasant) as a withinsubjects variable. After these preliminary tests, further data analyses fo-
AFFECT REGULATION AND BULIMIA NERVOSA
cused on the food pictures. These analyses used a mixed design (ANOVA)
again involving Pathology and Deprivation as between-subjects variables
and Category as a within-subjects variable. Because food cues are normally
rated as emotionally pleasant stimuli (Bradley et al., 2001), the main
contrast food versus (standard) pleasant pictures was tested in the analyses.
Unless otherwise noted, all statistical tests used the .05 level of statistical
significance. Greenhouse–Geisser adjustments of degrees of freedom were
used where appropriate. Partial eta squared values are reported as a
measure of effect size.
Results
First Experimental Session
Standard Affective Categories
As expected, differences among the standard pleasant, neutral,
and unpleasant pictures were observed for physiological, behavioral, and self-report measures (see Table 2).5 Most important, the
modulation of the physiological, behavioral, and self-report measures as a function of affective valence of these nonfood cues did
not vary for the four groups. Neither the overall Category ⫻
Pathology (participants with bulimia vs. control participants) nor
the Category ⫻ Deprivation (deprived vs. nondeprived participants) interaction was significant for any of these different measures. Thus, pictures that were unrelated to food prompted the
same affective responses in all four groups.
Food Cues
Startle response magnitudes. As predicted, the overall analysis of food and pleasant pictures resulted in a significant Category ⫻ Pathology interaction, F(1, 60) ⫽ 102.4, p ⬍ .01, ␩2 ⫽ .63.
The effect was also found for food cues compared with neutral
pictures, Category ⫻ Pathology, F(1, 60) ⫽ 70.1, p ⬍ .01, ␩2 ⫽
.54. Participants with bulimia showed a significant potentiation of
their startle responses to food cues relative to other pleasant
pictures, F(1, 30) ⫽ 241.4, p ⬍ .01, ␩2 ⫽ .89, and neutral pictures,
F(1, 30) ⫽ 83.4, p ⬍ .01, ␩2 ⫽ .74. By contrast, blink magnitudes
of the control participants were significantly reduced when elicited
during viewing of food cues relative to neutral pictures, F(1, 30) ⫽
11.4, p ⬍ .01, ␩2 ⫽ .28, whereas no differences were observed for
food cues compared with the standard pleasant pictures, F(1, 30)
⬍ 1. Moreover, startle responses elicited during viewing of food
cues were significantly larger for participants with bulimia than for
control participants, F(1, 60) ⫽ 65.9, p ⬍ .01, ␩2 ⫽ .52, but blink
magnitudes did not differ between groups for pleasant or neutral
pictures, F(1, 60) ⬍ 1. Mean blink response magnitudes elicited
during viewing of food cues and unpleasant, neutral, and pleasant
pictures for deprived and nondeprived participants with bulimia
and control participants are depicted in Figure 1.
The effect of food deprivation on the startle response magnitudes during viewing of food cues varied significantly between
participants with bulimia and control participants, Deprivation ⫻
Pathology, F(1, 60) ⫽ 32.3, p ⬍ .01, ␩2 ⫽ .35. Although fooddeprived control participants exhibited elevated startle response
magnitudes during viewing of food cues relative to nondeprived
control participants, F(1, 30) ⫽ 5.4, p ⬍ .05, ␩2 ⫽ .15, participants
with bulimia showed the reverse response pattern. In the bulimia
group, food-deprived participants exhibited significantly smaller
571
startle responses during viewing of food cues than nondeprived
participants, F(1, 30) ⫽ 29.8, p ⬍ .01, ␩2 ⫽ .50. Food-deprived
control participants showed a potentiation of their startle reflex
during viewing of food cues relative to other pleasant materials
whereas such potentiation did not occur for nondeprived control
participants, Category ⫻ Deprivation, F(1, 30) ⫽ 7.6, p ⬍ .01,
␩2 ⫽ .20. By contrast, this startle potentiation was smaller for
food-deprived participants with bulimia relative to those who were
not food-deprived before the experiment, Category ⫻ Deprivation,
F(1, 30) ⫽ 55.2, p ⬍ .01, ␩2 ⫽ .65. This differential responding
to food cues of participants with bulimia and control participants
as a function of deprivation is also supported by a significant
Category ⫻ Deprivation ⫻ Pathology interaction, F(1, 60) ⫽ 49.2;
p ⬍ .01, ␩2 ⫽ .45.
Corrugator facial muscle responses. The overall comparison
of corrugator responses to food cues and pleasant pictures revealed
a significant Category ⫻ Pathology interaction, F(1, 59) ⫽ 9.3,
p ⬍ .01, ␩2 ⫽ .14. Again, this effect also occurred if corrugator
responses to food cues were compared with those elicited by
neutral picture contents, Category ⫻ Pathology, F(1, 59) ⫽ 9.4,
p ⬍ .01, ␩2 ⫽ .14. Viewing of food cues resulted in a significant
increase of corrugator muscle activity relative to viewing of pleasant pictures in participants with bulimia, F(1, 30) ⫽ 19.1, p ⬍ .01,
␩2 ⫽ .39, whereas corrugator responses to food cues overall were
comparable with those evoked by other pleasant materials in
control participants, F(1, 29) ⬍ 1. Again, participants with bulimia
showed overall significantly larger corrugator responses during
viewing of food pictures relative to control participants, F(1, 59) ⫽
11.7, p ⬍ .01, ␩2 ⫽ .17, whereas no group differences were
observed for the other stimuli, F(1, 59) ⬍ 1. Deprivation significantly reduced the corrugator responses to food cues, F(1, 59) ⫽
10.6, p ⬍ .01, ␩2 ⫽ .15, for both groups, Deprivation ⫻ Pathology
F(1, 59) ⬍ 1. Mean corrugator responses elicited during viewing
of food cues and unpleasant, neutral, and pleasant pictures for
deprived and nondeprived participants with bulimia and control
participants are shown in Table 2.
Skin conductance, heart rate, and viewing times. Mean skin
conductance and heart rate responses, viewing times, and interest
ratings of food cues, unpleasant, neutral, and pleasant pictures for
food-deprived and nondeprived participants with bulimia and control participants are also shown in Table 2. Skin conductance and
heart rate responses to food cues as well as viewing times of these
stimuli did not vary for participants with bulimia and control
participants (all statistical tests of the Pathology factor were not
significant). By contrast, food deprivation had a significant effect
on these measures. Viewing times of food cues were significantly
longer for deprived relative to nondeprived participants, F(1,
60) ⫽ 9.8, p ⬍ .01, ␩2 ⫽ .14, and this effect did not vary for
Pathology, F(1, 60) ⬍ 1. Moreover, for deprived participants
viewing times of food cues were significantly longer than for
neutral pictures whereas nondeprived participants viewed food
5
Replicating previous findings, blink magnitudes, corrugator EMG, and
pleasure ratings were significantly modulated by the valence of the nonfood cues. By contrast, skin conductance responses, viewing times, interest, and arousal ratings varied with the arousal level of the nonfood
pictures, replicating previous research.
MAULER, HAMM, WEIKE, AND TUSCHEN-CAFFIER
572
Table 2
Physiological, Behavioral, and Subjective Responding to the Standard Affective and Food Pictures During the First and Second
Picture Viewing Session in Deprived and Nondeprived Participants With Bulimia and Control Participants
Session 1
Unpleasant
Neutral
Session 2
Pleasant
Food
Unpleasant
Neutral
Pleasant
Food
Startle blink (T scores)
Bulimic
Deprived
Nondeprived
Control
Deprived
Nondeprived
58.7 (1.6)
62.9 (1.5)
48.4 (0.8)
48.7 (0.9)
46.5 (0.8)
46.7 (1.0)
50.8 (0.6)
58.9 (1.3)
53.3 (1.1)
49.2 (1.2)
45.2 (0.5)
45.6 (1.0)
43.2 (0.5)
44.4 (0.9)
51.2 (0.9)
46.4 (1.6)
60.2 (1.2)
59.2 (1.4)
48.4 (0.8)
51.3 (1.0)
46.6 (0.4)
47.0 (1.0)
48.4 (0.9)
45.6 (0.8)
58.0 (1.3)
56.4 (1.8)
47.4 (0.8)
47.1 (0.8)
43.9 (0.6)
45.5 (0.7)
45.8 (1.0)
45.2 (1.0)
Corrugator (⌬ ␮V)
Bulimic
Deprived
Nondeprived
Control
Deprived
Nondeprived
.50 (.21)
.71 (.17)
.21 (.09)
.27 (.11)
.05 (.06)
⫺.09 (.07)
.19 (.11)
.45 (.09)
.79 (.21)
.53 (.22)
.30 (.15)
.40 (.11)
.14 (.12)
.10 (.13)
.45 (.14)
.21 (.08)
.63 (.31)
.80 (.31)
.28 (.16)
.16 (.12)
.01 (.15)
⫺.04 (.07)
⫺.27 (.13)
.17 (.09)
.60 (.23)
1.11 (.37)
.34 (.11)
.12 (.11)
.11 (.09)
⫺.01 (.15)
.22 (.20)
.36 (.17)
Skin conductance (log ␮S)
Bulimic
Deprived
Nondeprived
Control
Deprived
Nondeprived
.21 (.05)
.10 (.03)
.09 (.03)
.01 (.01)
.14 (.04)
.06 (.03)
.10 (.03)
.01 (.01)
.04 (.03)
.03 (.02)
.02 (.02)
.01 (.01)
.02 (.02)
.02 (.02)
.02 (.02)
.00 (.00)
.18 (.07)
.24 (.06)
.09 (.05)
.09 (.03)
.15 (.05)
.19 (.05)
.08 (.04)
.06 (.03)
.05 (.05)
.06 (.02)
.04 (.04)
.03 (.02)
.04 (.04)
.07 (.03)
.03 (.03)
.01 (.01)
Heart rate (⌬ beats/min)
Bulimic
Deprived
Nondeprived
Control
Deprived
Nondeprived
⫺0.91 (.49)
⫺0.17 (.60)
⫺0.87 (.29)
⫺0.64 (.33)
⫺0.21 (.55)
⫺0.65 (.50)
⫺0.03 (.50)
⫺0.63 (.54)
⫺0.92 (.42)
⫺1.18 (.57)
⫺1.04 (.27)
⫺0.38 (.35)
⫺0.63 (.48)
⫺0.74 (.41)
⫺0.19 (.44)
⫺0.39 (.31)
⫺1.57 (.60)
⫺2.51 (.85)
⫺1.29 (.58)
⫺2.13 (.82)
⫺1.02 (.52)
⫺1.64 (.69)
⫺0.11 (.44)
⫺2.15 (.50)
⫺1.63 (.61)
⫺1.06 (.85)
⫺1.51 (.83)
⫺1.25 (.47)
⫺1.68 (.53)
⫺1.00 (.39)
⫺1.60 (.48)
⫺0.70 (.59)
Viewing time (s)
Bulimic
Deprived
Nondeprived
Control
Deprived
Nondeprived
5.9 (1.0)
5.6 (0.5)
6.0 (1.1)
5.9 (0.6)
9.9 (1.7)
6.9 (0.5)
8.1 (1.4)
5.1 (0.4)
5.1 (1.0)
4.7 (0.7)
5.1 (0.9)
4.6 (0.6)
7.5 (1.1)
6.4 (0.7)
5.9 (1.0)
4.9 (0.7)
6.3 (1.0)
6.1 (0.6)
6.5 (1.1)
5.8 (0.6)
9.3 (1.4)
9.2 (0.8)
7.9 (1.3)
4.5 (0.4)
5.0 (0.7)
4.6 (0.6)
5.1 (0.8)
4.5 (0.5)
7.1 (1.1)
6.9 (0.8)
5.7 (0.9)
5.0 (0.5)
Pleasure rating (0–20)
Bulimic
Deprived
Nondeprived
Control
Deprived
Nondeprived
4.2 (0.2)
4.0 (0.2)
11.9 (0.7)
11.8 (0.5)
17.2 (0.3)
17.2 (0.3)
17.3 (0.3)
13.0 (0.3)
4.6 (0.3)
4.7 (0.3)
12.4 (0.7)
10.3 (0.7)
16.3 (0.3)
16.0 (0.3)
13.3 (0.4)
12.5 (0.4)
3.9 (0.2)
4.0 (0.2)
11.5 (0.3)
11.8 (0.4)
17.9 (0.2)
17.5 (0.3)
16.5 (0.2)
13.7 (0.3)
4.8 (0.3)
4.3 (0.3)
12.4 (0.7)
10.9 (0.7)
16.0 (0.4)
15.9 (0.2)
13.8 (0.5)
12.6 (0.2)
Arousal rating (0–20)
Bulimic
Deprived
Nondeprived
Control
Deprived
Nondeprived
16.3 (0.4)
16.7 (0.3)
6.9 (0.3)
6.4 (0.3)
11.7 (0.2)
10.9 (0.3)
11.0 (0.3)
11.8 (0.2)
14.4 (0.5)
14.1 (0.5)
7.4 (0.3)
7.6 (0.3)
10.7 (0.3)
10.8 (0.3)
9.3 (0.8)
8.0 (0.8)
17.2 (0.2)
16.8 (0.3)
6.6 (0.3)
7.1 (0.4)
12.6 (0.4)
12.1 (0.2)
13.5 (0.4)
4.9 (0.4)
14.8 (0.3)
14.7 (0.5)
7.3 (0.2)
7.2 (0.4)
10.8 (0.2)
10.7 (0.3)
4.2 (0.4)
4.1 (0.3)
Interest rating (0–20)
Bulimic
Deprived
Nondeprived
Control
Deprived
Nondeprived
Note.
14.2 (.3)
14.1 (.2)
7.7 (0.4)
7.8 (0.5)
14.5 (0.3)
14.3 (0.2)
15.5 (0.3)
12.7 (0.2)
13.3 (0.6)
13.2 (0.4)
9.3 (0.5)
8.8 (0.3)
13.4 (0.4)
13.1 (0.4)
11.6 (0.5)
11.6 (0.4)
14.3 (.3)
14.2 (.2)
8.6 (0.3)
8.1 (0.3)
15.4 (0.2)
15.0 (0.3)
15.3 (0.3)
7.5 (0.3)
13.2 (0.3)
13.4 (0.4)
9.1 (0.3)
9.0 (0.4)
13.4 (0.3)
12.8 (0.3)
8.4 (0.3)
7.8 (0.3)
Data are presented as means and (standard errors).
AFFECT REGULATION AND BULIMIA NERVOSA
573
Figure 1. Mean blink response magnitudes (standardized scores; ⫾ SE) for startles presented during viewing
of unpleasant, neutral, pleasant, and food cues for deprived and nondeprived participants with bulimia (left) and
control participants (right) during the first session of picture viewing.
cues as long as neutral materials, Category ⫻ Deprivation, F(1,
60) ⫽ 53.1, p ⬍ .01, ␩2 ⫽ .47. Again, this effect did not vary
with psychopathology. Deprivation also significantly affected
the heart rate responses elicited by food cues. Replicating
previous findings, deprived participants showed significantly
less heart rate deceleration to food cues relative to nondeprived
participants, F(1, 55) ⫽ 6.8, p ⬍ .05, ␩2 ⫽ .11. Electrodermal
orienting responses to food cues were also larger for fooddeprived relative to nondeprived participants (see Figure 2),
although this difference fell short of statistical significance,
F(1, 59) ⫽ 3.2, p ⫽ .08, ␩2 ⫽ .05. But again, these response
patterns did not vary between participants with bulimia and
control participants. Mean skin conductance, heart rate responses, viewing times, interest ratings, and ratings of the
desire to eat while processing food cues for deprived and
nondeprived participants are depicted in Figure 2.
Interest ratings, desire to eat, and affective judgments. In
agreement with the autonomic measures and viewing times, deprived participants also reported a significantly larger desire to eat
during viewing of food pictures, F(1, 60) ⫽ 511.7, p ⬍ .01, ␩2 ⫽
.90, and rated these stimuli as significantly more interesting, pleasant, and arousing than nondeprived participants, Fs(1, 60) ⫽
384.9, 134.7, and 140.6, ps ⬍ .01, ␩s2 ⫽ .87, .69, and .70 for
interest, valence, and arousal ratings, respectively. In contrast to
the physiological and behavioral data, however, deprivation status
changed verbal reports differently in participants with bulimia and
control participants. Among control participants, deprivation
caused a stronger increase in the rated desire to eat than in
participants with bulimia, suggesting that the verbal reports of
participants with bulimia were less explicitly influenced by the
internal state of hunger than those of the control participants,
Deprivation ⫻ Pathology, F(1, 60) ⫽ 32.93, p ⬍ .01, ␩2 ⫽ .35.
The interest ratings also revealed a significant Deprivation ⫻
Pathology interaction, F(1, 60) ⫽ 84.3, p ⬍ .01, ␩2 ⫽ .58.
Nondeprived participants with bulimia rated food cues as more
interesting and arousing than nondeprived control participants,
whereas no such differences occurred for deprived participants,
Deprivation ⫻ Pathology, Fs(1, 60) ⫽ 84.3 and 210.3, ps ⬍ .01,
␩2s ⫽ .58 and .78, for interest and arousal ratings, respectively
(see Table 2). In addition, participants with bulimia described food
cues more often as disgusting and fearful relative to control participants, ␹2(4, N ⫽ 64) ⫽ 38.5; p ⬍ .01. Of the participants with
bulimia, 53% rated 1–3 food cues as fear evoking, and 50% rated
1– 4 pictures as disgusting. Only 6.3% of the control participants
judged 1 of the 8 food cues as being disgusting, and 9.4% rated 1
of these pictures as fearful.
Food Consumption
As expected, deprived participants consumed significantly
more food than nondeprived participants, F(1, 60) ⫽ 20.6, p ⬍
.01, ␩2 ⫽ .26. The mean amounts of calories consumed by each
group were 568 (SE ⫽ 82) and 587 kcal (SE ⫽ 59) for deprived
participants with bulimia and control participants, respectively,
and 205 (SE ⫽ 51) and 308 kcal (SE ⫽ 85) for nondeprived
participants with bulimia and control participants, respectively.
Food consumption did not vary between participants with bulimia and control participants in this environment, Deprivation ⫻ Pathology, F(1, 60) ⬍ 1.
Second Experimental Session
Standard Affective Categories
The modulation of the physiological, behavioral, and self-report
measures as a function of the affective valence and arousal of these
nonfood stimuli replicated the findings from the first session.
574
MAULER, HAMM, WEIKE, AND TUSCHEN-CAFFIER
Figure 2. Mean (⫾ SE) skin conductance responses (range-corrected log transformation), heart rate changes
(during 6 s of picture viewing), viewing times (in seconds), ratings of interest, and the desire to eat (a line rating
on a scale from 0 to 20) during viewing of food cues for deprived and nondeprived participants with bulimia
(always left) and control participants (always right) during the first session of picture viewing. FIR ⫽ first
interval response.
Again, the results did not vary as function of psychopathology or
the prior status of deprivation.6
For nondeprived participants with bulimia, the pronounced startle potentiation during viewing of food cues compared with viewing of pleasant materials during the first experimental session was
Food Cues
Startle response magnitudes. Participants with bulimia continued to exhibit significantly larger startle responses when elicited
during viewing of food cues compared with control participants,
Pathology, F(1, 60) ⫽ 8.1, p ⬍ .01, ␩2 ⫽ .12. Although control
participants showed comparable blink magnitudes during viewing
of food cues and other pleasant materials, participants with bulimia
continued to show a significant potentiation of their startle eyeblinks elicited during viewing of food cues relative to other pleasant pictures, F(1, 30) ⫽ 25.4, p ⬍ .01, ␩2 ⫽ .46, or neutral
pictures, F(1, 30) ⫽ 13.0, p ⬍ .01, ␩2 ⫽ .30. This pattern of results
was confirmed by significant Category ⫻ Pathology interactions
for these comparisons, F(1, 60) ⫽ 12.3 and 15.8, ps ⬍ .01, ␩2s ⫽
.17 and .21, for the food versus pleasant content and the food
versus neutral content comparisons, respectively. Figure 3 illustrates the changes of the startle response potentiation (food minus
other pleasant pictures) for participants with bulimia and control
participants according to their prior status of deprivation.
6
Although startle blink and skin conductance response magnitudes were
generally reduced in the second relative to the first experimental session
(Session, F(1, 60) ⫽ 30.9, p ⬍ .01, ␩2 ⫽ .34; F(1, 59) ⫽ 26.6, p ⬍ .01,
␩2 ⫽ .31, for startle blink and skin conductance responses, respectively);
the modulation of these measures by the affective content of the pictures
remained unchanged during the second phase of the experiment. Again, a
comparable pattern was observed for corrugator activity and pleasure
ratings. Accordingly, although viewing times and interest ratings also
generally decreased across sessions (Session, Fs(1, 60) ⫽ 31.9 and 18.3,
ps ⬍ .01, ␩2s ⫽ .35 and .23, for viewing times and interest ratings,
respectively), pleasant and unpleasant pictures were viewed again for a
longer period of time and were rated as more interesting than neutral
pictures. The same pattern of results was obtained for the arousal ratings.
All interactions between Category ⫻ Psychopathology and Category ⫻
Deprivation were again not significant with one exception. Control participants had a stronger potentiation of their startle responses during viewing
of unpleasant pictures relative to neutral materials than participants with
bulimia in this second experimental session.
AFFECT REGULATION AND BULIMIA NERVOSA
Figure 3. Differences of the mean startle responses (⫾SE) elicited during
viewing of food cues and other pleasant pictures during the first session
and the second session of picture viewing for deprived and nondeprived
participants with bulimia and control participants. The second picture
viewing session followed food consumption from a breakfast buffet. Note
that deprived participants ate significantly more calories from the buffet
than nondeprived participants, irrespective of the psychopathology.
strongly reduced during the second session, whereas the amount of
potentiation increased for the previously deprived participants with
bulimia, Deprivation ⫻ Session, F(1, 30) ⫽ 29.5, p ⬍ .01, ␩2 ⫽
.50. These participants with bulimia, however, also consumed
significantly more food during the recreational break than the
previously nondeprived participants with bulimia, suggesting that
the affective valence of food cues changed as a result of eating. No
such interaction occurred for the control participants, Deprivation ⫻ Session, F(1, 30) ⬍ 1. This pattern of results was also
supported by a significant Deprivation ⫻ Session ⫻ Pathology
interaction, F(1, 60) ⫽ 22.0, p ⬍ .01, ␩2 ⫽ .27 (see Figure 3).
These findings were further supported by a correlational analysis
of the linear relationship between food consumption and change in
startle potentiation from Session 1 to Session 2. Although no
significant correlation between food consumption and change in
startle potentiation was found for control participants, (r ⫽ ⫺.08,
ns), a significant correlation between these variables was obtained
for participants with bulimia (r ⫽ .39, p ⬍ .03).
Corrugator facial muscle responses. Corrugator responses
showed the same pattern of results, although the effects were less
pronounced than for startle blink magnitudes. As observed for
startle responses, corrugator activity to food cues increased for
previously deprived participants with bulimia and decreased for
previously nondeprived participants with bulimia, Deprivation ⫻
Session, F(1, 30) ⫽ 11.6, p ⬍ .01, ␩2 ⫽ .28. Again, no such
interaction was observed for control participants, F(1, 29) ⬍ 1. In
contrast to the startle results, the three-way interaction was not
significant for corrugator responses in the between-group
comparison.
575
Skin conductance and viewing times. As expected, skin conductance to food cues as well as viewing times of these pictures
decreased significantly in the second session, Session, Fs(1, 59/
60) ⫽ 13.2 and 9.0, ps ⬍ .01, ␩2s ⫽ .18 and .13, for skin
conductance and viewing times, respectively. Viewing times of
food cues were still increased compared with those for neutral
pictures, Category, F(1, 60) ⫽ 11.5, p ⬍ .01, ␩2 ⫽ .16, but were
now significantly shorter than those for other pleasant materials,
Category, F(1, 60) ⫽ 61.1, p ⬍ .01, ␩2 ⫽ .50. A similar pattern of
results was observed for skin conductance. Electrodermal orienting
responses elicited by food cues were no longer more pronounced
than those evoked by neutral pictures but were now significantly
smaller than those evoked by other pleasant materials, Category,
F(1, 59) ⫽ 8.75, p ⬍ .01, ␩2 ⫽ .13. As during the first experimental session, psychopathology did not modulate this pattern of
results; that is, these effects did not vary for participants with
bulimia and control participants.
Interest ratings, desire to eat, and affective judgments. In line
with behavioral and physiological data, all participants rated food
cues as less interesting, arousing, and pleasant and reported a
reduced desire to eat in the second compared with the first experimental session, Session, Fs(1, 60) ⫽ 128.1, 96.8, 139.2, and
304.6, ps ⬍ .01, ␩2 ⫽ .68, .62, .70, and .84, for interest, pleasure,
arousal, and desire to eat ratings, respectively. Moreover, these
changes were stronger for previously deprived than for nondeprived participants, Session ⫻ Deprivation, Fs(1, 60) ⫽ 96.6, 36.6,
22.9, and 193.7, ps ⬍ .01, ␩2s ⫽ .62, .38, .28, and .76, for interest,
pleasure, arousal, and desire to eat ratings, respectively. In contrast
to behavioral and physiological data, the verbal report data again
clearly discriminated between participants with bulimia and control participants. Participants with bulimia, although no longer
hungry, still reported significantly higher interest in food cues and
rated these cues as more arousing relative to satiated control
participants, Pathology, Fs(1, 60) ⫽ 82.3 and 53.1; ps ⬍ .01,
␩2s ⫽ .58 and .47 for interest and arousal ratings, respectively, and
also reported a significantly higher desire to eat (M ⫽ 6.4, SE ⫽
0.5) than control participants (M ⫽ 4.1, SE ⫽ 0.4), Pathology, F(1,
60) ⫽ 14.6, p ⬍ .01, ␩2 ⫽ .20.
Discussion
Emotional Responses to Food Cues: The Influence
of the Bulimic Psychopathology
Although emotional responses to standard affective materials
were comparable for participants with bulimia and control participants, food cues prompted a different response pattern in both
groups. Food cues prompted an appetitive and positive affective
state in normal control participants as indicated by an inhibition of
the startle response comparable to that induced by other pleasant
stimuli. In contrast, participants with bulimia exhibited a substantial potentiation of their blink response magnitudes, almost comparable to the augmentation that could be observed during viewing
of frankly unpleasant emotional stimuli. These data suggest that
food cues, although having generally appetitive qualities in healthy
volunteers, prompted negative affect in those with bulimia and also
support findings indicating that individuals with bulimia consistently show a decreased initial salivary response to food cues
(Bulik, Lawson, & Carter, 1996; Wisniewski, Epstein, Marcus, &
576
MAULER, HAMM, WEIKE, AND TUSCHEN-CAFFIER
Kaye, 1997). Corrugator facial muscle activity also supports the
conclusion that food cues activate an aversive emotional response
pattern in participants with bulimia. In these individuals with
eating disorders, food cues elicited a strong increase in corrugator
muscle activity, whereas the control participants’ corrugator responses were comparable to those elicited by other pleasant cues.
Indeed, corrugator activity has been shown to have a very close
relationship with the negative valence of visual materials and is
specifically increased during aversive states of disgust (Bradley et
al., 2001; Hamm, Schupp, & Weike, 2003; Lang et al., 1993). An
interesting finding is that participants with bulimia rated the food
pictures overall as being as pleasant and interesting as did the
control participants. This suggests that the participants with bulimia may not have been aware of the negative affect elicited by
the pictures. On the other hand, if participants with bulimia are
instructed to label their feeling states associated with food cues,
these participants rated food cues more often as disgusting and
fearful than did control participants, thus revealing a discrepancy
between the dimensional and categorical judgments. The reason
for this discrepancy might be that during the dimensional ratings,
the participant is more directed to the food cue itself, whereas the
categorical judgment task might rather direct the participant to rate
her internal state. In any event, the categorical ratings support
other research in which individuals with bulimia report more
negative feelings than do others during eating or while looking at,
smelling, or touching food (Bulik et al., 1996; Buree et al., 1990;
Legenbauer, Vögele, & Rüddel, 2004; Neudeck, Florin, &
Tuschen-Caffier, 2001; Staiger et al., 2000). These negative feelings increase if purging is rendered impossible after eating a test
meal (Rosen, Leitenberg, Gross, & Willmuth, 1985) and decrease
after purging (Powell & Thelen, 1996). In the same vein deprivation and subsequent eating affected emotional responding to food
cues in a different way in participants with bulimia and control
participants in the current experiment.
Emotional Responses to Food Cues: The Influence of
Food Deprivation
Deprivation increased viewing times and electrodermal orienting responses to food cues in both groups. Moreover, deprived
participants rated food cues as being more interesting and arousing, suggesting that food cues become more salient when participants are hungry. More important, this increased incentive value of
food cues as a result of the motivational drive was not modulated
by psychopathology, indicating that the regulation of hunger motivation was comparable for both groups. In contrast, deprivation
affected the emotional impact of the food cues in qualitatively
different ways in the two groups. Healthy control participants
showed an increase in startle response magnitudes to food cues
when they were deprived, supporting the between-groups findings
of Drobes et al. (2001). Drobes and colleagues argued that food
cues might prompt a state of frustrative nonreward in deprived
subjects, because the experimental context did not allow immediate food consumption. Therefore, food cues might activate a negative affective state of frustration in hungry participants, and the
startle data of the current experiment support these conclusions. It
has to be mentioned, however, that corrugator activity was reduced
during viewing of food cues in deprived control participants replicating the findings of Drobes et al. (2001). Such a facial action
pattern is normally associated with positive valence and would
suggest that food cues indeed became more attractive after deprivation. A possible interpretation of these differences might be,
comparable to the differences in the verbal report measures, that
startle modulation primarily indexes the subcortically mediated
internal affective disposition, whereas corrugator activity is more
driven by the attractiveness of the external cues.
In contrast with control women, deprived women with bulimia
exhibited significantly less startle potentiation during viewing of
food cues than did nondeprived women with bulimia. In deprived
women with bulimia, startle response magnitudes elicited during
viewing of food cues were comparable to those evoked during
viewing of neutral pictures. These data indicate that deprivation
reduced the startle potentiation to food cues in women with bulimia. This finding supports an affect regulation model, suggesting
that the negative affect induced by food cues might motivate
individuals with bulimia utilizing fasting and restrained eating to
reduce the negative affect associated with food items. This interpretation was supported by the startle modulation during viewing
of food cues after food intake.
Food Intake and Affect Regulation in Bulimia Nervosa
Deprived control participants and participants with bulimia consumed significantly more food from the breakfast buffet than did
nondeprived participants. As expected, food consumption resulted
in a significant reduction of electrodermal orienting, viewing
times, interest, and arousal ratings of food cues, again supporting
the idea that these indices are related to the increased attention that
is allocated to food cues as a result of the motivational state of
hunger. Although autonomic orienting and behavioral data did not
differ between both groups, participants with bulimia still rated
food cues as being more arousing and interesting than did control
participants. Moreover, startle responses elicited during viewing of
food cues varied substantially between participants with bulimia
and control participants after food consumption. Whereas for the
control group startle response magnitudes were not affected by the
amount of food consumption, blink magnitudes during viewing of
food cues were significantly affected by the previous eating behavior in the bulimia nervosa group. Nondeprived women with
bulimia, who were not hungry and therefore consumed fewer
calories at the breakfast buffet, showed a pronounced decrease in
startle response magnitudes elicited during food cues: Blink magnitudes were now comparable to those elicited during viewing of
other pleasant pictures. This restrained food intake might have
induced a conviction of control that subsequently reduced the
aversive emotional quality of the food cues. This interpretation
was also supported by the results of corrugator activity. An opposite response pattern was observed for the previously deprived
participants with bulimia, who consumed a larger amount of food
because they were hungry. This group did not show a decrease but
exhibited a significant increase in startle response magnitude during viewing of food cues instead. These data are in line with the
hypothesis that the deprivation-induced incentive properties of the
food cues might now have been blunted by satiation or the effects
of perceived overeating.
AFFECT REGULATION AND BULIMIA NERVOSA
Implications for the Psychopathology of Bulimia Nervosa
In the present study we tested the emotional responding of
deprived and nondeprived women with bulimia to salient food
cues. Moreover, we investigated whether these affective responses
are modified by eating. The data clearly show that food cues evoke
negative emotional responses in individuals with bulimia comparable with those elicited by other unpleasant stimuli. This finding
has important implications for understanding the psychopathology
of bulimia nervosa. In his dual pathway model of bulimic pathology, Stice (2001) hypothesized that elevated pressure to be thin
fosters body dissatisfaction in individuals with bulimia. This increased body dissatisfaction then promotes negative affect. Our
data support and extend this model by demonstrating that food
cues in the environment effectively prime this negative affect. The
present data also suggest that the negative affect primed by food
items may motivate those with bulimia utilizing fasting and restrained eating to ameliorate the negative affect associated with
food cues. In a sense, individuals with bulimia make food less
frightening or threatening by demonstrating control over their
consumption of it. According to the dual pathway model, however,
deprivation further increases negative affect. Actually, prospective
studies revealed that fasting predicted overall enhancement of
negative affect (Stice & Bearman, 2001). Accordingly, deprivation
might produce the same negative affect that has been found to be
the motivational core of the drug withdrawal syndrome (see Baker,
Piper, McCarthy, Majeskie, & Fiore, 2004). From this perspective,
it is surprising that the food-induced potentiation of the startle
response was reduced in individuals with bulimia after deprivation.
Deprivation, however, not only induces general distress but also
inflates the incentive value of food cues (see Baker et al., 2004).
There is evidence from data obtained from former prisoners of war
that after severe food deprivation, these individuals not only eat
beyond metabolic requirements when given free access to food but
also show a strong preoccupation with food (Polivy, Zeitlin, Herman, & Beal, 1994; for discussion of these effects see also Baker
et al., 2004). The significant reduction of the protective startle
reflex during viewing of food cues in deprived participants with
bulimia is in line with this interpretation. Supporting this view,
greater activation of the amygdala and related paralimbic structures was found during viewing of food-related stimuli when
participants were hungry (LaBar et al., 2001). This increased
incentive value of the food cues together with the overall negative
affective state induced by deprivation might explain why contact
with specific food cues could trigger binge-eating episodes in
individuals with bulimia, almost comparable to the motivational
basis of drug cues triggering relapse (Baker et al., 2004). Recent
data from Mann and Ward (2004) also demonstrate that food
consumption is significantly increased, if food cues are made more
salient. Of course, deprivation might reduce startle among individuals with bulimia for another reason; a period of successful
deprivation might create a sense of control over food and this may
render it less threatening.
If the restrained eating pattern collapses, that is, if individuals
with bulimia fail to maintain tight control over their eating, food
once again becomes threatening. Participants with bulimia who ate
a greater number of calories from the breakfast buffet (i.e., the
previously deprived participants) subsequently showed a strong
potentiation of their startle reflex during viewing of food cues,
577
suggesting that these stimuli now prompted a defensive motivational state. This pattern of results is in line with cognitive models
of bulimic pathology suggesting that core beliefs such as “control
over eating” are central for bulimia nervosa (Cooper, Wells, &
Todd, 2004). Rigid self-regulation seems to be fundamental to the
self-esteem of women with bulimia nervosa (Fairburn, Cooper, &
Shafran, 2003). If this self-regulation is violated, the negative
affect induced by food cues seems to be increased as suggested by
the data of the current study. If, however, the women with bulimia
had the conviction that they were able to control their eating
behavior (e.g., as manifest in modest food intake during the breakfast or by fasting during the pre-experimental deprivation period),
startle responses evoked by food cues decreased.
The data of the current experiment not only reveal some new
aspects in the psychopathology of bulimia nervosa, but they may
also have some implications for the treatment of this disorder.
According to the present results, the effectiveness of cue exposure
therapy might be increased if exposure is conducted after the
consumption of a normal meal, because the patient with bulimia
has to cope with the negative affect associated with the violation
against the restrained eating pattern, that is, the increased (but
normal) food intake. Moreover, this paradigm might also be suitable for assessments of treatment effects beyond the level of verbal
report on the level of the basic motivational potency of food cues
during hungry and satiated states.
References
Allen, N. B., Trinder, J., & Brennan, C. (1999). Affective startle modulation on clinical depression: Preliminary findings. Biological Psychiatry,
46, 542–550.
American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: Author.
Baker, T. B., Piper, M. E., McCarthy, D. E., Majeskie, M. R., & Fiore,
M. C. (2004). Addiction motivation reformulated: An affective processing model of negative reinforcement. Psychological Review, 111, 35–51.
Bradley, M. M. (2000). Emotion and motivation. In J. T. Cacioppo, L. G.
Tassinary, & G. G. Berntson (Eds.), Handbook of psychophysiology (pp.
602– 642). New York: Cambridge University Press.
Bradley, M. M., Codispoti, M., Cuthbert, B. N., & Lang, P. J. (2001).
Emotion and motivation. I: Defensive and appetitive reactions in picture
processing. Emotion, 1, 276 –298.
Brewerton, T., Dansky, B., Kilpatrick, D., & O’Neal, P. (2000). Which
comes first in the pathogenesis of bulimia nervosa: Dieting or binging?
International Journal of Eating Disorders, 28, 259 –264.
Bulik, C. M., & Brinded, E. C. (1994). The effect of food deprivation on
the reinforcing value of food and smoking in bulimic and control
women. Physiology & Behavior, 55, 665– 672.
Bulik, C. M., Lawson, R. H., & Carter, F. A. (1996). Salivary reactivity in
restrained and unrestrained eaters and women with bulimia nervosa.
Appetite, 27, 15–24.
Bulik, C. M., Sullivan, P., Carter, F., & Joyce, P. (1997). Initial manifestations of disordered eating behavior: Dieting versus binging. International Journal of Eating Disorders, 22, 195–201.
Buree, B. U., Papageorgis, D., & Hare, R. D. (1990). Eating in anorexia
nervosa and bulimia nervosa: An application of the tripartite model of
anxiety. Canadian Journal of Behavioural Science, 22, 207–218.
Cacioppo, J. T., Klein, D. J., Berntson, G. G., & Hartfield, E. (1993). The
psychophysiology of emotion. In M. Lewis & J. M. Haviland (Eds.),
Handbook of emotions (pp. 119 –142). New York: Guilford Press.
Carter, F., & Bulik, C. M. (1996). Cue reactivity and bulimia nervosa:
578
MAULER, HAMM, WEIKE, AND TUSCHEN-CAFFIER
Refining and standardizing methodology. Behavior Change, 13, 98 –
111.
Center for the Study of Emotion and Attention (CSEA). (1995). The
International Affective Picture System (IAPS) [Photographic slides/CD].
Gainesville FL: The Center for Research in Psychophysiology, University of Florida.
Cook, E. W., Davis, T. L., Hawk, L. W., Spence, E. L., & Gautier, C. H.
(1992). Fearfulness and startle potentiation during aversive visual stimuli. Psychophysiology, 29, 633– 645.
Cooper, M., Wells, A., & Todd, G. (2004). A cognitive model of bulimia
nervosa. British Journal of Clinical Psychology, 43, 1–16.
Davis, M. (2000). The role of the amygdala in conditioned and unconditioned fear and anxiety. In J. P. Aggleton (Ed.), The amygdala (pp.
213–287). Oxford: Oxford University Press.
Davis, R., Freeman, R., & Garner, D. (1988). A naturalistic investigation
of eating behavior of bulimia nervosa. Journal of Consulting and Clinical Psychology, 56, 273–279.
Drobes, D., Miller, E. J., 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.
Fairburn, C. G., & Cooper, Z. (1993). The Eating Disorder Examination
(12th ed.). In C. G. Fairburn & G. T. Wilson (Eds.), Binge eating.
Nature, assessment, and treatment (pp. 317–360). New York: Guilford
Press.
Fairburn, C. G., Cooper, Z., & Shafran, R. (2003). Cognitive behaviour
therapy for eating disorders: A “transdiagnostic” theory and treatment.
Behaviour Research and Therapy, 41, 509 –528.
Fairburn, C. G., Stice, E., Cooper, Z., Doll, H., Norman, P., & O’Connor,
M. (2003). Understanding persistence in bulimia nervosa: A 5-year
naturalistic study. Journal of Consulting and Clinical Psychology, 71,
103–109.
Fridlund, A. J., & Cacioppo, J. T. (1986). Guidelines for human electromyographic research. Psychophysiology, 23, 567–589.
Globisch, J., Hamm, A. O., Schneider, R., & Vaitl, D. (1993). A computer
program for scoring reflex eyeblink and electrodermal responses written
in PASCAL [Abstract]. Psychophysiology, 30(Suppl.), S30.
Graham, F. K. (1978). Constraints in measuring heart rate and period
sequentially through real and cardiac time. Psychophysiology, 15, 492–
495.
Hamm, A. O., Cuthbert, B. N., Globisch, J., & Vaitl, D. (1997). Fear and
the startle reflex: Blink modulation and autonomic response patterns in
animal and mutilation fearful subjects. Psychophysiology, 34, 97–107.
Hamm, A. O., Schupp, H. T., & Weike, A. I. (2003). Motivational organization of emotions: Autonomic changes, cortical responses, and reflex
modulation. In R. J. Davidson, K. Scherer, & H. H. Goldsmith (Eds.),
Handbook of affective sciences (pp. 187–211). Oxford, England: Oxford
University Press.
Hamm, A. O., & Vaitl, D. (1993). Emotionsinduktion durch visuelle Reize:
Validierung einer Stimulationsmethode auf drei Reaktionsebenen [Emotion induction by visual stimuli: Validation of a method to evoke
emotion using three response systems]. Psychologische Rundschau, 44,
143–161.
Hawk, L. W., Baschnagl, J. S., Ashare, R. L., & Epstein, L. H. (2004).
Craving and startle modification during in vivo exposure to food cues.
Appetite, 43, 285–294.
Hodes, R. L., Cook, E. W., III, & Lang, P. J. (1985). Individual differences
in autonomic response: Conditioned association or conditioned fear?
Psychophysiology, 22, 545–560.
Konorski, J. (1967). Integrative activity of the brain: An interdisciplinary
approach. Chicago: University of Chicago Press.
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.
Lang, P. J. (1985). The cognitive psychophysiology of emotion: Fear and
anxiety. In A. H. Tuma & J. D. Maser (Eds.), Anxiety and the anxiety
disorders (pp. 131–170). Hillsdale, NJ: Erlbaum.
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1998). Emotion, motivation, and anxiety: Brain mechanisms and psychophysiology. Biological
Psychiatry, 44, 1248 –1263.
Lang, P. J., Greenwald, M. K., Bradley, M. M., & Hamm, A. O. (1993).
Looking at pictures: Affective, facial, visceral, and behavioral reactions.
Psychophysiology, 30, 261–273.
Lavy, E. H., & van den Hout, M. A. (1993). Attentional bias for appetitive
cues: Effects of fasting in normal subjects. Behavioural and Cognitive
Psychotherapy, 21, 297–310.
Legenbauer, T., Vögele, C., & Rüddel, H. (2004). Anticipatory effects of
food exposure in women diagnosed with bulimia nervosa. Appetite, 42,
33– 40.
Leitenberg, H., Gross, J., Peterson, J., & Rosen, J. C. (1984). Analysis of
an anxiety model and the process of change during exposure plus
response prevention treatment of bulimia nervosa. Behavior Therapy,
15, 3–20.
Leon, G. R., Fulkerson, J. A., Perry, C. L., & Early-Zald, M. B. (1995).
Prospective analysis of personality and behavioral vulnerabilities and
gender influences in the later development of disordered eating. Journal
of Abnormal Psychology, 104, 140 –149.
Lykken, D. T., & Venables, P. H. (1971). Direct measurement of skin
conductance: A proposal for standardization. Psychophysiology, 8, 656 –
672.
Mann, T., & Ward, A. (2004). To eat or not to eat: Implications of the
attentional myopia model for restrained eaters. Journal of Abnormal
Psychology, 113, 90 –98.
Neudeck, P., Florin, I., & Tuschen-Caffier, B. (2001). Food exposure in
patients with bulimia nervosa. Psychotherapy and Psychosomatics, 70,
193–200.
Patrick, C. J., Bradley, M. M., & Lang, P. J. (1993). Emotion in the
criminal psychopath: Startle reflex modulation. Journal of Abnormal
Psychology, 102, 82–92.
Patton, G., Johnson-Sabine, E., Wood, K., Mann, A., & Wakeling, A.
(1990). Abnormal eating attitudes in London schoolgirls—A prospective
epidemiological study: Outcome at twelve month follow-up. Psychological Medicine, 20, 383–394.
Polivy, J., Herman, C. P., & Howard, K. I. (1988). The restraint scale:
Assessment of dieting. In M. Hersen & A. Bellack (Eds.), Dictionary of
behavioral assessment techniques (pp. 377–380). New York: Pergamon
Press.
Polivy, J., & Herman, C. P. (2002). Causes of eating disorders. Annual
Reviews of Psychology, 53, 187–213.
Polivy, J., Zeitlin, S. B., Herman, C. P., & Beal, A. L. (1994). Food
restriction and binge eating: A study of former prisoners of war. Journal
of Abnormal Psychology, 103, 409 – 411.
Powell, A., & Thelen, M. (1996). Emotions and cognitions associated with
bingeing and weight control behavior in bulimia. Journal of Psychosomatic Research, 40, 317–328.
Prokasy, W. F., & Kumpfer, K. L. (1973). Classical conditioning. In W. F.
Prokasy & D. C. Raskin (Eds.), Electrodermal activity in psychophysiological research (pp. 157–202). New York: Academic Press.
Raynor, H., & Epstein, L. (2003). The relative-reinforcing value of food
under differing levels of food deprivation and restriction. Appetite, 40,
15–24.
Rosen, J., Leitenberg, H., Gross, J., & Willmuth, M. (1985). Standardized
test meals in the assessment of bulimia nervosa. Advances in Behavior
Research and Therapy, 7, 181–197.
Rosen, J., Tacy, B., & Howell, D. (1990). Life stress, psychological
symptoms and weight reducing behavior in adolescent girls: A prospective analysis. International Journal of Eating Disorders, 9, 255–267.
Spielberger, C., Gorsuch, R., & Lushene, R. (1970). Manual of the State-
AFFECT REGULATION AND BULIMIA NERVOSA
Trait Anxiety Inventory (self-evaluation questionnaire). Palo Alto, CA:
Consulting Psychologists Press.
Staats, A., & Hammond, O. (1972). Natural words as physiological conditioned stimuli: Food-word-elicited salivation and deprivation effects.
Journal of Experimental Psychology, 96, 206 –208.
Staiger, P., Dawe, S., & McCarthy, R. (2000). Responsivity to food cues in
bulimic women and controls. Appetite, 35, 27–33.
Stice, E. (2001). A prospective test of the dual-pathway model of bulimic
pathology: Mediating effects of dieting and negative affect. Journal of
Abnormal Psychology, 110, 124 –135.
Stice, E. (2002). Risk and maintenance factors for eating pathology: A
meta-anlaytic review. Psychological Bulletin, 128, 825– 848.
Stice, E., & Bearman, S. (2001). Body image and eating disturbances
prospectively predict growth in depressive symptoms in adolescent girls:
A growth curve analysis. Developmental Psychology, 37, 597– 607.
Stunkard, A. J., & Messick, S. (1985). The Three-Factor Eating Questionnaire to measure dietary restraint, disinhibition and hunger. Journal of
Psychosomatic Research, 29, 71– 81.
Venables, P. H., & Christie, M. J. (1980). Electrodermal activity. In I.
Martin & P. H. Venables (Eds.), Techniques in psychophysiology (pp.
3– 67). Chichester, England: Wiley.
579
Vrana, S. R., Spence, E. L., & Lang, P. J. (1988). The startle probe
response: A new measure of emotion? Journal of Abnormal Psychology,
97, 487– 491.
Webber, J., & Macdonald, I. A. (1994). The cardiovascular, metabolic, and
hormonal changes accompanying acute starvation in men and women.
British Journal of Nutrition, 71, 437– 447.
Williamson, D., Kelley, M., Davis, C., Ruggiero, L., & Veitia, M. (1985).
The psychophysiology of bulimia nervosa. Advances in Behavior Research and Therapy, 7, 163–172.
Wisniewski, L., Epstein, L. H., Marcus, M. D., & Kaye, W. (1997).
Differences in salivary habituation to palatable foods in bulimia nervosa
patients and controls. Psychosomatic Medicine, 59, 427– 433.
Wooley, O., & Wooley, S. (1981). Relationships of salivation in humans to
deprivation, inhibition, and the encephalization of hunger. Appetite, 2,
331–350.
Received October 1, 2004
Revision received May 31, 2005
Accepted January 10, 2006 䡲
Download