The sleep and circadian modulation of neural reward pathways: a protocol for a pair of systematic reviews
Byrne and Murray Systematic Reviews
The sleep and circadian modulation of neural reward pathways: a protocol for a pair of systematic reviews
Jamie E. M. Byrne 0
Greg Murray 0
0 Centre for Mental Health, Faculty Health, Arts and Design, Swinburne University of Technology , John St, Hawthorn, VIC 3122 , Australia
Background: Animal research suggests that neural reward activation may be systematically modulated by sleep and circadian function. Whether humans also exhibit sleep and circadian modulation of neural reward pathways is unclear. This area is in need of further research, as it has implications for the involvement of sleep and circadian function in reward-related disorders. The aim of this paper is to describe the protocol for a pair of systematic literature reviews to synthesise existing literature related to (1) sleep and (2) circadian modulation of neural reward pathways in healthy human populations. Methods: A systematic review of relevant online databases (Scopus, PubMed, Web of Science, ProQuest, PsycINFO and EBSCOhost) will be conducted. Reference lists, relevant reviews and supplementary data will be searched for additional articles. Articles will be included if (a) they contain a sleep- or circadian-related predictor variable with a neural reward outcome variable, (b) use a functional magnetic resonance imaging protocol and (c) use human samples. Articles will be excluded if study participants had disorders known to affect the reward system. The articles will be screened by two independent authors. Two authors will complete the data extraction form, with two authors independently completing the quality assessment tool for the selected articles, with a consensus reached with a third author if needed. Narrative synthesis methods will be used to analyse the data. Discussion: The findings from this pair of systematic literature reviews will assist in the identification of the pathways involved in the sleep and circadian function modulation of neural reward in healthy individuals, with implications for disorders characterised by dysregulation in sleep, circadian rhythms and reward function. Systematic review registration: PROSPERO CRD42017064994
Sleep; Circadian rhythm; Diurnal rhythm; Time of day; Reward; systematic review
There is a growing interest in moderators of the human
reward system, with biological rhythms (sleep and
circadian function) being a particular focus because of their
potential interplay in mental disorders. Sleep and
circadian function have been shown to be important in
numerous reward-related disorders (e.g. bipolar disorder,
depression, drug and alcohol use; [
]) but is also
relevant for optimal functioning in healthy individuals
]. Remarkably, no review to date has systematically
examined existing brain imaging evidence for sleep or
circadian modulation of the neural pathways of reward.
Understanding the neural pathways in these two
relationships may illuminate new clinical targets for
stabilising interacting biological rhythm and reward
dysregulation in these disorders. This protocol will begin
with a brief summary of the evidence for sleep and
circadian modulation of neural reward pathways, indicate
how imaging may examine neural reward, and suggest
some important issues in operationalising reward, before
turning to the methods and data analytic plan for the
proposed systematic review.
There is substantial evidence from animal research
that circadian and sleep function modulates neural
reward pathways. For example, Sleipness, Sorg and Jansen
] demonstrated that time of day differences in
dopamine transmission and reward-seeking behaviour
was reliant on the central circadian pacemaker, the
suprachiasmatic nucleus. Further, circadian clock gene
expression in the core reward regions (ventral tegmental
area [VTA], nucleus accumbens [NAc] and the medial
and dorsolateral prefrontal cortex [mPFC, DLPFC]) all
exhibit circadian rhythmicity [
]. In relation to
sleep, Hanlon, Andrzejewski, Harder, Kelley and Benca
] found that depriving rats of rapid eye movement
sleep led to a decrease in motivation to seek rewards the
following day. In humans, Volkow et al. [
] found that
sleep deprivation altered dopamine transmission in the
ventral striatum, which may represent a pathway for the
altered reward response seen in behavioural tasks [
] and positive mood response [
] following sleep
In humans, neuroimaging methods, particularly
commonly used functional magnetic resonance imaging
(fMRI) paradigms, have potential to illuminate the
putative sleep and circadian modulation of neural reward
pathways. In fMRI, neural activity is inferred from
changes in the blood-oxygen-level-dependent (BOLD)
signal, premised on regional blood flow. A common
approach to investigating neural reward functioning in
fMRI is via presentation of reward stimuli within a
taskbased protocol [
]. Reward studies have typically used
money, food, happy faces or attractive physical features
to activate reward regions in fMRI [
fMRI contrasts with resting state fMRI, a paradigm of
growing interest which aims to detect patterns of
fluctuating synchronous connectivity between structurally
distinct brain regions in the absence of a stimulus [
Any synthesis of fMRI studies of reward must attend
to the multiple methodological dimensions on which
studies may differ. One advantage of using task-based
imaging is that it allows for event-related and
blockbased tasks to temporally distinguish between these
reward components. Block designs employ blocks of
similar trial types which give higher power across many
trials; event-related designs can distinguish between
trials in a block, and separate out components within a
]. Reward in humans is probably not a unitary
process. Event-related designs have the potential to
distinguish between reward anticipation and reward
]. Block designs are less temporally
sensitive, but more powerful in detecting effects [
]. A second methodological consideration is that
imaging tasks use different stimuli (e.g. money, food, social
rewards) to measure neural reward [
]. In the present
context, sleep and circadian function may have different
interactions with (for example) money and food, making
it important to discriminate between studies using one
or other of these reward stimuli. A final consideration is
reward can be examined outside of the stimuli in resting
state fMRI. Resting state fMRI may capture a physiological
preparedness to engage with rewarding stimuli in the
The aim of this study is to synthesise existing research
on the putative modulation of neural reward pathways
by sleep and circadian function. An initial scoping of the
literature strongly suggested that (a) these two
modulation propositions would be best investigated separately
to minimise heterogeneity and facilitate synthesis, and
(b) there were sufficient studies in each area to support
two separate systematic reviews. Therefore, the objective
of this study is to conduct a pair of systematic reviews,
driven by the following questions.
1) What evidence is there for modulation of neural
reward pathways by sleep?
2) What evidence is there for modulation of neural
reward pathways by circadian function?
This systematic review will be written using the Preferred
Reporting Items for Systematic Reviews and Meta-Analysis
Protocols (PRISMA-P) guidelines (Additional file 1). This
systematic review has been registered with the
International Prospective Register of Systematic Reviews
(PROSPERO, registration number: CRD42017064994).
Criteria for study inclusion
(i) Study methods. Studies will be included if they use
naturalistic designs or experimental designs
(including cross-sectional, longitudinal, case-control
studies and cross-over) to manipulate sleep or circadian
function to examine neural reward functioning through
fMRI. In addition, articles must be written in English
and published in a peer-reviewed journal.
(ii)Study participants. Studies will be eligible for
inclusion if they include samples of human subjects
of any age. In the sleep systematic review, studies
that include insomnia, symptoms or disorders will
be included if these quasi-experimental groupings
formed the predictor variable, compared to another
sleep comparison group. So too, in the circadian
systematic review, delayed or advanced sleep-wake
phase will be included if these symptoms or disorders
are related to another circadian function comparison
group. In both reviews, clinical samples with
psychological or physical illnesses that may affect reward will
be excluded. Studies using samples with neurological
or physiological disorders that have a pronounced
effect on sleep (e.g. narcolepsy, Kleine-Levin syndrome,
obstructive sleep apnoea) or circadian function (e.g.
blind individuals or traumatic brain injury) will be
excluded from both reviews. Studies that use
pharmacological, acupuncture, transmagnetic stimulation or
administered reward-related substances (alcohol,
drugs [including caffeine and nicotine]) will be
excluded, as this intervention may affect both the sleep
or circadian predictor variable and the neural reward
activation outcome variable. Individuals who have
diagnoses of disorders known to affect the reward
system (e.g. bipolar disorder, major depressive disorder,
gambling disorder, alcohol and drug use disorders)
will be excluded. Studies investigating altered reward
response specific to a population (e.g. displaying
images of alcohol to heavy alcohol users) will also be
excluded, on the grounds that they effectively add an
additional interaction term to the two broad
relationships of interest in this systematic review.
(iii)Search strategy for study identification. Relevant
health and neuroscience electronic databases
(Scopus, PubMed, Web of Science, ProQuest,
PsycINFO and EBSCOhost) will be searched for
articles from the database inception until October
2017. Reference lists of selected articles, relevant
reviews and meta-analyses and supplementary data
files will be examined to identify any additional
articles. The search strategy includes examining the
article title, abstracts and keywords for relevant
criteria (Table 1).
As seen in Tables 1 and 2, search term 1 aims to
identify studies collecting data on sleep (Table 1) or circadian
function (Table 2). All studies must have a predictor
1 TITLE-ABS-KEY(SCN OR suprachiasmatic OR circadian OR diurnal
OR “clock gene*” OR “time of day” OR cortisol OR melatonin OR
owl OR lark)
2 TITLE-ABS-KEY(striatum OR “anterior cingulate” OR “ventral tegment*
OR putamen OR VTA OR NAc OR accumben* OR “medial prefrontal
cortex” OR MPFC OR “orbitofrontal cortex” OR OFC OR thalamus OR
insula OR “dorsolateral prefrontal cortex” OR DLPFC OR amygdal*
OR “locus coeruleus” OR LC OR dopamine* OR seroton* OR limbic
3 TITLE-ABS-KEY (reward OR arousal OR happ* OR food OR money
OR positiv* OR affect OR emoti* OR reinforcement OR instrumental)
4 TITLE-ABS-KEY(imag* OR FMRI OR MRI)
5 NOT TITLE-ABS-KEY(rat OR rodent OR mouse OR mice OR hamster
6 (LIMIT-TO(DOCTYPE,“ar”) OR LIMIT-TO(DOCTYPE,“ip”)
7 2 OR 3
8 1 AND 4 AND 5 AND 6 AND 7
variable which is an experimental manipulation, or a
naturalistic (quasi-experimental) quantification of sleep
or circadian function.
a. For the sleep review, studies that included different
sleep stages or insomnia symptoms will be included
as well as more traditional sleep deprivation or sleep
b. For the circadian function review, studies will be
deemed to speak to the circadian function of reward
if they use a repeated-measure protocol at different
times of day (measuring a diurnal [daily] rhythm)
and measure circadian phase through preformed
chronotype (morning, evening type individuals)
groups or use more endogenous markers of
circadian function such as circadian genes,
melatonin or cortisol levels.
Search term 2 identifies studies collecting data on the
neural basis of reward, while search term 3 identifies
reward stimuli that may be used in imaging studies.
Neural reward activation as measured by fMRI will be the
outcome variable of both the planned systematic literature
reviews. Reward functioning can be examined as an
outcome of reward tasks, or through resting state scans that
examine brain regions or neuronal activity associated with
rewards. Search terms will be broad, including terms for
reward stimuli, neural reward regions of interest and
whole-brain analyses in fMRI studies. Search term 4
identifies fMRI paradigms, with search term 5 excluding
commonly used animals in sleep and circadian research,
and limits to full articles that are already in press (search
term 6). Search term 7 aims to identify studies that have
searched for or identified neural reward regions or used
an imaging paradigm with reward-based stimuli.
Articles will be screened in two stages. Stage 1 (titles
and abstract) will screen for inclusion and exclusion
criteria (see Additional file 2). Stage 2 will collate the
study selection results, and two authors will review the
full texts for any discrepancies with Cohen’s Kappa for
inter-rater agreement assessed and reported. If
agreement cannot be reached, a third reviewer from the
authors will make the final decision.
A data extraction form in Microsoft Excel will be used
to compile the method and results from each of the
selected studies for the (1) sleep systematic review and
(2) the circadian systematic review (see Additional file 3).
Two independent reviewers will complete this form for
the selected articles. Given the diverse measurements of
sleep, circadian function and reward, this form will detail
the sleep or circadian variable and how this was used in
the method, whether a stimuli was or was not used in
the neuroimaging protocol (with a description of the
reward stimuli), participant information and
characteristics, the imaging procedures used and regions of interest
investigated and/ or identified, results, interpretation
and limitations of the research, with two reviewers
independently completing this extraction. Two authors will
then complete a quality assessment of the articles using
the Effective Public Health Practice Project (http://www.eph
quality assessment tool measuring the robustness of articles
through an examination of selection bias, study design,
confounders, blinding, data collection methods, withdrawal and
dropout, intervention integrity and analyses. The strength of
this measure is that it allows for component and global ratings
to be made; thus, components in this literature that may be
less relevant (such as blinding) can be discussed without losing
the important cross-study evaluation of the relevant quality
assessment components. Where consensus is not reached on
the quality assessment, a third reviewer will be relied on. In
studies which investigate bi-directional influences between
sleep/circadian and reward activation, only the primary
direction of interest here (sleep and circadian modulation of
reward) will be considered.
As we expect the studies to be heterogeneous in both
the sleep and circadian systematic reviews and the
operationalisation of reward variables, the main data analysis
will follow a narrative synthesis of articles in both cases.
Popay et al.’s [
] four-step framework for developing an
effective narrative synthesis will be used. The first step
in the narrative synthesis will provide an explanation for
how sleep or circadian function may causally impact
different neural reward pathways. This step will map the
potential neural pathways of reward in humans, and
how these may relate to the different reward stages
(reward anticipation and reward outcome). The second
step entails a preliminary synthesis of the identified
studies, describing the pattern of results by sleep and
circadian function separately. The primary aim of this
step will be to identify whether the neural reward
outcome is modulated by sleep or circadian function, paying
attention to the region affected, the direction of effect
and the magnitude of observed effects in each individual
study. A third step will involve analysis of these findings
across studies, concentrating on cross-study design and
methodological factors that may explain discrepancies
between studies. For the present review, an important
focus at this step will be cross-study differences in
reward measurement (stimuli and imaging method used)
and the reward stage (anticipation and outcome)
examined. The final step will involve assessing the strength of
evidence for the sleep and circadian modulation of
reward as organised by reward stage and region. This
will involve collating the results of the EPHP quality
assessment (above) to see if some findings should be
weighted more highly through both the quantity of
evidence for an approach and the design qualities which
may best address the current research question for the
final narrative synthesis.
Currently, no systematic literature reviews have
considered the impact of either sleep or circadian function on
neural reward pathways. This is an important gap in
knowledge, because recent empirical and theoretical
evidence (e.g. [
]) have suggested a disturbed
interaction between sleep/circadian function, and reward
processes may be pivotal to serious reward-related
psychopathologies including bipolar disorder, major
depression and alcohol and drug use disorders. Better evidence
in the general population for the putative existence,
direction and strength of such relationships at the neural
level in a pair of systematic reviews has the potential to
improve understanding and ultimately management of a
range of psychopathologies.
We expect that the primary limitation of these systematic
literature reviews will be heterogeneity across identified
studies. The measurement of neural reward activation has
not been standardised across studies, with different
designs using different types of reward stimuli, and varied
focus between reward stages (anticipation and outcome).
In addition, some studies will investigate neural reward
through stimuli-response paradigms while others use
resting state data to speak to a neural preparedness to engage
in reward behaviour. While all these studies may speak to
a sleep and circadian modulation of neural reward
activation, differences in study paradigms will be important
qualifications on any synthesis. On the basis of the results
of the narrative synthesis, however, we expect to be able
to identify which protocols may best illuminate the sleep
and circadian modulation of neural reward activation in
A final potential limitation of the literature is that few
studies are expected to speak to both sleep and circadian
function, which are known to be deeply interdependent.
As such, this pair of reviews will emphasise that while it
is scientifically important to examine sleep and circadian
functioning separately, practically, these two studies will
be confounded by the respective sleep or circadian
process. As a result, these two systematic reviews can
help inform future research ofsome of the ways that
neuroimaging may better manage the interplay between
sleep and circadian rhythms in their joint determination
of neural reward functioning.
Additional file 1: PRISMA-P (Preferred Reporting Items for Systematic
review and Meta-Analysis Protocols) 2015 checklist: recommended items
to address in a systematic review protocol*. (DOC 60 kb)
Additional file 2: Article Selection. (XLSX 8 kb)
Additional file 3: Data Extraction. (XLSX 11 kb)
No applicable funding for the reviews.
Availability of data and materials
Blank article selection and data extraction forms are available as additional
files. Upon publication of the review, article selection and data extraction
forms will be made available with email requests.
JB wrote the first draft of the protocol and contributed to the design. GM
contributed to the design, drafting of the manuscript and original idea for
review. Both authors read and approved the final manuscript.
Ethics approval and consent to participate
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
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