Physiology & Behavior 84 (2005) 313 – 319

Effects of allocation of attention on habituation to olfactory

and visual food stimuli in children
Leonard H. Epstein*, Frances G. Saad, April M. Giacomelli, James N. Roemmich
Department of Pediatrics, School of Medicine and Biomedical Sciences, State University of New York,
Farber Hall; Room G56, 3435 Main Street, Buffalo, NY 14214, United States

Received 9 August 2004; received in revised form 6 December 2004; accepted 15 December 2004

Abstract

Responding to food cues may be disrupted by allocating attention to other tasks. We report two experiments examining the effects of
allocation of attention on salivary habituation to olfactory plus visual food cues in 8–12-year-old children. In Experiment 1, 42 children were
presented with a series of 8 hamburger food stimulus presentations. During each intertrial interval, participants completed a controlled (hard),
or automatic (easy) visual memory task, or no task (control). In Experiment 2, 22 children were presented with 10 presentations of a pizza
food stimulus and either listened to audiobook or no audiobook control. Results of Experiment 1 showed group differences in rate of change
in salivation ( p=0.014). Children in the controlled task did not habituate to repeated food cues, while children in the automatic ( pb0.005) or
no task ( pb0.001) groups decreased responding over time. In Experiment 2, groups differed in the rate of change in salivation ( p=0.004).
Children in the no audiobook group habituated ( pb0.001), while children in the audiobook group did not habituate. Changes in the rate of
habituation when attending to non-food stimuli while eating may be a mechanism for increasing energy intake.
D 2004 Elsevier Inc. All rights reserved.

Keywords: Habituation; Salivation; Attention; Olfaction

A large and consistent body of research has shown that
rats [1–5], non-human primates [6,7] and humans [8–13]
habituate to repeated food cues, and dishabitutate or recover
responding when a new food cue is presented. Research has
also shown that habituation to food cues is associated with
the termination of eating in non-human primates [6,7] and
humans [8], and the rate of change for salivary habituation
and motivated responding for food is very similar in
children [14]. Presenting a new food after habituation can
result in dishabituation of salivary responding and a
recovery of eating [8]. Similarly, presenting a new food in
a motivated behavior paradigm will result in a resumption in
responding for the new food in children [14]. Dishabituation
of responding to new food cues may in part mediate the
influence of food variety on increases in food intake [15].
* Corresponding author. Tel.: +1 716 829 3400; fax: +1 716 829 3993.
E-mail address: LHENET@buffalo.edu (L.H. Epstein).
0031-9384/$ - see front matter D 2004 Elsevier Inc. All rights reserved.
doi:10.1016/j.physbeh.2004.12.009
In addition to the influence of novel food cues on
dishabituation or recovery of responding, non-food stimuli
can serve to dishabituate responding to food cues. For
example, playing a video game in between food presenta-
tions can slow the rate of habituation [16]. Playing video
games can dishabituate responding, and the more arousal
generated by a video game the greater the degree of
dishabituation [10]. One model that may help understand
how food or environmental stimuli can act to influence
responding to repeated food cues is the information
processing model developed by Wagner [17–19]. Wagner
argues that habituation is mediated in part by the matching
of new information to information that is stored in short-
term memory, and allocation of attention to new information
removes information from short-term memory and disrupts
habituation. The information processing model was tested
by having participants engage in either a controlled search
task (demanding attentional resources), an automatic search
task (needing fewer attentional resources), or no task in
314 L.H. Epstein et al. / Physiology & Behavior 84 (2005) 313–319
between presentations of repeated food cues in two experi-
ments [12]. Research has suggested that there is a distinction
between automatic and controlled modes of information
processing [20–22]. Automatic processes require fewer
attentional resources and are possible when stimuli are
consistently and reliably mapped to their appropriate
responses. On the other hand, controlled responses demand
more attentional resources when the stimulus-response
mappings are inconsistent and unreliable. Consistent with
the allocation of attention hypothesis, the automatic and no
task groups habituated to the repeated presentation of food
cues in both experiments, but the controlled search group
did not.
The purpose of this study is to extend our research on
the influence of allocation of attention on habituation to
food cues to children. Research suggests that children
consume a substantial amount of energy while engaged in
other activities, such as watching television [23,24], and
reducing access to behaviors such as television watching
may reduce energy intake [25]. Consistently engaging in
alternative activities while eating may alter the rate of
habituation to repeated food cues, and thus, increase
energy intake. We have completed an initial study in
children demonstrating habituation to repeated food cues
and showed that the habituation model fit both salivation
as well as motivated responding to obtain food [14]. The
two studies in this report are designed to replicate the
influence of tasks that vary in their attentional demands on
habituation to repeated food cues, and to examine the
influence of common auditory distractors on the rate of
habituation. Experiment 1 compares the influence of
memory tasks that require different degrees of attention,
while Experiment 2 evaluates the influence of attending to
interesting audiobooks.
1. Experiment 1
1.1. Method
1.1.1. Participants
Participants were 21 male and 21 female non-obese (b95
BMI percentile) [26] children between the ages of 8 and 12
years old recruited from a newspaper advertisement and
provided US$20.00 compensation for participation. Poten-
tial participants were excluded if they met any of the
following criteria: medications or conditions that could
influence olfactory sensory responsiveness or appetite (e.g.,
upper respiratory illness, diabetes, ADHD, methylpheni-
date); dietary restraint that would alter responding to food
cues; current psychological disorder or developmental
disability; or not rating test foods at least moderately liked.
Participants were randomly assigned to one of the three
groups: controlled search task, automatic search task and no
task. The sample included 98% non-Hispanic white children
and 2% African American children.
1.1.2. Procedures
Parents of the participants were screened by telephone
to determine whether they met the above inclusion
criteria, with the exception of liking of the test foods,
which was assessed during the session. Eligible partic-
ipants were scheduled for a 90-min appointment and the
parents were instructed to not have the children consume
the test food for 24 h and not to eat for at least 3 h prior
to coming to the laboratory. Upon arrival to the
laboratory, participants and parents read and signed
informed consent and assent forms. Parents then com-
pleted a socioeconomic form [27], while children com-
pleted 5-point Likert scales, which assessed liking of the
study foods and hunger, the Dutch Eating Behavior
Questionnaire adapted for children [28] and a same-day
food recall. Participants’ heights and weights were then
measured.
1.1.2.1. Experimental tasks. To adapt participants to the
experimental methods, participants received four 1-min
practice sessions of the search task, followed by a 1-min
habituation trial using water as a neutral stimulus. They
were then provided with eight 1-min habituation trials to
half of a fresh Burger KingR hamburger sandwich served on
a 7 in. plate and heated in a microwave oven for 25 s. After
each habituation trial, food stimuli were promptly removed
from the experimental room. During salivation collection,
participants wore headphones and listened to 62 dB of white
noise to control for auditory stimulation. After completion
of the habituation trials, food liking was reassessed. The
search tasks took place in the 1-min period between
habituation trials 1 and 8, presented on a color video
monitor controlled by a BASIC computer program. The
tasks consisted of a four consonant memory-set presented
for 10 s followed by 20 presentations of 2 character search
frames shown for 2 s. Each search frame remained on the
screen for the same duration to equate total task duration
across groups. Participants responded yes by pressing the
left mouse button if a search frame matched the memory-set
or no by pressing the right button if the search frame did not
match a memory-set.
The controlled search task had target and distractor
consonants that varied from trial to trial [20,21]. The
controlled task provided participants with memory-set that
included four consonants, and search frames that either
included at least one consonant that matched the consonants
in the memory-set (correct response) or two incorrect
consonants (incorrect response). The automatic search task
required less allocation of attention than the controlled
search task since the search frames included either a correct
consonant and a numeric character (correct response) or two
numeric characters (incorrect response). The no task
condition did not involve attending to a task, and
participants in the no task condition continued to listen to
white noise during the intertrial interval. The number of
errors in each memory-set trial were recorded as a
 L.H. Epstein et al. / Physiology & Behavior 84 (2005) 313–319
manipulation check for the controlled search and automatic
search groups.
1.1.2.2. The laboratory environment. The laboratory used
for these experiments was specially constructed for eating
and olfactory experiments. To isolate the olfactory stimuli,
and eliminate any possibility that stimuli from earlier trials
could influence current responding, the food stimulus was
removed after each trial and brought into another room.
The laboratory is equipped with an air delivery system that
continually cycles fresh air into each room. The rooms are
in negative pressure, so that the exhaust has greater cubic
feet per minute than the supply, and the air in the
laboratory rooms is circulated approximately 10 times/h,
or new air is circulated once every 6 min. In addition, the
experimental room (1385 ft3) includes a HEPA (high
efficiency particle arresting) filter that circulates air from
150 to 175 ft3/min. The combination of the air control
system and the HEPA filter reduce the possibility of smells
lingering in the room beyond an individual stimulus
presentation.
1.1.3. Measures
1.1.3.1. Salivation. Whole mouth parotid salivary flow was
measured using the Strongin-Hinsie Peck method [29].
Participants were seated in a comfortable chair and instructed
on proper dental roll placement (cylindrical, 7 mm diameter,
38 mm length, Richmond Dental, Charlotte, NC). They
placed cotton rolls under the tongue and on both the left and
right sides of mouth between the cheek and lower gum. After
the experimenter ensured that placement of the cotton rolls
was correct, participants were instructed not to swallow any
saliva, not to move their tongue, talk or make any chewing
motions. Olfactory and visual stimuli were presented and
saliva collected for 1-min periods, followed by 1-min
intertrial intervals. The food stimulus involved having
participants smell and look at food stimuli held approx-
imately 3 in. from their nose, and to attend to the aroma of the
food while imagining its taste. The food stimuli were
microwaved prior to presentation to enhance olfactory
stimulation. After the 1-min collection period, subjects
removed the dental rolls and returned them to the plastic
bag. Salivation was measured by pre- and post-weights of
cotton rolls to 0.01 g on an Ohaus Precision Standard Scale
(Florham Park, NJ). The difference from baseline served as
the dependent measure.
1.1.3.2. Subjective ratings. Liking of study foods, Burger
KingR hamburgers in Experiment 1 and Domino’sR cheese
pizzas in Experiment 2, were rated on 5-point Likert-type
scales [30] with 1 anchored by bdo not likeQ and 5 anchored
by blike very muchQ. Hunger was assessed by a 5-point
Likert scale, anchored by 1 as bnot hungryQ to 5 anchored as
bvery hungryQ. Food consumed the day of the experiment
was assessed to evaluate total energy intake consumed prior
315
to the test appointment, to ensure that the participants did
not consume the test foods earlier in the day and to ensure
that children did not eat 3 h prior to the test appointment.
Energy intake was calculated using Nutritionist V nutrient
analysis software [31].
1.1.3.3. Dietary restraint. Dietary restraint was measured
using the dietary restraint scale of the child version of the
Dutch Eating Behavior Questionnaire that has been used for
both males and females in previous studies [28]. A total
score greater than 7 for questions 1 through 6 was
considered dietary restrained.
1.1.3.4. Demographics. A demographic questionnaire [27]
was utilized to obtain information about socioeconomic
status, class, ethnicity and race.
1.1.3.5. Anthropometrics. Height (cm) was assessed by
using a SECA (SECA, Hanover, MD) stadiometer, and
weight (kg) was measured by the use of a balance beam
scale calibrated daily. Height and weight were converted to
BMI (kg/m2).
1.1.4. Analytical plan
Characteristics of the participants were compared
between groups using a one-way analysis of variance
(ANOVA). Changes in salivation from baseline were
assessed using a mixed analysis of covariance (ANCOVA),
with group (controlled search, automatic search, no task
control) as the between-subjects variable and trials (1–8) as
the within-subjects factor and baseline salivation as the
covariate. Baseline salivation was used as the covariate
because of the relationship between initial levels of
salivation and change in salivation over trials, which was
significant for seven of the eight trials in Experiment 1.
Linear contrasts were used to examine the rate of change by
group over the eight salivation trials. Accuracy on the
memory tasks were assessed using a two-factor mixed
repeated measures ANOVA with group (controlled search,
automatic search) as the between-subjects variable and
intertrial intervals (1–7), as the within-subjects variables.
Statistical analyses were completed using SYSTAT version
10 [32].
1.2. Results
The average participant was 10.9F1.4 (MFS.D.) years
of age, had a body mass index (BMI=kg/m2) of 18.0F2.5, a
BMI percentile of 53.3F27.7 and a dietary restraint score of
2.2F1.9. Participants rated the test food as moderately to
highly liked on a 5-point Likert scale of liking (hamburger
sandwich=4.1F0.8). Average baseline salivation was
1.18F0.71 g. No significant differences were observed in
any baseline measures between groups (Table 1).
The salivation results are presented for the three groups in
the left graph of Fig. 1. A significant interaction of grouptrial
316 L.H. Epstein et al. / Physiology & Behavior 84 (2005) 313–319

Table 1
Characteristics of participants in the controlled search, automatic search and the no task groups for Experiment 1
Group
Control task Automatic task No task
M S.D. M S.D. M S.D.
Age (years) 11.3 1.2 10.9 1.3 10.6 1.5
Body mass index (BMI) 17.9 2.4 18.4 2.8 17.6 2.4
BMI percentile 50.5 26.8 57.2 30.2 52.3 27.6
Restraint scores 2.5 1.7 2.2 2.4 2.0 1.8
Hamburger liking 4.0 0.7 4.0 1.0 4.3 0.8
Subjective hunger 4.5 0.5 4.1 0.9 4.7 0.6
Hamburger olfactory hedonics 4.4 0.6 3.9 1.1 3.9 1.0
Self-reported calories (kcal) 753 299 697 272 777 311
Socioeconomic status 43.1 12.1 42.5 8.9 46.3 10.4
Baseline salivation (g) 1.27 0.71 1.09 0.72 1.18 0.75

was found for salivary habituation ( F(14,266)=2.07,
p=0.014), and there was a significant change over trials
( F(7,266)=2.55, p=0.015). Contrasts showed the automatic
search group ( F(1,38)=9.04, p=0.005) and the no task group
( F(1,38)=21.67, pb0.001) displayed habituation over the
trials as their salivation gradually decreased, and there was no
significant difference in their rate of change. The controlled
task showed no significant change over trials. Contrasts
revealed a significant difference in the rate of change between
the controlled task versus the two groups that did habituate
(automatic search and no-task groups) ( F(1,38)=6.25,
p=0.017). Children showed a non-significant increase in
liking ratings from 4.1 to 4.4, with no differences in the
change by groups.
The analysis of the accuracy on trials 1–7 showed a
significant interaction of grouptrial ( F(6,156)=4.53,
pb0.001), with a main effect of total errors ( F(1,26)=21.82,
pb0.001), as well as a main effect of trials ( F(6,156)=3.29,
p=0.004). Contrasts showed a significant decrease in errors
over trials for the controlled search group ( F(1,26)=23.96,
pb0.001). The differences between groups in errors and the
change pattern of errors over trials are presented in the right
graph of Fig. 1.
2. Experiment 2
2.1. Methods
2.1.1. Participants
Participants were 12 male and 10 female 9–12-year-old
non-obese (b95 BMI percentile) [26] children. Participants
were randomly assigned to one of two groups: audiobook
and no audiobook. The sample included 59% non-Hispanic
white children, 9% Hispanic children, 18% African Amer-
ican and 14% were mixed race of African American and
American Indian.
2.1.2. Procedures
General procedures were identical to those of Experiment
1. Before the habituation trials began, the participants rated
how much they liked the study food stimulus, Domino’sR

Fig. 1. Changes (meanFS.E.M.) in salivation (left panel) and errors (right panel) for participants in the controlled search, automatic search and no task groups
for Experiment 1.
 L.H. Epstein et al. / Physiology & Behavior 84 (2005) 313–319 317

Table 2 multiple-choice questions about the story which were

Characteristics of participants in the audio book group and the no audio written at the third grade level and the liking scales were
book group for Experiment 2
administered. Participants in the no audiobook group
Group
continued to listen to 62 dB of white noise during the
Audiobook No audiobook intertrial intervals.
M S.D. M S.D.
Age (years) 10.7 1.1 11.4 1.2 2.1.3. Analytical plan
Body mass index (BMI) 18.4 1.5 19.3 2.8 A one-way ANOVA compared characteristics of the
BMI percentile 64.9 19.5 64.6 24.7 participants between groups. Changes in salivation from
Restraint scores 4.1 3.3 3.2 2.2
Pizza liking 4.7 0.5 4.8 0.4
baseline were assessed using a mixed analysis of covariance
Subjective hunger 4.4 0.8 4.0 0.9 (ANCOVA), with group (audiobook, no audiobook) as the
Pizza olfactory hedonics 4.5 0.8 4.3 1.2 between-subjects variable and trials (1–10) as the within-
Self-reported calories (kcal) 545 378 817 452 subjects factor and baseline salivation as the covariate.
Socioeconomic status 38.2 13.1 45.0 10.9 Baseline salivation was used as the covariate, as baseline
Baseline salivation (g) 1.15 0.66 1.23 0.50
levels were related to change for 7 of the 10 trials in
Experiment 2. Contrasts were used to examine the rate of
cheese pizza and each of the three audiobooks using a 5- change over the 10 salivation trials for each group.
point Likert scale, with 1 indicating bdo not like at allQ and 5
indicating blike very muchQ. The participants then ranked 2.2. Results
the audiobooks, placing the number 1 next to their most
favorite and the number 3 next to their least favorite. The The average participant was 11.0F1.1 years of age,
three audiobooks were from a series of Bunnicula children’s had a BMI of 18.8F2.2, had a BMI percentile of
audiobooks [33–35]. Children were provided with ten 1-min 64.7F21.7 and a restraint score of 3.6F2.8. Participants
habituation trials with a fresh slice of a Domino’sR cheese rated the habituating food stimulus pizza and audiobooks
pizza served on a 9 in. plate and heated in the microwave as moderately to highly liked on a 5-point Likert scale of
for 10 s. liking (pizza=4.8F0.4, audiobooks=3.7F0.6). Average
Participants in the audiobook group were presented baseline salivation was 1.19F0.57 g. No significant
sequential presentations from their most preferred audio- between group differences were observed in any of the
book stimuli using a Sony DiscmanR (Sony, Tokyo, Japan) baseline measures (Table 2). All children in the audio-
during the 1-min intertrial intervals that preceded each of the book condition answered two questions about the story
10 salivary habituation trials. Participants were told to correctly.
attend to the audiobook and they would be asked questions Salivation results presented in Fig. 2 showed a between-
at the conclusion of the experimental session. When the group difference ( F(1,19)=10.54, p=0.004) and a signifi-
habituation trials were completed, children were asked two cant interaction of grouptrial ( F(9,171)=2.34, p=0.016).

Fig. 2. Changes (meanFS.E.M.) in salivation for participants in the continuous audio group and no audio group for Experiment 2.
318 L.H. Epstein et al. / Physiology & Behavior 84 (2005) 313–319
The no audiobook group showed habituation over trials
( F(1,19)=28.08, pb0.001), while the audiobook group
showed no significant changes over trials. Children showed
a non-significant increase in liking ratings from 4.4 to 4.7,
with no differences in the change by groups.
3. Discussion
These experiments replicate the findings that children
habituate to repeated food cues [14], and Experiment 1
extends the observation that allocation of attention disrupts
the development of habituation that has been shown in
adults [12] to children. Children who were in the automatic
search group habituated, as shown by a significant differ-
ence in salivation over the eight trials, while children in the
controlled task group did not show a significant change over
time. Both tasks require a matching response, but differ in
the degree of allocation of attention, which controls for the
influence of the overt behavioral response on habituation.
Not every environmental stimulus will disrupt habituation.
The degree of allocation of attention to an external stimulus
is related to the disruption of the process of habituation
[17,19].
Experiment 2 shows that listening to an audiobook can
disrupt the development of habituation to food cues.
Listening to audiobooks represents a situation that requires
attending to auditory stimuli. Watching television or videos
requires attending to both auditory and visual cues, and thus
would be expected to be more distracting than auditory
stimulation alone. An alternative paradigm would be to
investigate the influences of reading, an activity that
involves only visual cues and is often paired with food
consumption.
The influence of attending to external stimuli on
habituation to food cues may provide insight into
mechanisms by which attending to external stimuli while
eating may increase the amount of energy consumed
during a meal. This may be relevant to understanding why
television watching and obesity are related in children
[36,37], as well as providing a mechanism for under-
standing why people consume more energy when eating
with others than when alone, often called social facilitation
of eating [38,39].
The present study focused on how attentional processes
may influence habituation in normal children. Habituation
may also be a model for disordered eating. For example,
both obese [40] and bulimic [41] participants show differ-
ences in the rate of habituation to repeated food cues when
compared to participants without these disorders. Compared
to non-obese participants, obese participants habituate at a
slower rate [40], and habituating at a slower rate may be
related in part to the slower development of satiety and
greater energy intake in obese compared to non-obese
persons. Bulimia represents a disorder that is characterized
by repeated episodes of binge eating, which may be due to
the failure of bulimics to experience satiation to increased
energy and food volume. Consistent with this hypothesis,
bulimic participants increase responding or sensitize to
repeated food cues [41] which is consistent with binge
eating meals that are part of bulimic psychopathology. It is
not known whether these differences in the rate of
habituation precede the development of these disorders,
and may be etiological, or emerge after obesity or bulimia
are stable.
The design of Experiment 1 contrasted tasks that differed
in their requirement for allocation of attentional resources,
but required a similar response, suggesting that only tasks
that require controlled attention will disrupt the develop-
ment of habituation. Experiment 2 compared groups that
differed in attending to an auditory story or doing no task,
which provides an initial attempt to assess generalization of
controlled laboratory tasks to behaviors similar to those that
children may engage in while eating. However, it is not
possible to know from this study whether listening to any
sounds would have the same effect on habituation, even if
they were familiar or not stimulating. An interesting
experiment would be to vary the familiarity of the audio
stories, and have children listen to familiar or unfamiliar
stories. Since children may have to allocate less attention to
familiar versus unfamiliar stories, it could be predicted that
children assigned to the unfamiliar story condition would
not habituate whereas children assigned to the familiar
condition would habituate.
One limitation of the present studies is that food intake
was not measured. Research in adults has consistently
shown a relationship between the development of habitu-
ation and the termination of eating [6–8], and that the
introduction of a novel food will recover habituated
responding and a recovery of consumatory behaviors [8].
However, research on habituation and eating in children is
in the beginning stages, and the limits of the generalization
from habituation to food cues to eating in children is not
known. Additional research is needed to examine how
relevant findings obtained using the habituation paradigm is
for understanding factors that influence meal termination
and energy intake.
This study focused on the attentional properties of
environmental stimuli, but previous research has shown
that the degree of arousal can influence the strength of
dishabituating stimuli [10]. It is possible that the controlled
attentional task would also increase arousal relative to the
automatic task, and arousal may independently influence
habituation, as well as interacting with the degree of
allocation of attention. Future research examining the
influence of other environmental stimuli such as television
watching on the development of habituation to food is
needed. Studying the relationship between factors that
disrupt the development of habituation and energy intake
in children is another area that needs to be investigated. It
would also be interesting to examine whether there are
individual differences in how children attend to external
 L.H. Epstein et al. / Physiology & Behavior 84 (2005) 313–319
stimuli and how these individual differences may influence
the process of habituation and food intake. Children who
experience a greater disruption of habituation may be those
children who consume more food while attending to other
environmental stimuli, such as watching television.
Acknowledgements
This research was supported by grant HD 44725 awarded
to Dr. Epstein.
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