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Reward immediacy and subjective stress modulate anticipation of primary and secondary rewards in temporarily-abstinent cigarette smokers

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Reward immediacy and subjective stress modulate anticipation of primary and secondary rewards in temporarily-abstinent cigarette smokers

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Content REWARD IMMEDIACY AND SUBJECTIVE STRESS MODULATE ANTICIPATION
OF PRIMARY AND SECONDARY REWARDS IN TEMPORARILY-ABSTINENT
CIGARETTE SMOKERS

by

Louise Debs Cosand

_________________________________________________________

A Dissertation Presented to the
FACULTY OF THE USC GRADUATE SCHOOL
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
DOCTOR OF PHILOSOPHY
(PSYCHOLOGY)

May 2013

Copyright 2013 Louise Debs Cosand
ii
Abstract
The majority of cessation attempts in nicotine-dependent individuals result in relapse. It
is unknown if cessation failure is related to a change in a reward’s motivational value
(incentive salience), a change in inhibitory ability, or is attributable to other factors. To
test for stress effects on incentive salience, and specifically assessing a potential
differential effect on immediate versus delayed reward, neuroimaging and behavioral
data were collected while 17 overnight-abstinent male cigarette smokers engaged in a
reward anticipation task. During the task, which was an adaptation of the monetary
incentive delay paradigm (MID; Knutson, Westdorp, Kaiser, & Hommer, 2000),
participants attempted to win prizes varying in immediacy (now or in seven days) and
type (money or nicotine vapor). When a participant won immediately-available nicotine
vapor, he was allowed draw one puff of nicotine vapor before the subsequent trial
began. Participants were scanned twice; once after stress induction using the cold
pressor task (Lovallo, 1975) and once after a control task. Reward immediacy was
associated with faster reaction times (RT) and stronger blood oxygen level-dependent
(BOLD) signals in the bilateral insula and anterior cingulate cortices. Under greater
stress, however, the immediacy-related anterior cingulate BOLD signal was significantly
lower than in the control condition. Furthermore, slower RTs in the stress condition
suggested that stress decreases incentive salience of anticipated rewards. These
results were unexpected, and may be related to anhedonia associated with acute
withdrawal.

iii
Table of Contents

Abstract ii

Introduction 1

Methods 7
Participants 7
Procedure overview 9
Enrollment Session 9
Experimental Sessions 10
Stress and Cortisol 11
Incentive delay task 12
Neuroimaging data 14
Scan Parameters 14
Data Processing 15
General Linear Model 17
Imaging Contrasts 18
Region of Interest Signal Extraction 19

Results 20
Stress Manipulation 20
Self-report 20
Cortisol 22
Incentive Delay Task: Reaction Times 23
Extracted Signal 24
Whole Brain Analysis 26

Discussion 28
Effect of Delay 31
Effects of Stress 33
Type of reward 35
Conclusion 35

References 38

Appendix A 55

Tables 57
Captions 58

Figures 59
Captions 67

Bibliography 71
1
Stress Reduces Incentive Salience of Money and Nicotine in Temporarily-
Abstinent Cigarette Smokers.
The majority of nicotine-dependent individuals would like to quit
smoking cigarettes (UK ONS, 2011) and the majority of quit attempts fail
(Rose, Salley, Behn, Bates, & Westman, 2010). Even after successfully
quitting, urges to smoke can persist through more than a decade of
abstinence (Fletcher & Doll, 1969). Certain traits, including impulsivity and
particular genetic markers, predict cessation attempt outcomes (Krishnan-
Sarin et al., 2007; Yoon et al., 2007). These traits’ outcomes may be
clinically important, as they may provide a basis for matching therapeutic
approaches to individuals (Marlatt & Donovan, 2005). However, to the
extent that these traits are stable, they are not directly useful as therapeutic
targets. In the case of impulsivity, knowing that an individual’s impulsivity
puts her at risk for relapse is less useful if there is no possible remediation.
Psychophysiological states also influence individual variability in self-
controlled decision making. Variation in an individual’s state may explain
why a particular person is able to successfully abstain from smoking on
some days but unable to abstain on other days. This belief is integrated into
the health care community’s understanding of addiction, illustrated by
cessation guides (WHO, 2001) that identify stress as an obstacle to
successful abstinence. Stress is a psychophysiological state that has been
linked to relapse in individuals attempting to quit smoking (al’Absi, 2006),
2
linked to failures of self-control in restricting cigarette smoking (Shiffman &
Waters, 2004), and also to increased smoking intensity among individuals
not attempting to quit (Pomerleau & Pomerleau, 1991). Empirical evidence
from human laboratory studies, however, has not yet conclusively identified
mechanisms of stress-related success and failure in smoking cessation.
The effects of stress on drug seeking behavior have been studied
extensively in preclinical models. Studies in rodents have shown that stress
triggers reinstatement of drug consumption, including nicotine, after
abstinence (Di Ciano & Everitt, 2004; Shaham, Erb, & Stewart, 2000).
Addictive drugs evoke DA release in the NAcc (Deutch & Cameron, 1992; Di
Chiara et al., 2004), and both within- and between-system modifications
result in increased drug sensitivity and increased vulnerability to stress
(Sorg & Kalivas, 1991; Goeders, 2003; Li & Sinha, 2008; Koob & Volkow,
2010). Stress-induced DA increases, leading to increased motivational value
of the stimulus called ‘incentive salience,’ elicits anticipatory ‘wanting’
(Berridge, Robinson,& Aldridge, 2009) as well as heightened sensitivity to
attention capture by drug-related cues (Hitsman et al., 2008; see Shiffman
& Gwaltney, 2008 for counter-evidence from a non-laboratory, experience-
sampling study). A nicotine-dependent individual in the early stages of a
cessation attempt may have insufficient self-regulatory abilities to cope with
increased incentive salience.
3
Laboratory-based stress induction increases craving for tobacco
cigarettes (Buchmann, et al., 2010; Childs & de Wit, 2010; Dagher et al.,
2009; Perkins & Grobe, 1992) in cigarette smokers. Stress-induced cravings
are higher in participants with variants of DA receptor and DA transporter
alleles (Franklin et al., 2011; Erblich, Lerman, Self, Diaz, & Borbjerg, 2004).
In addition to cravings, stress increases the vigor with which people smoke,
as measured by inhalation intensity (Pomerleau & Promerleau, 1987), total
number of inhalations (Payne , Schare, Levis, & Colletti, 1991; Schacter,
Silverstein, Kozlowski, Herman, & Liebling, 1977a; Schacter, Silverstein, &
Perlick, 1977b), and rate and duration of inhalation (Cherek, 1985; Payne et
at, 1991). Stressed participants also left fewer milligrams of tobacco in the
butts of smoked cigarettes (Payne et al., 1991). These various examples
may all reflect increased incentive salience of cigarettes and dopaminergic
invigoration of consumption behavior.
In an fMRI investigation of responses to smoking cues under stress,
regions sensitive to stress corresponded with increased sensitivity to
smoking cues (based on Smoking Cue – Neutral Cue contrast). When
contrasting smoking cues with neutral cues, without regard to stress, a
pattern of activation corresponding to visual attention was stronger (Dagher
et al., 2009). Responses to drug cues (Yalachkov et al., 2012), including
smoking cues (Brody et al., 2002; McBride et al. 2006), are most frequently
seen in the ACC, OFC, and various other cortical regions. The limbic and
4
striatal subcortical regions reported by Dagher and colleagues (2009) may
have been sensitized by the stress response, explaining their strong MR-
signal response to smoking cues. The stress-related sensitivity to cues,
however, leaves open questions about how a cessation attempt may be
derailed under stress.
If reward processing is enhanced under stress, leading to increased
nicotine consumption or relapse, does that suggest that the rewards
associated with cessation are differently affected by stress? Rewards related
to cessation tend to be delayed health benefits, and evidence of steeper
delayed discounting suggests that smokers are less sensitive to delayed
rewards (Bickel, Yi, Kowal, and Gatchalian, 2008). A delayed reward elicits
lower striatal response than a value matched immediate reward in cigarette
smokers (Luo et al., 2011). Although a heavy smoker might express a
preference for abstinence, he or she may have a blunted ability to
experience anticipatory pleasure for the extremely delayed health benefits.
Damage to the ventromedial prefrontal cortex (vmPFC), a region
sensitive to stress, parallels this deficit in processing delayed rewards.
Damage to the vmPFC causes patients to experience a ‘myopia for the
future’ and exhibit poor decision-making skills (Bechara, 2005) which may
be related to a shorter temporal horizon (lesion: 5.6yr; control:13.0yr) for
both themselves (Fellows & Farah, 2005) and hypothetical others (Goel et al,
1997). In one study that looked specifically at temporal discounting, vmPFC
5
lesion patients exhibited streeper delayed discounting compared with a
control lesion group (Sellitto, Ciaramelli, & di Pellegrino, 2010; however
Fellows and Farah, above, report a null finding with a similar research
design). Stress causes temporary impairment of the prefrontal cortex, also
shifting focus to the present moment (Arnsten, 2009; Sapolsky,2004).
Stress and impulsivity are likely linked via multiple systems.
While direct lab evidence of steeper discounting under stress is sparse,
several studies suggest that humans tend to choose immediate rewards over
delayed rewards when under stress. One study induced stress by guiding
participants through visualization of a narrative about being lost in the
desert, on the brink of death. Participants then performed a delay-
discounting task pitting money against water, and found a steeper
discounting curve after the stress manipulation (Takahashi, Ikeda, &
Hasegawa, 2008). In a series of studies on implicit learning tasks,
participants who were more stressed due to either an experimental
manipulation or life events made more short-sighted decisions (Gray, 1999).
Circulating cortisol is the glucocorticoid that serves as a negative
feedback signal in the HPA-axis stress response, and is often used as a
biomarker of stress. However, cortisol also influences neural systems
independently of stress. Some influences of stress on smoking behavior may
be through direct effects of post-stressor cortisol changes. Oral
administration of 40 mg hydrocortisone in a double-blind, placebo-controlled
6
study increases preference for risky gambles with high potential reward,
relative to the placebo condition (Putman, Antypa, Crysovergi, & van der
Does, 2010). Impulsivity is related to stress responses and DA function
(Cools, 2008), and delay discounting is often used as a proxy for impulsivity.
In healthy adults, L-DOPA, but not placebo, increased dopaminergic
transmission and was associated with steeper discounting of monetary prizes
(Pine, Shiner, Seymour, and Dolan, 2010). Low DA levels are associated
with anhedonia, which is associated with making more far-sighted choices
(Lempert & Pizzagalli, 2010). The implications of these findings are unclear
in the case of stressed cigarette smokers, however, because both smoking
and stress have been linked to anhedonia-like reward processing (Bruijnzeel,
2012; Hommer, Bjork, & Gilman, 2011; Peters et al., 2011).
The present study used a modified monetary incentive delay (MID)
task to assess the effects of delay and stress on incentive salience of money
and nicotine rewards in cigarette smokers. Incentive salience was inferred
by BOLD signal responses during reward anticipation within a network of
brain regions previously shown to be sensitive to the magnitude of incentive
(Luo et al. 2009), and by RTs on the button press-response to win the
rewards. Reward anticipation, compared with the control (no reward)
anticipation period, was hypothesized to decrease RTs and increase BOLD
signals in the ventral striatum, anterior insula (AIns), amygdala, ACC, and
OFC. Further, this effect was expected to be stronger for immediate rewards,
7
compared with delayed rewards. Stress was predicted to increase measures
of incentive salience, and the interaction between stress and immediacy was
expected to correspond with higher reward-related BOLD signals while
anticipating immediate (versus delayed) prizes in the stressed condition
compared with the control condition. Finally, because nicotine interacts with
the dopaminergic system, anticipation of nicotine was expected to elicit` a
stronger stress-related response than money.
Methods
Participants
Male volunteers who were regular smokers but otherwise healthy were
recruited from advertisements on a popular classifieds website
(www.craigslist.org/losangeles). A brief phone screening identified potential
participants based on their smoking history, the absence of psychiatric
diagnoses, the absence of psychoactive drug use, and their ability to
undergo MRI procedures. A total of 22 participants met the inclusion criteria
to complete the experimental sessions of the study and 17 of these 22
participants completed the series of four experimental sessions. The
inclusion criteria defined a “cigarette smoker” as a person who currently
smokes 15 or more cigarettes per day for a minimum of two years. The
inclusion criteria also required each participant to have a level of expired
carbon monoxide (CO) greater than 15ppm, a score of four (out of 6) or
higher on the Fägerström Test for Nicotine Dependence (Heatherton,
8
Kozlowski, et al. 1991), and a favorable response to the smoke produced by
an electronic cigarette. Of those participants who qualified for the study but
did not complete all of the sessions, one participant reported being too busy,
one participant developed a dislike for the electronic cigarette, and three
participants were unable to follow task instructions during the experimental
sessions. The final sample with complete data included 17 male cigarette
smokers who were otherwise healthy with an age range between 24 and 55
years old (36.9±10.1 years old, mean ± standard deviation). Study
enrollment was limited to males because the study required precise
scheduling and measured stress responses. Female hormonal cycles
influence stress responses, which is sometimes controlled for by scheduling
based on the woman’s cycle (Ossewaarde et al., 2010). The delay
discounting-related requirement of seven days between an MRI session and
its linked behavioral interfered with scheduling hormone-matched sessions.
Further demographic information and a characterization of the smoking
behaviors of each participant are presented in Table 1.
All participants gave informed consent to participate in the study
before responding to the screening questionnaires during the Enrollment
session. Participants received financial compensation for their time and were
reimbursed for their parking expenses. A financial bonus was provided as an
incentive to comply with the abstinence instructions and as a prize in the
9
reward anticipation task. All procedures were approved by the Institutional
Review Board of the University of Southern California.
Procedure overview
Participants engaged in a reward anticipation task in an MRI scanner
on two separate occasions. A 2x2 within-subject experimental design was
used to measure the effects of Condition (Stress, Control) and Immediacy
(Now, Week) on the BOLD signal during reward anticipation. The Condition
factor was manipulated between sessions and counterbalanced to reduce
order effects. The Immediacy factor was manipulated within each session,
such that each scanning session included both trials with immediate
outcomes and trials that were rewarded by prizes that could not be collected
for seven days. Consequently, each MRI session was scheduled with a
corresponding laboratory visit exactly one week later. During this
subsequent visit, participants completed a battery of behavioral tasks and
received their winnings from the previous week's MRI session. In total, the
study was comprised of five laboratory visits: an Enrollment session to
determine eligibility, the Stress MRI-Behavioral session pair, and the Control
MRI-Behavioral session pair. The Behavioral sessions will only be discussed
to the extent that they are relevant to the interpretation of the MRI data.
Enrollment Session
The enrollment session had a three-fold purpose: to determine study
eligibility, to administer a battery of self-report measures, and to familiarize
10
the participants with the experimental tasks. Participants were instructed to
smoke ad libitum the day of the enrollment session to ensure that each
participant arrived to the laboratory in a nicotine-satiated state. Immediately
following the informed consent process, the experimenter measured the
level of expired CO in each participant and administered the Urge to Smoke
and Shiffman-Jarvik questionnaires. The participant was then given an
electronic cigarette to smoke ad libitum for the duration of the session.
Participants responded to a series of questionnaires to determine study
eligibility, smoking behavior, and individual traits. Participants that were
likely to meet the criteria for the MRI sessions were trained on the scanner
task and practiced minimizing their head movements while smoking the
electronic cigarette through several feet of narrow polyurethane tubing.
Participants rated their enjoyment of the electronic cigarette after
approximately 45 minutes of ad libitum use.
Experimental Sessions
All four experimental sessions required that participants abstain from
nicotine for 8 to 12 hours preceding the visit to increase the incentive
salience of the electronic cigarette during the MRI scans. This same
abstinence requirement was implemented during the behavior-only sessions
to match the immediate and delayed smoke in every way but immediacy. All
sessions were administered in the morning before noon to improve
compliance to this abstinence requirement. To diminish the influence of the
11
cortisol awakening response (CAR; Fries, Dettenborn & Kirschbaum, 2009)
on salivary cortisol measures, participants were asked to awaken at least
two hours before the first saliva sample and their wake time was confirmed
via telephone. Participants were also asked to limit their caffeine intake to
their typical morning consumption levels and to avoid exercise in the hour
prior to arriving to the laboratory.
Participants arrived to the laboratory one hour prior to the MRI scan.
Upon arrival to the laboratory, compliance to the abstinence requirement
was verified by both the CO in an expired breath and self-report. Participants
were asked to rate their craving severity (Urge to Smoke, Shiffman-Jarvik)
and baseline levels of psychological stress (Daily Stress Inventory).
Participants also rehearsed the scanner task. Participants were given an
eight-ounce bottle of water to drink and asked to relax for 20 minutes prior
to the baseline saliva sample.
Stress and Cortisol
In the MRI center, the participant was prepared for scanning and the
baseline saliva sample was collected using a sublingual sorbette. Then, the
experimenter assumed an unfriendly demeanor and instructed the
participant to look straight ahead and submerge his hand in a pitcher of
water for 3 minutes. The experimenter held a notebook, watched a
stopwatch, and verbally notified the participant after one minute had elapsed
and again when 30 seconds remained. In the stress condition, the water was
12
filled with ice cubes to a temperature between 0 and 3°C. In the control
condition, the water temperature was between 27 and 30°C. The participants
responded to a brief questionnaire about the stressor (Water Task
Questionnaire) and then were positioned in the scanner with a response
button in the right hand and a tube connected to the electronic cigarette in
the left hand. The participants took one practice puff of the electronic
cigarette before the scan started. A saliva sample was collected 23 min post-
stressor while the participant was positioned in the scanner bore. The
scanning session included two experimental scans to measure the BOLD
signal during the incentive delay task (described below), beginning 25 min
and 40 min post-stressor, respectively. Standard protocol scans were also
administered and included an arterial spin labeling resting state scan and
one or more structural scans.
Incentive delay task
In the scanner the participants performed an incentive delay task (see
Figure 1) that was inspired by the Monetary Incentive Delay task (Knutson,
Westdorp, Kaiser, & Hommer, 2000). Each trial began with a display of an
image that informed the participant about the prize that was at stake for
that trial. The prizes varied in type (smoke, money) and immediacy (now,
week) for a combination for four trial types: SmokeNow, MoneyNow,
SmokeWeek, and MoneyWeek. A fifth trial type, Null, displayed a symbol
which indicated that no prize was available on the current trial to serve as a
13
motor control. After the prize was shown to the participant, the prize image
disappeared and was replaced by a target (“+”). The participant believed
that he could win the available prize by pressing the response button as
quickly as possible when the target appeared. Once a response was
recorded, a message notified the participant if he was “fast enough” or “too
slow” to win that prize. Following this message, the screen became white for
4.5 to 5.5 s before the start of the next trial for most trials. However, in
cases in which the prize was “SmokeNow” and the participant was “fast
enough,” the participant was given 4.5 to 5.5s to take a puff of the
electronic cigarette before the start of the next trial. Each run of the ID task
included 15 trials of each trial type for a total of 75 trials. Within each trial
type, the program was rigged to result in eight wins and seven losses;
however, a trial that was rigged as a win would be counted as a loss if the
response button was not pressed within 1000 ms of the appearance of the
target. Each winning money trial added $0.50 USD to the bonus pay, which
the participant received either immediately following the scan or at the
behavior-only session that was scheduled for the following week. Smoke was
administered during both the scan and the behavior-only session. During the
behavior-only session, an audio recording chimed on a schedule that was
yolked to the timing of the SmokeWeek wins from the participant’s MRI
session. The participant was allowed to take a puff after each chime.
14
At the end of the scan, the participants were asked to rate their
current craving level (Urge to smoke) and their enjoyment of the electronic
cigarette (Liking Questionnaire). The participants then received their bonus
money from the experimental task and confirmed their availability for the
linked behavior-only session. The MRI session data was still valid even if the
participant had to reschedule the behavior-only session, because at the time
the BOLD signal was measured the participant believed that he would
receive the prize in a week. At the end of the scan, saliva samples were
frozen at -20°C until processing. The processing of the samples was
outsourced to Salimetrics (State College, PA).
Neuroimaging data
Scan Parameters
The imaging data were collected using a 3T Siemens MAGNETOM
Tim/Trio scanner with a 12-channel head coil that is located in the Dana and
David Dornsife Cognitive Neuroscience Imaging Center at the University of
Southern California.
A structural scan was imaged for each participant using a T1-weighted
3D MPRAGE (magnetization prepared rapid gradient echo) sequence
(TI=900 ms, TR=1950 ms, TE=2.26 ms, flip angle=90°). Functional scans
employed an echo planar imaging sequence (FOV=192, matrix=64×64, 3mm
slice thickness, TR=2000ms, TE=25ms, flip angle=90°) with a prospective
acquisition correction that was intended to reduce the effects of head motion
15
on the data slice coverage. Thirty-two 3-mm thick axial slices were used to
cover the whole cerebral cortex without a gap; however, the brains from
several participants exceeded the dimensions of the coverage area. Slices
were positioned to include both frontal and striatal regions, which resulted in
an incomplete coverage of the ventral posterior regions. The images of the
coverage maps appear in Appendices A1 and A2.
Data Processing
The first two volumes of each functional run served as a period of
signal stabilization and were subsequently discarded from the analysis.
Dicom files that were produced by the scanner were converted to nifti format
with dcm2nni (Rorden, 2007, www.idoimaging.com) and processed using
FMIRB’s Software Library (FSL; www.fMRIb.ox.ac.uk/fsl; Jenkinson,
Beckmann, Behrens, Woolrich & Smith, 2012; Smith et al., 2004; Woolrich
et al., 2009). Although the Siemens imaging system provides an option for
motion-corrected data, the non-motion corrected raw files provided a
greater control over the corrections that were applied to the data. A custom
MATLAB script was used to extract the parameters related to motion and
prospective acquisition correction that were used in the eventual model. The
data preprocessing steps that were performed included skull stripping (BET;
Smith, 2002), spatial smoothing with a 5-mm Gaussian kernel, high pass
filtering at 100 s, and an independent component analysis (MELODIC).
16
The study required that the participant inhale the electronic cigarette
after each winning SmokeNow trial, which constituted 50% of all SmokeNow
trials. Movements larger than 1.5 mm were observed in 38% of the runs and
larger than 3 mm in over 20% of the runs. These head motions occurred
mainly after winning SmokeNow trials and were presumed to be associated
with inhalation. Of the components that were identified by MELODIC, those
components that resembled structured noise (Lighthall et al 2012, Kelly et
al. 2010, Tohka et al. 2008) were removed using visual inspection in
conjunction with a trainable MATLAB script (Aron et al., 2006, Tohka et al.
2008). These removal decisions were made conservatively because of the
correlation between noise and SmokeNow trials. A second approach to
remove noise from the data was to make masks of regions where the signal
would not be expected to co-vary with the condition and extract time
courses to use as nuisance regressors. One of these masks extracted a
signal from the white matter regions and a second mask extracted a signal
from a ring in the empty space around the skull. In a final step to measure
meaningful signal changes related to the anticipation of immediate nicotine,
SmokeNow Win trials were modeled separately from SmokeNow Loss trials.
The reason for this separation is that SmokeNow trials that were
subsequently followed by a loss did not contain the high level of artifact that
was presumed to be associated with inhalation in the SmokeNow Win trials.
Therefore, these trials may allow for a better assessment of the anticipation-
17
related signal that is expected to be recruited by the SmokeNow trials.
Consequently, the general linear model included separate predictors for
SmokeNow trials in which the participant experienced a loss (SmokeNow_L)
compared with a win (SmokeNow_W). Unless otherwise specified, the
anticipation contrasts that involved SmokeNow trials excluded SmokeNow
trials that were followed by smoking (i.e., excluded winning SmokeNow
outcomes). SmokeNow_L was used in all contrasts.
General Linear Model
Ten event-related explanatory variables, which were convolved with a
double-gamma hemodynamic response function and temporal derivatives,
were used to model the BOLD signal. Six regressors were used to model the
anticipation periods for the SmokeNow_L, MoneyNow, MoneyWeek, and Null
trials. The SmokeNow_W trials were included in the model as a separate
explanatory variable and were not used in any contrasts due to noise. The
remaining four regressors modeled the response period, the “too slow”
notification, the “fast enough” notification, and the time period after the
SmokeNow_W trials during which the participant was inhaling the nicotine
vapor. Unmodeled time served as an implicit baseline.
Several types of confound variables were included in the models. Six
motion parameters that were extracted from the dicom files by a MATLAB
script were included in the model as confound variables. Two more confound
18
variables, the previously mentioned extractions from the ring and the white
matter, were also added to the model.
Imaging Contrasts
Within-run contrasts
Contrasts within a run were produced by comparing the response to
each individual prize against the Null, which resulted in four separate
contrast parameter estimate maps (SmN
-N
, MoN
-N
, SmW
-N
, and MoW
-N

contrasts). The responses to the two immediate prizes (SmokeNow_L and
MoneyNow) were also contrasted with the responses to the two delayed
prizes (SmokeWeek and MoneyWeek) within each run to produce one
contrast parameter estimate map (Immediacy contrast).
Within-session contrasts
Because each session involved two runs, each participant’s
corresponding contrasts were averaged using a fixed-effects analysis, which
forced the variance of the random effects to equal zero in FLAME (FMRIB's
Local Analysis of Mixed Effects; Beckmann, Jenkinson, & Smith, 2003). The
resulting contrast parameter estimate maps were labeled by the condition of
the session, Stress or Control. These parameter estimate maps were later
used in mixed-effects models that contrasted Stress and Control.
Within-participant contrasts
To evaluate the BOLD responses that were associated with reward
anticipation, all Prize versus Null contrasts were collapsed within each
19
participant, which forced the variance of random effects to equal zero and
produced statistical maps for higher-level analyses. The Immediacy
contrasts were similarly combined to produce Z-statistic maps in the MNI
standard space. Unlike the within-session modeling, this approach combined
the data from both the Stress and Control conditions.
Between-participant contrasts
Statistical maps from the second-level analyses (Z-statistic maps in
the MNI standard space) served as inputs for group analyses using the
mixed-effects models, FLAME stage 1 and stage 2 (Beckmann, 2003;
Woolrich; 2004). FLAME’s robust outlier detection function identified and de-
weighted aberrant values. The analyses produced activation maps that
consisted of all voxels with signal differences that exceeded both a Z = 2.3
threshold and cluster-extent thresholding. The cluster-extent thresholding
controlled for a family-wise error across the entire brain at p < 0.05.
Region of Interest Signal Extraction.
A signal was extracted from regions that are broadly associated with
reward anticipation to both reduce multiple comparisons and to relate these
data to existing studies. A map of the activations that were related to the
reward anticipation was used as a mask to extract this signal. This map was
generated on www.neurosynth.org from a forward inference meta-analysis
of 78 “anticipation” studies. Many of these studies employed the MID task or
some derivative of this task. The size of the map was 10,956 voxels in MNI
20
standard space and included the bilateral ventral striatum, the dorsal
striatum, and the insula. The mask is shown in Appendix A3. The FSL
function fslmaths was used to compute the mean of all of the non-zero
voxels within the mask for the contrast parameter estimate maps that were
generated for the individual runs.
The extracted data were subjected to a 2x2x2 repeated measures
ANOVA in SPSS. The ANOVA evaluated three factors: Immediacy (Now,
Week), Type (Smoke, Money), and Condition (Control, Stress).
Results
Stress Manipulation
Self-report
Self-reported overall stress levels (Overall, how stressed or anxious do
you feel right now?; 1-10) were collected approximately 30 minutes before
the cold pressor task and again immediately after the task. Eleven of 17
participants reported a higher stress level after performing the cold pressor
task than they had reported initially, while the remaining six participants
reported the same levels before and after. After the warm water task
(control condition), six participants reported a slightly increased stress level
(median increase of one point), eight participants reported the same stress
level, and three reported a decreased level (median decrease of one point).
Pre-task ratings and post-task ratings (Fig. 2a) were compared with a 2×2
(time × stress) repeated-measures ANOVA. There was a significant effect of
21
stress [F (16) = 9.328, p = 0.008], with stress ratings being higher overall
in the cold pressor group. The effect of time was also significant [F (16) =
5.463, p = 0.033]. The interaction between stress and time, which serves as
a manipulation check, did not show that the stress manipulation had a
different effect on stress levels than did the control task [F (16) = 1.423, p
= 0.250]. A post-hoc, two-tailed, paired-samples t-test compared the pre-
manipulation stress ratings to determine if they were different, and the
baseline stress levels on the days of participants’ stress manipulation were
higher [t(16) = 2.554, p = 0.021]. The self-reported stress scores after the
manipulation remained significantly higher in the stressed condition than in
the control condition [t(16) = 2.675, p = 0.017]. The lack of interaction
means that the cold pressor cannot be credited with increasing the scores.
Nevertheless, immediately before the imaging data were collected,
participants in the stressed condition reported significantly higher levels of
stress than participants in the control condition. The baseline stress
differences are likely random, because the stress manipulation was within-
subject and participants were unaware that one of the scan sessions would
definitely involve stress manipulation.
Self-reported stress levels also provided data that are important for
interpreting the utility of the control condition. The study was designed to
compare reward anticipation under stress in comparison to reward
anticipation under normal conditions; however, our data suggest that the
22
control condition was actually a mild stress condition. Withdrawal can elicit a
stress response, and participants were in withdrawal during both the stress
scan and control scan. Participants were, however, allowed to smoke ad
libitum before their baseline screening session at the start of the study. The
self-reported stress level from this non-abstinent enrollment session was
used as a point of comparison to test for effects of overnight abstinence on
subjective stress. The baseline stress score was compared with the stress
rating that was collected immediately before the control condition scan. A
two-tailed, paired-samples, t-test showed that the participants were less
stressed when satiated than in when in withdrawal [t(16) = 2.207, p =
0.042]. Accordingly, the experimental conditions should be considered stress
and control rather than stress and non-stress.
Cortisol
Salivary cortisol levels collected after the cold pressor task showed a
modest increase from cortisol levels just prior to the cold pressor task (Fig.
2b). Not all participants provided sufficient saliva for analysis, and one
extreme outlier (value – 3×SD > nearest value) was removed from the
stress condition, so the numbers reported here are based on reduced sample
sizes (n
stress
= 15, n
control
= 14). The interaction in the available samples
between condition and time was not significant [F(1,12) = 1.01, p = 0.340].
However, the pattern of cortisol level changes was consistent with the
anticipated elevating effect of the manipulation on salivary cortisol
23
measurements. In particular, during the stress condition, among the 15
participants with usable pre- and post- assays, there was a mean increase in
salivary cortisol of 0.082 + 0.15 µg/dL, which was marginally significant by
paired t-test [t(14) = 2.09, p = 0.055]. For the control condition, however,
pre- and post- cortisol levels remained similar [difference score, 0.002 ±
0.08 µg/dL; t(14) = .09, p = 0.930].
Incentive Delay Task: Reaction Times
Prior to analyzing reaction times (RTs), trials in which the RT was less than
100 ms were removed, because this indicated that the response was likely
initiated prior to the presentation of the target. Based on this criterion, 55 of
5,395 trials were censored from analyses. Additionally, variance related to
practice effects was removed by fitting the log of trial number to the RT for
each participant. The residuals from these regressions (one regression model
for each participant) were then standardized as participant-specific z-scores.
For each condition of interest, the Z-score median was then calculated for
each participant. As a manipulation check to establish whether prizes during
anticipation affected RT, we first carried out a paired t-test comparing the RT
during Any Prize trials with RT during No Prize trials (in each case, collapsing
across Condition, and in the case of Any Prize, collapsing also across Reward
and Delay). These data were separated by condition (Stress vs. No Stress)
and were subjected to repeated-measures ANOVA. The RT was significantly
faster for Prize relative to No Prize [F(1,16)) = 23.55, p < 0.001].
24
Responses were also significantly slower in the Stress condition [F(1,16) =
5.82, p = 0.030]. There was no significant interaction between Prize vs. No
Prize and Stress condition [F(1,16) = .406, p = 0.533].
To assess whether the observed Stress effect on RT interacted with the
type of Prize or its Immediacy (Now vs. Next Week), we carried out
repeated-measures ANOVA with Stress, Reward (smoke vs. money), and
Immediacy as independent variables (excluding the No Prize condition
because the Immediacy variable was not applicable). Immediacy was
associated with significantly shorter RTs [F(1,16) = 19.82, p = 0.001]
(Figure 3). There was a trend towards slower responses in the Stress
condition [F(1,16) = 3.69, p = 0.070]. No main effect of Prize was observed
[F(1,16) = 2.4, p = 0.140]. No interactions between the three independent
variables were significant [Stress × Prize: F(1,16) = 1.14, p = 0.300; Stress
× Immediacy: F(1,16) = .41, p = 0.530; Prize × Immediacy: F(1,16) =
1.49, p = 0.240; Stress × Prize × Immediacy: F(1,16) = 2.16, p = 0.160].
Extracted Signal
To test for relationships between all independent factors, β-values
were extracted from the “anticipation” map produced by neurosynth.org’s
meta-analytic software. A 2×2×2 repeated-measures ANOVA tested for
relationships between extracted β-values from each condition, prize delay,
and prize type (Figure 4). A primary hypothesis of the study, that stress
devalues delayed rewards, was rejected. The interaction of Stress and
25
Immediacy was not significant [F(1,16) = 0.501, p = 0.489, ηp
2
= 0.030],
reflecting similar differences between immediate prizes and delayed prizes in
both conditions. We predicted a steep drop in anticipation-related signal for
delayed prizes under stress. Signal during anticipation of delayed prizes was
roughly half the strength of the signal associated with immediate prizes in
the both the stress condition (M
Now
= 3.920, SE = 1.071; M
Week
= 1.982, SE
= 0.895) and control condition (M
Now
= 6.175, SE = 1.455; M
Week
= 3.236,
SE = 1.171). A second prediction of the study was that stress would
enhance incentive salience of reward, measurable as stronger BOLD signal
during reward anticipation. Consistent with the RT scores reported above,
this prediction was not supported by the data. We observed weaker
anticipation-related signal under stress (M = 2.951, SE = 0.845) than in the
control condition (M = 4.705, SE = 1.215), although this pattern is not
sufficiently strong to conclude that stress dampened reward responsivity
[F(1,15) = 1.765, p = 0.203, η
p
2
= 0.099]. The interaction between stress
and prize type provides another data pattern that is descriptively interesting
but not statistically significant [F(1,15) = 1.858, p = 0.192, ηp
2
= 0.104].
Between stress and control conditions, the signal means associated with
money anticipation are similar (M
Stress
= 5.323, SE = 1.161; M
Control
= 5.946,
SE = 1.281) while anticipation of nicotine appears to decrease MR-signal
under stress relative to control (M
Stress
= .578, SE = 1.277; M
Control
= 3.465,
SE = 1.503). The mean activations from a three-way interaction between
26
stress, immediacy, and type [F(1,15) = .000, p = 0.992, ηp
2
= 0.0] do not
follow a pattern that clarifies the potential meaningfulness of the non-
significant stress-related means reported above.
The expectation that immediate rewards would be associated with
stronger signal was confirmed by the data [F(1,15) = 10.696, p = 0.005, η
p
2

0.401]. Immediate prizes elicited higher activity in anticipation-related areas
than prizes delayed by 1 week (M
Now
= 5.047, SE = 1.033; M
Week
= 2.609,
SE = 0.728). The type of prize was also significantly related to β-values
[F(1,15) = 7.227, p = 0.016, η
p
2
= 0.311], reflecting a stronger signal while
anticipating money prizes (M = 5.635, SE = 0.963) than smoke prizes (M =
2.022, SE = 1.138). There is no interaction between immediacy and type of
prize [F(1,15) = 0.708, p = 0.412, η
p
2
0.042].
Whole Brain Analysis
Response to reward
The first analysis tested whether participants exhibited BOLD signal
patterns typical of reward anticipation tasks, by combining all types of Prize-
NoPrize contrasts. Similar to other studies using reward anticipation tasks,
anticipation was associated with strong bilateral BOLD signals in the AIns,
mediodorsal thalamic nuclei, and striatal structures (Zmax = 4.65, -10, 4, -
2). Signal also increased in the anterior, posterior (Zmax = 3.58, -2, -38,
40), and paracingulate gyri. Anticipated reward increased left premotor and
motor cortex signals (Zmax= 5.22, -44,0,32), likely indicating more
27
recruitment of activity associated with preparation to press the response
button. Further signal differences trials are detailed in Figure 5.
Stress and reward
Stress effects on reward anticipation (Figure 6) indicated stronger
BOLD signals in the right primary somatosensory cortex (Zmax = 4.0), and
a cluster covering the lingual gyrus and posterior-most thalamus (Zmax =
3.59). A Stress × Reward interaction was observed in the anterior cingulate
and paracingulate cortices. Counter to predictions, the signal differential for
the Reward vs. No Reward contrast was lower in these regions during the
stressed condition than with the control condition (Zmax 3.78 and 3.95,
respectively).
Reward immediacy
Contrasting immediate with delayed rewards identified the limbic
cortices as sensitive to the immediacy of prizes. Stronger signals were
measured bilaterally in the posterior OFC, AIns, and ACC (see Table 7).
Activation also increased along the right angular and supramarginal gyri
(Zmax = 3.69), but a drop was observed in the left occipital pole (Zmax =
5.12).
Stress and immediacy
First level contrasts between immediate prizes and delayed prizes from
the stress condition were compared with matched contrast images from the
control condition using a paired-sample t-test. The Immediacy effect
28
interacted with stress, but not in the predicted direction. Stress was
hypothesized to enhance the immediacy effect relative to the control
condition, but the reverse relationship was observed (Figure 7). Activity in
the ACC during anticipation of immediate rewards (minus delayed rewards)
was lower in the stress condition than in the control condition (Zmax= 3.4, p
= 0.004, 374 voxels, -4,12,22).
Discussion
The present study used within-subject fMRI to examine the stress
effects on reward anticipation in cigarette-addicted individuals. Because of
animal literature discussed above that suggests stress induces increases in
striatal DA release (Thierry, Tassin, Blanc, & Glowinski, 1976), we
hypothesized that abstinent smokers would exhibit stress-related increases
in striatal BOLD signals during reward anticipation. Further, this effect was
expected to be stronger in relation to anticipating immediate rewards
compared with delayed rewards (received 7 days later). Although nicotine
vapor and money prizes were not value-matched, the stress and immediacy
effects were expected to be more dramatic for nicotine vapor because it is a
primary reward.
Basic comparisons, such as BOLD signal and reaction time differences
between the Prize versus Null conditions, yielded several results consistent
with those found in previous studies. Reward anticipation (all prizes versus
Null) was associated with a pattern of BOLD signal differences that were
29
consistent with those observed in similar studies using both primary and
secondary rewards (Clithero et al., 2011; Valentin & O’Doherty, 2009).
Bilateral striatum, thalamus, AIns, and ACC signals were stronger during
reward anticipation, which is consistent with their purported role in incentive
salience and reward (Bechara, 2005). The similarities in findings between
previously published MID studies and the present study’s Reward contrast
result serve as a simple manipulation check to confirm that data collection
and analysis were generally effective.
Manipulation checks were unclear regarding the effectiveness of the
cold pressor task as a stressor, but both measures of stress (cortisol, self-
report) were higher on the stress day (compared with the control day) at the
time of neuroimaging data collection. By chance, the participants reported
higher stress on the stress day (relative to control day) prior to the cold
pressor task. While this obfuscates the effectiveness of the manipulation on
subjective stress, the imaging data can still be interpreted because the
participants were in the stress state to which they had been randomly
assigned. However, it should be noted that caution is warranted because the
absence of a condition by time (i.e., pre- post-Cold Pressor Task) interaction
implies the absence of full experimental control over our central independent
variable.
Salivary cortisol was measured as a biomarker of stress; however, the
results were inconclusive. Paired t-tests comparing pre- and post-
30
manipulation levels (for participants with useable data) indicated that there
was a marginally significant increase for participants in the stress group.
There was no difference between the pre- and post-manipulation cortisol
levels in the control group. However, there was no evidence of an interaction
between condition and time (pre vs. post), and unlike the self-report stress
ratings, the cortisol levels post-cold pressor task were not higher during the
stress session, relative to the control session. The absence of a cortisol
response, even when self-reported stress was higher, was not surprising.
Previous studies have reported atypical HPA-axis profiles in smokers, such
as high baseline cortisol levels with decreased stress reactivity (al’Absi,
Wittmers, Erickson, Hatsukami & Crouse, 2003; Childs & de Wit, 2009).
Nicotine directly stimulates the HPA-axis, even in the absence of subjective
stress, leading to allostatic adaptations to cope with repeated nicotine
challenges (Bruijnzeel, 2012).
The AIns and ACC play a role in estimating the emotional impact of an
anticipated reward (Garvan, 2010). The AIns is associated with
interoception, and projections from the region synapse in the ACC for
evaluating the information coded in the signal (Craig, 2010). Both structures
have been repeatedly linked to drug craving in experimental paradigms
(Yalachkov et al, 2012), and lesion damage to the right AIns leads to
spontaneous cessation in cigarette smokers (Naqvi & Bechara, 2007).
Comments by these lesion patients suggest that cigarettes are no longer
31
appealing, implicating insular involvement in evaluating the reward potential
of a stimulus (Naqvi & Bechara, 2007; Verdejo-Garcia, 2009). Consistent
with existing literature on reward anticipation, we found that BOLD signals
were stronger in limbic cortices during reward anticipation (anticipating
either money or nicotine) as compared with Null trials.
Additionally ,we found that attentional and sensory systems were also
engaged during reward anticipation. Frontal and parietal cortical regions
associated with attentional control were strongly positive during reward
anticipation as compared with Null trials, while the visual cortex and
somatosensory regions were relatively negative.
Effect of Delay
Our finding that reaction times were faster for immediate prizes and
for Prize versus Null groups is consistent with existing literature. Previous
studies have also found the same BOLD data pattern and negative
correlations between reaction times and signal differences in similar groups
as those studied here (Luo et al., 2009).
The basal ganglia play a role in the initiation of movement, and
regions associated with motivation and reward evaluation are contiguous
with the motor systems used during approach behavior/drug-seeking.
Motivation values driving the motor system are related to the limbic system
(Balleine & Killcross, 2006). Recent findings on reaction time indices of
motivation showed that enhanced speed was related to AIns BOLD signal
32
during prize anticipation and that this effect was mediated by NAcc BOLD
signal (Clithero et al., 2011). The present study found anticipation-related
signal differences in the dorsal striatum, dorsomedial thalamus, and left
premotor cortices, reported above, which likely reflect preparation of the
motor pathways for the impending right-handed button press response.
Expectedly, immediate prizes, relative to prizes delayed by 1 week,
corresponded with higher signal in reward-responsive regions. Previous
studies have repeatedly found that lower amounts of money elicit lower
reward-related signals and that delayed rewards are perceived as lower in
value than the same immediate reward (Ballard & Knutson, 2009). Because
all monetary prizes in this study were $0.50, immediate-prize signals should
reflect higher incentive salience. Indeed, immediate rewards corresponded
with faster reaction times and stronger BOLD in the network of brain regions
previously linked to reward anticipation and delay (Luo et al., 2009).
Unexpectedly absent from that contrast, however, was an immediacy-related
cluster in the striatum. Incentive-delay paradigms consistently elicit signal
changes in the striatum, which mediates the translation of a reward’s
incentive salience into an approach behavior (Wise, 2009). Examination of a
non-cluster corrected z-stat result image from the Null group (thresholded at
z = 2.3) did, however, suggest greater signal within the striatum during
immediate (relative to delayed) reward anticipation. Moreover, the extracted
signal from the “anticipation regions” mask, which included the bilateral
33
striatum, confirmed that there was a strong effect of delay on the BOLD
signal response. Presumably, immediately available rewards increase the
reward’s incentive salience and prime the system to approach behaviors.
Effects of Stress
A key hypothesis of this study was that stress would sensitize the striatum
to reward, increasing behavioral and signal correlates of incentive salience.
Stress-elicited DA elevations in the striatum were expected to prime the
basal ganglia to activate more readily to earn a reward via button-press.
This led to a prediction of faster responses on rewarded trials under stress,
due to increased incentive salience of the rewards Contrary to expectations,
RTs were actually slower under stress, and the primary effect of stress was a
decrease in BOLD signals during reward anticipation.
The current understanding of dopamine, stress and reward was primarily
established in rodents. While human molecular neuroimaging studies have
been used to measure striatal dopamine in humans (Pruessner, Champagne,
Meaney, & Dagher, 2004; Wang et al., 2005), the relations between stress,
striatal dopamine, and reward processing are more nuanced (Egerton et al.,
2009). Neuroimaging studies have linked drug reward processing and stress
(Sinha et al., 2005) and with pharmacologically induced dopamine increases
(Volkow et al, 2008). Many studies, however, report less clear relations (eg.
Dagher et al., 2009, Montgomery, Mehta, and Grasby, 2006). One study
reported no change in striatal dopamine levels in response to inhaled
34
nicotine (Montgomery, Lingford-Hughes, Egerton, Nutt, & Grasby, 2007),
serving as a reminder that striatal dopamine may be less tightly linked to
reward-seeking behavior in humans.
In hindsight, the basis for predictions regarding stress effects on
incentive salience is not straightforward, given the context of withdrawal
from smoking. Chronically, nicotine exposure does appear to cause
anhedonic behavior in animals (Cryan, Bruijnzeel, Skjei, & Markou, 2003;
Iniguez et al., 2008), an effect likely mediated by drug-induced adaptations
within mesocorticolimbic dopamine circuitry (D’Souza & Markou, 2010;
Paterson & Markou, 2007). The effect of withdrawal after chronic nicotine
exposure can include pronounced motivational disturbances, especially
anhedonia. Abstinence from nicotine increases the availability of unbound a
4b2 nAChRs within the ventral tegmental area (Staley et al., 2006) and is
associated with an increase in the threshold for intracranial self-stimulation
(Koob, Sanna, & Bloom, 1998) indicating refractoriness to reward (Epping-
Jordan, Watkins, Koob, & Markou, 1998). Presuming then that smokers in
withdrawal exhibit reduced reward-related signaling, the critical question
with regard to our study, is how a mild stressor effects that signaling,
approximately 20-30 minutes after its occurrence. Particularly given that
nicotine withdrawal symptoms are elevated after a stressor (Paolini & De
Biasi, 2011), reduced reward sensitivity subsequent to our stressor may be
more consistent with prior findings than we had previously conceived.
35
Type of reward
Money and stress were not value matched, precluding a direct
comparison, but this study examined discounting within types of rewards.
Because smoke is a primary reward (it is consumed upon delivery) it was
expected to be more closely related to reward anticipation. There was no
support for this prediction, and indeed the pattern of data was in the
opposite direction.
The incentive salience of the Smoke Now prize may have decreased
throughout the scanning session due to increasing nicotinic receptor
occupancy. Heavy smokers who performed a similar task, but whom
received cigarette rewards after exiting the scanner, responded similarly to
money and smoke prizes (Bühler et al., 2010). The use of real cigarettes
may also have influenced the incentive salience of smoke prizes as the
electronic cigarette lacks important aspects of smoking’s sensorimotor
experience (Rose, 2006).
Conclusion
The study, overall, provided surprising results relating to stress and
nicotine addiction. Whereas stress was expected to enhance incentive
salience and motivate reward seeking, stress seems to dampen that
response. This may be an effect particular to nicotine-dependant individuals,
as prolonged exposure to nicotine and tobacco may alter reward and stress
sensitivity. This effect was not tested in females, so there is no basis to say
36
that this occurs in all cigarette smokers. An important next step would be to
develop a version of this study to test stress effects on female cigarette
smokers because motivational systems in men and women respond
differently under stress (Lighthall et al., 2009).
The dampened response sensitivity observed in the present study is
somewhat consistent with the anhedonia account of addiction. One
inconsistence, however, is that the model of anhedonia suggests that the
individual is hyperresponsive to drug rewards and hyporesponsive to non-
drug rewards (Bjork, Smith, & Hommer, 2008). The data presented in this
report, however, find that participants seem more motivated to obtain
money relative to nicotine. Shared mechanisms may underlie devaluation of
both types of prizes, and dampened responsivity may be influenced by
multiple systems (eg HPA-axis, nicotinic receptor signaling).
A broader question to pursue, given that anhedonia reduces motivation,
is how reduced motivation can produce behavior. Incentive salience provided
a mechanism by correlating with excitation of the ventral striatum, which
elicits excitation of the motor circuitry. Anhedonia is associated with the
absence of this effect, suggesting that it must stimulate reward seeking via a
separate route. One possibility is that the dorsal striatum habit circuitry is
triggered in states of anhedonia. Devaluation of goals does not affect dorsal
striatal activity, meaning that well-learned habits (ie drug taking) and cues
(Carter & Tiffany, 2001) would function normally, but the goal-related
37
system relying on the ventral striatum would no longer be engaging in goal-
oriented behavior (Kalivas, 2009). Hence, the dorsal striatum may be
activated at typical levels with no competition from the ventral striatum, and
over-learned behaviors prevail.
Stress and drug addiction are two constructs that encompass
heterogeneous fields of research and likely cannot be reduced to one
common mechanism. Cigarette smoking is sensitive to factors as wide
ranging as social acceptance in a peer group to sensory gating deficits in
schizophrenia. The link between stress and this behavior provides a point of
intervention relevant to most people even without understanding the
biological mechanism.

38
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Appendix A
Coverage of higher-level analyses

Unique voxels coverage

56

3. Forward inference anticipation map

57
Tables
Table 1
Measure Mean Std. Dv Range
Age 36.9 10.1 24 - 55
Education 14.4 1.6 12 - 16
Shipford-Hartley Estimated IQ 112.6 8.5 94 - 121
Liked Njoy compared with cigarettes 6.6 2.1 3 - 10
Would like Njoy after abstaining 8-
12hrs
8.6 1.6 5 - 10
Number of Cigarettes per day 19.4 4.4 12 - 30
Months Smoking at Current Rate 183.2 132.2 20 - 447
Age of Dependence Onset, Years 17.0 3.1 12 - 22
Duration of Dependency, Years 19.9 11.4 4 - 37
Max Duration of Quit Attempt, Days 235.2 536.9 0 -
219
0
Expired CO, Parts per million 21.9 9.3 10 - 38
Fagerstrom 5.1 2.0 1 - 9
WISDM: Affiliative Attachment 4.2 2.0 1 - 7
WISDM: Automaticity 4.3 1.7 1 - 7
WISDM: Pos. Reinforcement 5.4 1.2 4 - 7
WISDM: Cognitive Enchancement 4.8 1.5 1 - 7
WISDM: Weight Gain 2.2 1.5 1 - 6
WISDM: Tolerance 5.4 1.2 3 - 7
WISDM: Craving 5.4 1.3 3 - 7
WISDM: Social Env. Goals 4.0 2.1 1 - 7
WISDM: Loss of Control 4.3 1.5 1.8 - 6.8
WISDM: Neg Reinforcement 5.3 1.2 2.7 - 7.0
WISDM: Taste & Sensory 5.3 1.6 1.8 - 7.0
WISDM: Cue Exp-Assoc Processes 5.2 1.3 2.3 - 7.0
WISDM: Behav. Choice-Melioration 4.3 1.5 1.0 - 6.7
WISDM: Total Score 60.1 14.1 33.4 - 85.5
TPI: Negative Affect Score 45.6 6.2 34 - 60
TPI: Anhedonia 42.5 4.1 34 - 52
TPI: Anxious Arousal 43.3 6.4 32 - 60
BIS-11: Non-Planning 24.8 6.5 13 - 36
BIS-11: Motor 24.0 5.4 18 - 40
BIS-11: Cognitive 14.9 4.3 8 - 26
BIS-11: Total Impulsiveness 63.7 14.5 42 - 102
ZTPI: Future 3.7 .4 2.7 - 4.3
ZPTI: Present 2.6 .6 1.7 - 3.6

58
Table Captions

Table 1. Characteristics of the study sample.
NJoy: Electronic cigarette; CO: Carbon monoxide; WISDM: The Wisconsin
Inventory of Smoking Dependence Motives; TPI: Tripartite Pleasure
Inventory; BIS-11: Behavioral Impulsivity Scale; ZTPI: Zimbardo Time
Perspective Inventory

59
Figures
Figure 1

60
Figure 2

61

Figure 3

62
Figure 4

63
Figure 5

64
Figure 6

65
Figure 7

66
Figure 8

67
Figure Captions

Figure 1. The modified Monetary Incentive Delay task displayed the prize at
stake during an anticipation period, a screen signaling the opportunity to
press the button to win the prize, and a feedback screen to notify the
participant of wins (“Fast enough”) and losses (“Too slow”). Participants
were instructed to press the button as quickly as possible to win prizes
(Smoke, Money) delivered immediately or 7 days later (Now,Week) and
control condition required a button press for no prize. Winning “Smoke Now”
trials were followed by a brief opportunity to inhale electronic cigarette
smoke through a tube. Participants completed 75 trials (15 per prize) during
each of two fMRI runs.

Figure 2. a. Self-reported subjective stress levels. Participants reported
subjective stress on measure of emotional and physiological state both upon
arrival (Baseline) and, for experimental sessions, after the experimental
manipulation (Cold Pressor Task, Control Task). Participants reported higher
stress levels overall (main effect of stress, F(16) = 9.328, p = 0.008),
although the Cold Pressor Task was not responsible for that difference (time
by stress interaction, F(16) = 1.423, p = 0.250). Baseline self-reported
stress was higher on the the stress day than the Enrollment day [t(16) =
2.554, p = 0.021].
68
b. Salivary cortisol concentrations. Salivary cortisol was measured
immediately before the control/stress as well as 23 min post-control/post-
stress. There was no interaction between stress conditions and pre- versus
post-task [F(1,12) = 1.01, p = 0.340]. Within the stress condition
exclusively, a paired samples two-tailed t-test between salivary cortisol
levels pre- and post-task finds that post-task levels were marginally higher
than pre-task levels [t(14) = 2.09, p = 0.055]. A similar comparison with
control condition cortisol did not detect a similar trend [t(14) = .09, p =
0.930].

Figure 3. Reaction times during the incentive delay task, presented as
within-subject z-scores to highlight relative reaction times for the various
prizes. Reaction times from trials with no prize are not pictures, but were
significantly slower than reaction times on trials with prizes.

Figure 4. Signal extracted from a mask of anticipation-related regions. Mean
BOLD signal within the mask area was extracted from each participant’s
contrasts, and the mean of those means are presented here. This procedure
was done for eight separate contrasts. Four contrasts from the stress
condition (SmN
-N
, MoN
-N
, SmW
-N
, MoW
-N
) and the same four from the
control condition. Immediate [F(1,15) = 10.696, p = 0.005, η
p
2
0.401] and
money [F(1,15) = 7.227, p = 0.016, η
p
2
= 0.311] prizes corresponded with
69
high BOLD signal in antipation related regions. The effect of stress was not
significant [F(1,15) = 1.765, p = 0.203, η
p
2
= 0.099].

Figure 5. Anticipation of All Prizes versus No Prize. A Z-statistic map of BOLD
signal differences between the anticipation period on trials when a prize was
a stake vs trials on which no prize was at stake. Maximum activation
difference of a cluster is listed with cluster size in standard font and other
peaks within the cluster are listed with the cluster size in italics to identify
which cluster the pears are in. Image is threshold at Z = 2.3, p < 0.05
cluster-corrected for multiple comparisons.
ACC: Anterior cingulate cortex; OFC: Orbitofrontal cortex; MNI Coordinates:
millimeter coordinates in the Montreal Neurological Institute standard brain
(2mm voxel version)

Figure 6. Stress effects on prize anticipation, reflecting an interaction
between reward and stress. Anticipation of all prizes, contrasted with No
Prize, from the control condition was contrasted with the same comparison
from the stress condition. Threshold at Z = 2.3, p < 0.05 cluster-corrected.

Figure 7. Immediacy effects on prize anticipation. Anticipation of all
immediate prizes contrasted with all delayed prizes. Threshold at Z = 2.3, p
< 0.05 cluster-corrected.
70
IFG: Inferior Frontal Gyrus

Figure 8. Interaction between stress and immediacy. Anticipation of all
immediate prizes contrasted with all delayed prizes from the control
condition contrasted with the same contrast from the stress condition.
Threshold at Z = 2.3, p < 0.05 cluster-corrected.

71
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Creator Cosand, Louise Debs (author)

Core Title Reward immediacy and subjective stress modulate anticipation of primary and secondary rewards in temporarily-abstinent cigarette smokers

School College of Letters, Arts and Sciences

Degree Doctor of Philosophy

Degree Program Psychology

Publication Date 05/08/2013

Defense Date 03/14/2013

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag Addiction,anhedonia,anticipation,Cigarette,cortisol,delay discounting,fMRI,functional magnetic resonance imaging,human,incentive salience,Money,Motivation,neuroimaging,nicotine,OAI-PMH Harvest,reward,Smoking,Stress

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Language English

Contributor Electronically uploaded by the author (provenance)

Advisor Monterosso, John R. (committee chair), Bechara, Antoine (committee member), Kutch, Jason J. (committee member), Saxbe, Darby E. (committee member)

Creator Email lcosand@gmail.com

Permanent Link (DOI) https://doi.org/10.25549/usctheses-c3-252796

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Legacy Identifier etd-CosandLoui-1672.pdf

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Source University of Southern California (contributing entity), University of Southern California Dissertations and Theses (collection)

Access Conditions The author retains rights to his/her dissertation, thesis or other graduate work according to U.S. copyright law. Electronic access is being provided by the USC Libraries in agreement with the a...

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