Repeated afternoon sleep recordings indicate first‐night‐effect‐like adaptation process in family dogs

Abstract

The importance of dogs (Canis familiaris) in sleep research is primarily based on their comparability with humans. In spite of numerous differences, dogs' comparable sleep pattern, as well as several phenotypic similarities on both the behavioural and neural levels, make this species a most feasible model in many respects. Our aim was to investigate whether the so‐called first‐night effect, which in humans manifests as a marked macrostructure difference between the first and second sleep occasions, can be observed in family dogs. We used a non‐invasive polysomnographic method to monitor and compare the characteristics of dogs' (N = 24) 3‐hr‐long afternoon naps on three occasions at the same location. We analysed how sleep macrostructure variables differed between the first, second and third occasions, considering also the effects of potential confounding variables such as the dogs' age and sleeping habits. Our findings indicate that first‐night effect is present in dogs' sleep architecture, although its specifics somewhat deviate from the pattern observed in humans. Sleep macrostructure differences were mostly found between occasions 1 and 3; dogs slept more, had less wake after the first drowsiness episode, and reached drowsiness sleep earlier on occasion 3. Dogs, which had been reported to sleep rarely not at home, had an earlier non‐rapid eye movement sleep, a shorter rapid eye movement sleep latency, and spent more time in rapid eye movement sleep on occasion 3, compared with occasion 1. Extending prior dog sleep data, these results help increase the validity of further sleep electroencephalography investigations in dogs.

Full text

J Sleep Res. 2020;00:e12998.  
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1 of 10
https://doi.org/10.1111/jsr.12998
wileyonlinelibrary.com/journal/jsr
1 | INTRODUCTION
The dog (Canis familiaris) has been proved to be an interesting and
valid animal model of human socio-cognitive skills not just at the
behavioural level (Miklósi & Topál, 2013), but also in the area of
neurocognitive research, including sleep-related cognition (Bunford,
Andics, Kis, Miklósi, & Gác si, 2017). One prominent line of canine
neuroscience literature focuses on awake functioning, mainly using
Received:9December2019
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Revised:23Januar y2020
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Accepted:26Januar y2020
DOI : 10.1111 /js r.12998
REGULAR RESEARCH PAPER
Repeated afternoon sleep recordings indicate first-night-effect-
like adaptation process in family dogs
Vivien Reicher1 | Anna Kis2 | Péter Simor3,4 | Róbert Bódizs4,5 | Ferenc Gombos6,7 |
Márta Gácsi1,8
This is an op en access article under t he terms of the Creat ive Commons Attributio n License, which permits use, dist ribution and reproduc tion in any medium,
provide d the orig inal work is proper ly cited .
© 2020 The Authors . Journa l of Sleep Re searchpublishedbyJohnWiley&SonsLtdonbehalfofEuropeanSleepResearchSociety
1DepartmentofEthology,Institute
ofBiolog y,EötvösLorándUniversity,
Budapest, Hungary
2ResearchCentreforNaturalSciences,
Institute of Cognitive Neuroscience and
Psychology, Budapest, Hungary
3InstituteofPsychology,EötvösLoránd
University,Budapest,Hungar y
4InstituteofBehaviouralSciences,
SemmelweisUniversity,Budapest,Hungary
5JuhászPálEpilepsyCenter,National
Instit ute of Clinical Neuroscien ce, Budapest,
Hungary
6Department of General Psychology,
PázmányPéterCatholicUniversity,
Budapest, Hungary
7MTA-PPKEAdolescentDevelopment
Research Group, Budapest, Hungary
8MTA-ELTEComparativeEthologyResearch
Group, Budapest, Hungary
Correspondence
VivienReicher,DepartmentofEthology,
InstituteofBiology,EötvösLoránd
University,PázmányPétersét ány1/C,1117
Budapest, Hungary.
Email:vivien.reicher@gmail.com
Funding information
HungarianScientificResearchFund,
Grant/AwardNumber:OTKAK115862,
OTKAK132372,OTKAFK128242and
NKFIFK128100;HungarianAcademy
ofSciences,Grant/AwardNumber:MTA
01031;BIALFoundation,Grant/Award
Number:169/16
Summary
The importance of dogs (Canis familiaris) in sleep research is primarily based on their
comparability with humans. In spite of numerous differences, dogs' comparable sleep
pattern, as well as several phenotypic similarities on both the behavioural and neural
levels, make this species a most feasible model in many respects. Our aim was to
investigate whether the so-called first-night effect, which in humans manifests as
a marked macrostructure difference between the first and second sleep occasions,
canbeobservedinfamilydogs.Weusedanon-invasivepolysomnographicmethod
to monitor and compare the characteristics of dogs' (N = 24) 3-hr-long afternoon naps
onthreeoccasionsatthesamelocation.Weanalyse dhowsle epmacrostructurevari-
ables differed between the first, second and third occasions, considering also the
effects of potential confounding variables such as the dogs' age and sleeping habits.
Our findings indicate that first-night effect is present in dogs' sleep architecture, al-
thoughitsspecificssomewhatdeviatefromthepatternobservedinhumans.Sleep
macrostructure differences were mostly found between occasions 1 and 3; dogs slept
more, had less wake after the first drowsiness episode, and reached drowsiness sleep
earlier on occasion 3. Dogs, which had been reported to sleep rarely not at home,
had an earlier non-rapid eye movement sleep, a shorter rapid eye movement sleep
latency, and spent more time in rapid eye movement sleep on occasion 3, compared
withoccasion1.Extendingpriordogsleepdata,theseresultshelpincreasethevalid-
ity of further sleep electroencephalography investigations in dogs.
KEY WORDS
dog model, neuroethology, non-invasive electroencephalography

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functionalmagneticresonanceimaging (Andics et al., 2016; Berns,
Brooks , & Spivak, 2012) an d electroe ncephalogr aphy (EEG)-based
(ERP)methods(Howell,Conduit,Toukhsati,&Bennett,2011;Kujala
et al., 2013). A somewhat independent line of research investigates
the characteristics of the dogs' sleep, mainly building on the fact that
thegeneralarchitectureofhuman sleepis better approximated by
dog sleep, and not by the most commonly used laborator y animals
(Toth&Bhargava,2013).Strong interrelatedness has been discov-
ered between dogs' sleep and awake functioning, including mem-
ory con solidation (Io tchev et al., 2017; Kis, Szak adát, et al., 2 017)
andemotionprocessing(Kis,Gergely,etal.,2017).Earlystudieson
dogs' sleep focused on neurological conditions (e.g. epilepsy), and
usedinvasivemethodsonlaboratorydogs(Shimazono etal.,1960;
Wauquier,Verheyen,Broeck,&Janssen,1979).Recently,anon-inva-
sivepolysomnography(PSG)methodhasbeen developedtoinves-
tigate the sleeparchitecture of familydogs (Kis,Szakadát,Kovács,
et al., 2014), which has been successfully used to monitor natural
sleepindogsasafunctionofpre-sleepexperiencesand/orindivid-
ual differences (Bunford et al., 2018; Kis, Gergely, et al., 2017; Kis,
Szakadát,etal.,2017).
However, the basic characteristic s of dogs' natural sleep patterns
(without pre-sleep treatment) have only been tangentially investi-
gated(Kis,Sz akadát,Kovács ,etal.,2014),wh ereasadescr iptiveanal-
ysis of sleep macrostructure was provided only for a single recording
session. To gain more insight into the basic mechanisms of natural
sleep in family dogs, we conducted three consecutive sleep record-
ings without affecting the dogs with any pre-sleep activity or han-
dling. Our primar y goal was to assess the so-called first-night ef fect
(FNE), a phe nomenon well k nown in human sl eep researc h, which
manifests in marked macrostructure differences between the first
andsecondsleepoccasionsmeasuredbyPS G.Themajorfactorsthat
contributetoFNEareunfamiliarsurroundings(e.g.sleeplaboratory),
discomfor t and limited mobility caused by electrodes, and psycho-
logical pressure of being under observation (Le Bon et al., 20 01).
It is a common practice in human sleep studies to consider the
first sleeping occasion as an adaptation session and thus discard
it from fur ther analysis without direct comparison to the follow-
ingoccasions.Studies thathaveassessedthedifferencesbetween
the sleep macrostructure of the first versus second night spent in
thelaboratoryhaveconsistentlyfound that FNEisassociatedwith
an increased state of alertness, which results in alterations in the
sleep pat tern: increased number of awakenings and more time spent
awakeaftersleeponset(WASO)leadingtolesstimespentsleeping,
increasedwakefulness,lessrapideyemovement(REM),longerREM
latencyandincreasedslow-wavesleep(SWS)latency(Agnew,Webb,
&Williams,1966;LeBonetal.,2001).Althoughthephenomenonis
calledtheFNE,humanstudiesindicatethat,forcertainparameters,
morethan1 nightisneededtoachievestability,forexampleREM-
relatedvariables(LeBonetal.,2001;Schmidt&Kaelbling,1971).
All previous non-invasive dogPSG measurements were either
carriedoutwiththeexclusion ofthefirstsleepoccasionandcoun-
terbalancing pre-sleep treatments between the second and third oc-
casions(Bunfordetal.,2018;Kis,Gergely,etal.,2017;Kis,Szakadát,
et al., 2017;Kis, Szakadát, Kovács, et al., 2014),or exclusively fo-
cused on one-time recordings (Iotchev et al., 2019). This was based
ontheassumptionthat,similarlytohumans(Agnewetal.,1966;Le
Bon et al., 2001), there must be specific differences in dogs' sleep
patterns and brain activity between the consecutive sleep occa-
sions. Additionally, some of these studies (Kis, Gergely, et al., 2017)
reported a lack of order effect between the second and third sleep
occasions, indicating that at that stage, adaptation effects could be
of smaller magnitude compared with the effect of pre-treatments
used. In light of our scarce knowledge on the number of occasions
needed for dogs to adapt to sleep with electrodes on their heads and
bodiesina newenvironment,amorethoroughanalysisofFNEhas
become essential.
Age is an important factor that both influences sleep−wake
rhythm(Takeuchi & Harada, 2002) and theEEGspectrum of dogs
(Kis, Szakadát, Kovács, et al.,2014;Takeuchi & Harada, 2002) and
humans (Carrier, Land, Buysse, Kupfer, & Monk, 20 01). Thus, in
order to gain pure insight into the effect of repeated laboratory
testing (PSG recordings) on dogs’ sleep structure, variables such
as age need to be included as potential confounding factors in the
analyses. Moreover, the sleep laboratory is a novel and potentially
perceived as a stressful environment, which might have a determi-
nantroleinsleepquality(Lima,Rattenborg,Lesku,&Amlaner,2005;
Voss, 2004). As dogs tend to vary with regard to their sleeping hab-
its(frequencyofsleepingawayfromhome),itcanbeassumedthat
differences will emerge bet ween dogs that rarely versus those that
often sleep away from home, making it imperative to control for such
environmental factors.
Similarlyto humans,dogs'sleepingpattern is sensitivetothe
timing of sleep: at night-time, dogs tend to sleep more, spend more
timeinnon-rapideyemovement(NREM) and REM andlesstime
indrowsiness,andwakeafterfirstdrowsiness(WASO1,formore
details onWASO1indogs,seeSection2.5) comparedwithday-
time (Bunford et al., 2018). However, during the day, dogs are also
prone to sleep, especially during the afternoon period (Tobler &
Sigg, 1986).Thus, forpractical reasons(e.g.inorder to reachan
adequatesamplesize),alldogstudiessofarhavebeenbasedonaf-
ternoon sleep recordings. Though we are not aware of any human
studiesdocumentingFNEin thecontextoftheafternoonnap,it
is plausible to assume that an adaptation effect is also present in
repeatedafternoonsleepsessions.Furtherdifferencescompared
with human studies arise from the fact that due to practical rea-
sons (availability of dog owners volunteering for the study), dog
PSG measurements are not recorded on consecutive days, but
with gaps of several days/weeks/months between occasions. The
effect of this procedural confound has not yet been addressed but,
basedongeneralhabituation−dishabituationtheory,thetimebe-
tween measurements might interfere with the general adaptation
(FNE)effect.
Taken together, prior research into human sleep indicates sig-
nificant and relevant differences in sleep structure between the
first two(andpotentiallymore)sleepoccasions.Wesuggest that
inorder to runvalidcomparative EEGstudies, it is an important

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precond ition to examin e the process of do gs' adaptatio n to the
PSG test si tuation. We assumed that human-li ke FNE could be
observed between the first/second and possibly the second/third
measurement in dogs, resulting in relatively similar changes in
their sleep structure to that of humans, including more intermit-
tentwaketime( WASO),decreasedsleepeff iciency(percentageof
timespentsleepingduringthe3-hr-longmeasurement),lessREM
sleep, lo nger REM and slee p latencies dur ing the firs t occasion.
Wealsoexaminedtheeffectsofageandsleephabitsontherele-
vant sleep parameters.
2 | METHODS
2.1 | Subjects
Wemeasured30familydogswhoattendedthecanineEEGlabwith
theirowners.Sixdogswereexcludedeitherduetothelackofsleep
(four dogs) or recording ar tefacts caused by high muscle tone (two
dogs). The 24 dogs whose data were used for the analysis were
7 months–9 years old; nine males and 15 females (14 out of the 15
female dogs had been neutered, and the remaining one female dog
was not in heat during any of the recording occasions); from nine dif-
ferent breeds and 10 mutts.
Owners were recruited from the Family Dog Project (Eötvös
Loránd University, Department of Ethology) database. All experi-
mentalprotocolswereapprovedbytheScientificEthicsCommittee
for Animal Experimentation (Állatkísérleti Tudományos Etikai
Tanács) of Budape st, Hungar y (number of ethic al permissio n: PE/
EA/853-2/2016). The location of the measurements was a fully
equippedlaboratoryforcanineEEGmeasurementsattheResearch
CentreforNaturalSciences,InstituteofCognitiveNeuroscienceand
Psychology.
2.2 | Procedure
ParticipationinthesleepEEGresearchdidnotrequirepriortrain-
ing. All subjects were measured on three occasions at the same
location. All the recordings were conducted during the afternoon,
withastarttimebetween12:00 hoursand17:00 hours.Foreach
individual dog, the starting time of the three different nap op-
portunities was kept within a ±2 hr interval between recording
occasions. Recordings were conducted within 11.03. 2017 and
22.12.2018 interval.For one dogall three recordings werecon-
ducted within the same season (during autumn); while for others
they were spread out from spring to summer N = 3; from spring
to autumn (first two recordings in spring, third recording in au-
tumn) N = 8; from autumn to winter N = 10; from summer to au-
tumn N = 2. Between occasions 1 and 2, 1–4 weeks passed, while
between occasions 2 and 3 for a subgroup (N = 10) 3–4 weeks
passed, and for the other subgroup (N=14)5weeks–6months
passed. Applying this set-up allowed us to investigate the effect of
time elapsed between the recordings.
All measurements were carried out after a relatively active day
(i.e. a physic ally and mentally loaded day due to advanced train-
ing,excursion).Thoughtheactivitylevelcouldbeslightlydifferent
between dogs, an individual's activity level was the same before
allsleepingoccasions.Beforethemeasurement,theexperimenter
explained the processto the owner while the dogcould explore
the room (5–10 min). Then the owner settled on the mattress with
the dog and held the dog's head gently while the experimenter
was placing the surface electrodes. During electrode placement,
dogs were rewarded using social (e.g. petting, praise) and/or food
reward.After the electrode placementandthecheckof the PSG
signals, owners were asked to mute their cell phones and engage
in a quiet activitysuch asreading, watching a movie on alaptop
withearphonesor sleeping duringthemeasurement.The experi-
menter lef t the room and monitored the measurement on a laptop
in the adjacent room. In case of the rare event of the malfunction
of an electrode, theexperimenter replaced or changed the elec-
trode. The canine sleep laboratory is a room with no window, thus
an inbuilt heating and air-conditioning system was set to keep the
temperature at the same level (about 22°C), and a reading lamp was
provided for those owners who wished to read (which was then on
for all recordings).
2.3 | PSG placement and monitoring
SleepwasmonitoredbyPSG,whichallowedtheparallelrecording
ofEEG,electrooculogram(EOG),electrocardiogram (ECG), respi-
ration (PNG) and electromyography (EMG). In thisresearch pro-
ject, wefollowedthe previouslyvalidated PSG method ondogs
(Kis,Szakadát,Kovács,etal.,2014)withthesingleadditionofan-
otherelectrodeontherightzygomaticarch.Withthisnewset-up
insteadoftwo,fourEEGchannelsandaneyemovementchannel
had been recorded. The two electrodes placed on the right and
left zygomatic archnext to the eyes(F8,F7) andthescalp elec-
trodes overtheanteroposterior midlineoftheskull(Fz,Cz)were
referred to the G2, a reference electrode that was in the posterior
midlineoftheskull(occiput;externaloccipitalprotuberance).The
ground electrode (G1) was attached to the left musculus tempo-
ralis. ECGelectrodeswereplacedbilaterally over the secondrib.
SeeFigu re1forphotoofadogwithelectrodeplacement;Figure2
fordetaileddrawingofadogwiththenamesandexactplacement
oftheelectrodes;andFigure3forexamplesofPSGdatafromthe
four different sleep stages.
Fortherecordings,gold-coatedAg/AgClelectrodeswereused,
secured bySigna SprayElectrode Solution (Parker)and EC2 Grass
Electrode Cream (Grass Technologies). The impedance values of
the EEGelectrodeswerekept under20kΩ during the recordings.
Thesignalswerecollected,pre-filtered,amplified anddigitizedata
samplingrate of 1,024 Hz perchannel,using the 25-channelSAM

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25R EEG System (Micromed), and the System PlusEvolutionsoft-
warewithsecond-orderfiltersat0.016Hz(highpass)and70Hz(low
pass).
2.4 | Questionnaire
We sent out an online questionnaire to all participating owners
about the sleeping habits of the dogs. This was done based on the
assump tiontha td ogs,w hichsleep frequ entlyou tside theirho meen-
vironment, might find it less stressful to sleep in a laboratory. In the
questionnaireownershadtoratetheirdogsona0–3(never;rarely;
often; ver y often) scale on the following statements: How often
does the dog sleep (a) in a novel environment in the presence of the
owner (who is engaged in other activities; work, meeting) during the
afternoon; (b) not at home but in a familiar environment in the pres-
ence of the owner (who is engaged in other activities; work, meeting)
during the afternoon; (c) in a novel environment in the presence of the
owner at night; (d) not at home but in a familiar environment in the
presence of the owner at night?
Most owners reported that their dogs never or rarely slept not
at home in a familiar (79%) or new environment (100%) during the
night. Moreover, most owners (75%) reported that their dogs never
or rarely slept in the afternoon in a new environment. Therefore,
only the second question yielded reasonable variability in re-
sponses, therefore we included it as a factor in our analysis, lumping
never and rarely responses (N=0 + 10; mean age=4.8±2.2)and
often and very often responses (N=10 + 4;meanage= 4.9±2.9)
so that in the end we had two categories for “sleep habits”: rarely
sleepin g away from home (RS AH); and often sl eeping away from
home(OSAH).
2.5 | Data analysis
Sleep re cordings were visua lly scored in accorda nce with standa rd
criteria (Berryetal., 2015), adapted for dogs(Kis, Szakadát,Kovács,
etal., 2014). A self-developed program (by FerencGombos;Fercio's
EEGPlus,2009–2019)was used to analyseandexportdata. The re-
cordings were manually scored, and the program provided data for
exportingmacrostructuralvariables.Thismanualcodingreliablyiden-
tifies the stages of wake, drowsiness, NREM and REM in dogs (Kis,
Szakadát,Kovács ,etal.,2014).Anota bledifferenc ei nt hecanin esleep
stage scoring, compared with human studies, arises from the fact that
in dogs there is a stage called drowsiness that bears characteristics
ofbothhuman Stage1 NREMsleepand quietawake.Drowsinessis
characteristic of insectivore and carnivore mammals (including dogs),
asinthesetaxathetransitionfromwakefulnesstosleepisnotasclear
as in humans ( Zepelin et al., 2005). Due to this difference, we used t wo
approaches/measurestodetermineWASO,sleeplatencyandREMla-
tency.IncaseofWASOandREMlatency,WASO1andREMlatency1
weremeasuredfromthefirstdrowsinessepisode,whileWASO2and
REMlatency2wereme asuredfromthefirstNREMepisode.Inc as eof
sleep latency, sleep latency 1 was measured until the first drowsiness
FIGURE 1 Photo of a dog with electrode placement before the
measurement.Electroencephalogram(EEG)andelectrooculogram
(EOG)electrodeswereplacedonthescalp,electrocardiogram
(ECG)electrodeswereplacedbilaterallyoverthesecondrib,and
electromyogram(EMG)electrodeswereattachedonthemusculus
iliocostalis dorsi. Respiration was recorded by a respirator y band.
Note: during the measurement the owner's hand was not on the dog
FIGURE 2 Placement of the electrodes
andtherespiratorybelt(Fz-Cz:frontal
andcentralmidline;F7-F8:rightandleft
electrodesplacedonthezygomaticarch;
G2: reference electrode; G1: ground
electrode;ECG:electrocardiographic
electrodes;EMG:electromyography
electrodes;PNG:respiratorybelt−
respiratory inductance plethysmography)

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episode,whilesleeplatency2wasmeasureduntilthefirstNREMepi-
sode. It also needs to be noted that in dog sleep research the different
stagesofNREMarenotdistinguished,buthandleduniformlyasSWS
orNREMsleep(Kis,Szakadát,Kovács,etal.,2014).
2.6 | Analytic plan
For alls tatisticalm odelsthe 10 dependent macrostructural variables
of interest were: sleep efficiency (the percentage of time spent asleep:
drowsiness+NREM+REMduringthe3-hr-longmeasurement),thedu-
ration of time spent awake after the first epoch scored as drowsiness
(WASO 1)and NREM (WASO2)sleep, the latencytofirstdrowsiness
(sleep latency 1) and NREM (sleep latency 2) sleep, theproportion of
time spent in drowsiness,NREM andREM sleep, the latency toREM
slee pa fterd ro wsiness(R EMlatency1)an dN REM(REMlatenc y2)slee p.
To measure the effect of the time elapsed between occasions,
weranseparategeneralizedlinearmixedmodels,wherethesubject
ID was included as a random factor, the macrostructural variables
were entered as target s, and time intervals between occasions were
enteredasfixedfactors.
TomeasureFNE,thedifferencebetweensleepmacrostructure
(for the above-described 10 variables of interest) on sleep occasions
1,2and3wasanalysedwithgeneralizedlinearmixedmodelswith
backward elimination. Statistical analyses were performed using
IBM's SPSS25.0 software.The subject ID wasincludedas a ran-
dom factor. The macrostructural variables were entered as targets,
whereas occasion, dogs' sleep habits, age (in years), and the inter-
actionofoccasionandsleephabitswereenteredasfixedfactors.
In case of sleep and REM latencies the statis tical analyses
wereconductedin R3.6.1(RCoreTeam,2014).Thesevariables
were analysed using Mixed Effects Cox Models (R package
‘coxme’;Therneau,2015),withoccurrenceofREMsleepastermi-
nal event. The subject ID was included as a random factor. In all
initial models, the effect of occasion, sleep habits, age (in years),
and interaction of occasion and sleep habits were included as
fixedfactors.
3 | RESULTS
Elapsedtimebetweenoccasionshadnoeffectonthesleepvariables
(all p > .05), thus we did not include it in further analyses.
3.1 | Sleep efficiency
Occasion had an effect on sleep efficiency (F2, 65= 19.874,p < .001),
which was greatest on occasion 3. Pairwise post hoc analysis revealed
a difference between occasions 1 and 3 (p < .001) and occasions 2 and
3 (p = .019), but no difference between occasions 1 and 2 (p = .111;
Figure4a).Dogs'sleephabitshadanoccasion-specificeffectonsleep
efficiency (F2, 65 = 3.655,p=.031):OSAHdogssleptmoreduringocca-
sion1comparedwith RSAHdogs(p=.016;Figure6).Moreover,age
had a main effect on sleep efficiency: older dogs slept more, compared
to younger dogs (F(2,65) = 8.382, p = .005).
3.2 | WASO 1 and WASO 2
Occasio n affected WASO 1 (F2 ,67 = 5.3 44, p = .007). More specifi-
cally, dogs spent less time awake after the first drowsiness episode
FIGURE 3 Representativepolysomnographic(PSG)tracesfromthesleepstagesof(a)wake,(b)drowsiness,(c)non-rapideyemovement
(NREM),(d)rapideyemovement(REM)

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on occasion 3, compared with occasion 1 (p = .013) and occasion 2
(p = .05), while occasion 2 did not differ from occasion 1 (p = .989;
Figure4b).AgeaffectedWASO1: olderdogsspentlesstimeawake
after their first drowsiness episode, compared to younger dogs
(F2,67=5.658,p =.020).Moreover,dogs’sleephabitshadatendency
effect (F2,67 = 3.725, p=.058):OSAHdogsspentlesstimeawake,
comparedtoRSAHdogs.
Occasio n showed a trend o n WASO 2 (F2,68 = 2.943, p = .059;
Figure 4c). In addition, age had a main effect on WASO 2
(F1,68 = 5.580,p = .021): older dogs spent less time awake after their
firstNREMepisode,comparedwithyoungerdogs.Dogs'sleephab-
its showed no effec t (F1,67 = 2.580,p = .113).
3.3 | Sleep latency 1
The Cox model proved to be significant in case of sleep la-
tency 1, and occasion had a main effect ( χ2
3=25.65; p < .001;
AIC = 19.65). Dogs reached drowsiness sleeplater onoccasion
1,comparedwithoccasions2(exp(β) = 0.379, z=−2.82,p = .0 01)
and3(exp(β) = 0.243, z=−3.89,p < .001), but no difference was
found bet ween occasions 2 and 3 (exp(β) = 0.384, z = −1.34,
p=.375;Figure5a).Moreover,ageandsleephabit shadnoeffect
(all p > .05).
3.4 | Sleep latency 2
TheCoxmodelprovedtobesignificantincaseofsleeplatency2,
including an interaction of occasion and sleep habits (χ2
6=23 .4 6;
p<.001;AIC=11.46).RSAHdogsreachedNREMsleeplateron
occasion1,comparedwithoccasions2(exp(β) = 0.251, z=−2.56,
p=.028)and3(exp(β) = 0.135, z=−3.53,p = .001), while occa-
sion 2 did notdifferfrom occasion 3 (exp(β) = 0.54, z = −1.24,
p=.4 33).Moreover,RSAHdogsre ac he dNREMsleepl ateronoc-
casion1,comparedwithOSAHdogs(exp(β) = 0.245, z=−2.019,
p=.043;Figure5b).Ageshowednoeffect(exp(β) = 1.087,
z = 0.81, p = .42).
FIGURE 4 The effect of occasion on (a) sleep efficiency, (b) wake after first drowsiness and (c) wake after first non-rapid eye movement
(NREM)episode.Note:sleepefficiency,wakeafterfirstdrowsinessandNREMsleepindogsindividuallyareindicatedwithcolouredlines;
mean values (± SE) are indicated with black
FIGURE 5 The effect of occasion on sleep latency 1 (a); and occasion-specific effects of dogs' sleep habits on sleep latency 2 (b)

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3.5 | Relative drowsiness duration
Occasion, age and dogs' sleep habits did not influence the relative
duration of drowsiness (all p > .05).
3.6 | Relative NREM duration
Occasion, age and dogs' sleep habits did not influence the relative
durationofNREMsleep(allp > .05).
3.7 | Relative REM duration
OccasiondidnotinfluencetherelativeREMduration(F2,66 = 1.005,
p = .372), but the dogs' sleep habits had a significant main effect
(F2,66 = 8.070, p=.006):OSAHdogs spent moretimeinREMsleep
compared with the RSAH dogs. A significant interaction of oc-
casion an d sleep habits o n relative REM dura tion was also foun d
(F2,66=3.265,p=.044);onoccasion1,OSAHdogsspentmoretime
inREMsl eepcomparedwithRSAHdogs(p<.001;Figure6).Agehad
no effec t (F2,65 = 0.321, p = .573).
As OSAH do gs did not seem to sh ow significant FN E, we ran
an additional model to assess the effect of occasion in relative
REMdurationonRSAH dogs.Wefoundamain effect ofoccasion
(F2,27=13.116,p< .001),thatis,RSAHdogshadlessrelativeREM
duration on occasion 1, compared with occasion 3 (p < .001), but no
difference between occasions 1 and 2 (p = .19), and between occa-
sions 1 and 3 (p=.92;Figure6b,blueline).
3.8 | REM latency 1
The Cox model proved tobesignificant in case of REM latency 1,
including an interaction of occasion and sleep habits (χ2
6 = 23.8;
p=.005;AIC = 11.8). Inthe subgroup of RSAHdogs we revealed
longer REM latency on occasion 1 compared with occasions 2
(exp(β)= 0.236,z=−2.19, p=.03)and3(exp(β) = 0.239, z=−2.34,
FIGURE 6 Occasion-specific effects of
dogs’sleephabitson(a)sleepefficiency
(mean±SE)and(b)relativerapideye
movement(REM)duration(mean±SE).
The effect of occasion on rarely sleeping
awayfromhome(RSAH)dogs(mean±SE)
(b). *p < .05; ***p < .0 01
FIGURE 7 Occasion-specificeffectsofdogs'sleephabitsonrapideyemovement(REM)latency1(a)and2(b)

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p=.02 ),but nodif f ere ncebet wee noccasions2and3(ex p(β) = 0.013,
z = 0.027, p=.99).Moreover,RSAHdogsreachedREMsleeplateron
occasion1,compared with OSAH dogs (exp(β) = 0.123, z = −3.24,
p=.001;Figure7a).Agehadnoeffect(exp(β) = 1.049, z= −0.53,
p = .59).
3.9 | REM latency 2
The Cox modelproved to besignificant in caseofREM latency 2,
including an interaction of occasion and sleep habits (χ2
6 = 20.29;
p = .002; A IC = 8.29). In the subg roup of RSAH dogs we n either
revealed difference between occasions 1 and 2 (exp(β) = 0.315,
z=−2.043,p=.10),norbetweenoccasions2and3(exp(β) = 0.951,
z=−0.100,p=.99),butdogstendedtohavelongerREMlatencyon
occasion 1, compared with occasion 3, although the effect did not
reachsignificance(exp(β) = 0.30 0, z = −1.93, p = .054). Moreover,
RSAHdogsreachedREMsleep lateronoccasion1,comparedwith
OSAHdogs(exp(β) = 0.180, z=−2.807,p=.005;Figure7b).Agehad
noeffect(exp(β) = 1.017, z=−0.20,p = .84).
4 | DISCUSSION
Acomplexpatternofdifferenceswasrevealedbetweensleepocca-
sions when conducting repeated afternoon sleep recordings in fam-
ily dogs. These adaptation effects on sleep macrostructure present
both similarities to and differences from the FNE phenomena de-
scribed in humans when conducting sleep recordings on consecutive
nights.Dogs experience (sleephabits)andagealso seemtoaffect
the sleep architecture, which parallels human findings.
Sleep occasion had an effect on dogs' sleep macrostructure;
however, contrar y to humans (Agnew et al., 1966; Le Bon e t al.,
2001), in dogs most significant differences were found not bet ween
the first two occasions, but between occasions 1 and 3. One possible
explanationforthemostly“second-night”insteadofthe“first-night”
effectmightbethevariation indogs' sleepinghabits (frequency of
sleeping away from home). These findings are in line with human
studies suggesting that a novel and potentially dangerous environ-
menthasadeterminantrole in sleepquality,for examplereducing
thetime spentinREMsleep(Lima et al., 2005).With NREM−REM
cycles,thelowandhigharousalthresholdsalternate,andREMsleep
with high arousal threshold results in low behavioural awareness
and high vulnerability to dangerous surroundings (Lima et al., 2005;
Voss,2004).Inhumanstudies,areverseversionoftheFNEhasalso
been reported; in contrast to healthy subjects, in whom the novel
environmentresultsinlowerqualityofsleep(Agnewetal.,1966),in
patients with insomnia the awareness of being watched had a pro-
motingeffectonsleepquality,presumablybecausetheenvironment
was interpreted as more secure (Hauri & Olmstead, 1989). Previous
studies on monkeys and laboratory rat s also found that sleep archi-
tecture (e.g. sleep efficiency, number of arousals and proportion of
time spent in REM) was sensitive to theperceived security of the
environment(e.g.laboratoryrats were exposedtoa laboratorycat
under var ious conditions ; Bert, Balz amo, Chase, & Pegra m, 1975;
Broughton, 1973). Our results regarding REM-related variables,
sleep latency and sleep efficiency suggest that dogs that rarely sleep
away from home are more sensitive to the new test situation (sleep-
ing in a new environment with electrodes) compared with dogs that
often sleep away from home.
However,this doesnot explain the lack of a linear habituation
process over the sleep occasions at the individual level. Dogs are
known to show individual-level variation that outnumbers humans'
by several magnitudes both in morphological and behavioural fea-
tures (McGreevy et al., 2013), as well as physiological parameters
(Báli ntetal.,2019).Suchindividualvariationsmightmaskalinearha-
bituation process, but as we did find differences between occasions
(1 and 3), it is unlikely that the noise caused by individual variability
would produce such a pattern.
Prior hum an FNE studies th at showed convincin g data on FNE
wereconductedon43(Agnewetal.,1966),26(LeBonetal.,2001)
and 12 (Lorenzo & Barbanoj, 2002) subjectson consecutive nights.
Our data were obtained from a sample of 24 dogs, which – in the
light of the remarkable individual differences – might not be large
enough. Moreover, due to practical reasons, our measurements were
conducted neither on three consecutive days nor during the night.
Althoughwe cannotexcludethat therelatively great time intervals
between the measurements interfered with our results, the present
data do not provide statistic al evidence for the ef fect of the elapsed
time between occasions. However, as our set-up followed that used
indogPSGstudies,theminimumtimeelapsedbetweenrecordings
was 1 week, thus our findings regarding this circumstance might not
beextendabletoasituationwhererecordingsareperformedoncon-
secutiv e nights. Lore nzo and Barban oj (2002) colle cted data on 12
nights, with a minimum of 1 month between three periods, and one
period consisted of4 consecutive nights. They foundthat the FNE
was only present in the first night of the first period (called the “very
first night”). This study is in line with earlier data obtained in a re-
searchimplyingthatFNEmightlas tformorethan1night,specifically,
REM -relatedparametersa remoresensitiveandtheirs tabilityprocess
might ext end up to 4 nights (L e Bon et al., 20 01). Interestin gly,w e
foundFNEinREMlatency,butmarkeddifferenceswerealsopresent
betwee n occasions 1 and 3. T hese findings s trengthen th e assumption
thatREM-relatedparametersneedmoresleepoccasionstostabilize.
Previous studies have already documented that several sleep pa-
rametersincluding EEGspectrum(Kis, Szakadát, Simor,etal.,2014)
and sleep spindles (Iotchev et al., 2019) co-vary with age. Here we
found that older dogs slept more and spent less time awake after the
first d rowsiness and NREM sl eep. The same mac rostructur al vari-
ables were also suggested in humans to be a marker of age-related
sleep changes (Carrier, Monk, Buysse, & Kupfer, 1997), but the rela-
tionship is opposite to the one we found in dogs. Human studies have
also documented anage-specific effect on FNE,for example it has
been reported that children and elderly need 3 instead of 2 nights
toadapt(Schmidt&Kaelbling,1971).Noindicationofaninteraction
between age and occasion was found here in dogs.

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9 of 10
REICHER E t al.
In sum, our findings indicate that in case of dogs' afternoon sleep
recordings, the ef fect of adaptation during the first occasion is con-
siderably smaller thanwhat weexpected based on the humanlit-
erature.However,thehumanFNEliteratureisbasedondata from
consecutive night-time recordings, we could not find any study in-
vestigating adapt ation effects for afternoon recordings in humans.
Most macrostructural differences in our study were detected be-
tween sleep occasions 1 and 3, which raises issues for future dog
PSGresearch.Alternatively,theadaptationsleepmightnotbenec-
essary (considering the few significant effects between occasions
1 and 2). It is, however, imperative to control for dogs' sleep habits.
Futureresearch–evaluatingtheeffectsof,forexampleattachment,
personality and sensitivity – needs to confirm that a simplified mea-
surement procedurewithoutadaptationand/ortheinclusionofex-
perienced dogs is indeed feasible.
IthasbeensuggestedthatthewayFNEmanifestsinhumansat
the individual level could be used as a diagnostic criterion in certain
sleep disorders and psychiatric conditions (e.g. a more pronounced
FNE can be o bserved in pati ents with idiopa thic nightmares ; Kis,
Szakadát,Simor,et al., 2014),whilealesspronouncedFNE ischar-
acteristicofpatientswithdepression(Toussaint,Luthringer,Staner,
Muzet,&MacHer,2000).Consideringthatthefamilydogisincreas-
inglyrecognizedasamodelforhumanneuropsychiatricconditions,
including obsessive-compulsive disorder (Ledford, 2016), autism
(Topál, Román, & Turcsán, 2019), and sleep disorders, like narco-
lepsy(Ripley,Fujiki, Okura,Mignot,& Nishino, 2001), sleep-disor-
dered breathing (Hinchliffe, Liu, & Ladlow, 2019), our findings might
open up new directions for the investigations of the links between
environmental factors and brain mechanisms underlying cognitive
(dys)functions,whichcouldhelpbetterunderstandcomplexdogand
even human phenotypes.
ACKNOWLEDGEMENTS
Financia l support was prov ided to V. R. and M. G. by Hun garian
ScientificResearchFund(OTKAK115862,OTKAK132372)andthe
HungarianAcademyofSciences(MTA01031);toA.K.byHungarian
ScientificResearchFund(OTKAFK128242),BIALFoundation(grant
no.169/16), János Bolyai Research Scholarship of the Hungarian
Academy of Sciences; to P. S. by Hungarian Scientific Research
Fund(NKFIFK128100)oftheNationalResearch,Developmentand
InnovationOffice;R.B.byHigherEducationInstitutionalExcellence
Program of the Ministry of Human Capacities in Hungary, within the
frameworkof the Neurology thematicprogramof the Semmelweis
University.TheauthorsthankÁdámMiklósiforhiscommentsonan
earlier versionofthe manuscript, andTamás Faragó forhishelpin
the statistical analyses.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
AUTHOR CONTRIBUTIONS
Conceptualization,V.R.,A.K.,P.S.,R.B.andM.G.;methodology,V.
R.,A.K.,P.S.,R.B.andM.G.;software,F.G.;validation,V.R.,A.K.
and M. G.; formal analysis, V. R. and A . K.; investigation, V. R.; data
curation V. R.; writing – original draft, V. R.; writing – review and
editing,allauthors;visualization, V. R.; supervision, M. G.;funding
acquisition,M.G.
ORCID
Vivien Reicher https://orcid.org/0000-0001-8285-826X
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