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University of Groningen
Serotonin manipulations and social behaviorHogenelst, Koen
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Summary
153
SUMMARY
This Doctoral Thesis is concerned with the role of the neurotransmitter serotonin in the
regulation of social behavior. Upon examining the literature, I found that previous exper-
imental studies on the effects of serotonin manipulations on human social behavior most-
ly took place in the laboratory. While the results of these studies tend to suggest that
changes in brain serotonin lead to changes in aspects of social functioning, their rele-
vance for real-life interactions often remained unclear. Only two past studies have com-
bined serotonin manipulation with the ecological momentary assessment of social inter-
actions. Both studies, conducted in healthy never-depressed individuals, found that tryp-
tophan administration, which increases brain serotonin, reduces quarrelsomeness, and
may also enhance agreeableness. As depression has been associated with alterations in
brain serotonin and in social functioning, laboratory and ecological momentary assess-
ment studies on the effects of serotonin manipulations on social functioning may have
implications for individuals at risk for depression. I extended previous work by (a) study-
ing individuals with a family history of depression, and (b) using outcome measures with
improved ecological validity.
I conducted a laboratory study in never-depressed individuals with (FH+) and
without (FH-) a family history of depression on the effects of acute tryptophan depletion
(ATD), which temporarily reduces brain serotonin, on multiple measures of social func-
tioning, selected for their high ecological validity (Study 1). In FH+ individuals I also
conducted an ecological momentary assessment study on the effects of tryptophan admin-
istration on quarrelsomeness, agreeableness, dominance, and submissiveness in everyday
life (Study 2).
In Study 1, ATD reduced the time individuals waited before speaking, but oth-
erwise did not significantly alter social speech. Moreover, ATD did not significantly alter
empathic accuracy, behavioral mimicry, or mood in either family history group. In Study
2, tryptophan administration improved mood during social interactions. Further, taking
tryptophan resulted in an increase in quarrelsomeness and a decrease in agreeableness,
specifically during social interactions at home. Furthermore, negative social cognitions
appeared to decrease over the course of the study. In sum, an acute lowering of brain
serotonin had few effects on social functioning (assessed more naturalistically compared
to previous studies) and a longer-term increase in serotonin had effects on social behavior
that were unexpected.
The findings of Study 1 imply that an acute lowering of serotonin has few if any
effects on social functioning in never-depressed individuals. The findings of Study 2
Summary
154
imply that increasing serotonin might enhance quarrelsomeness and reduce agreeableness
in some depressed patients, even when it may reduce quarrelsomeness and enhance
agreeableness in other patients and in both groups be associated with an improvement in
mood. In this Doctoral Thesis I argue that short-term decreases in brain serotonin may
have no immediate impact on social functioning in previously depressed patients; I elabo-
rate on the idea that antidepressants may work by altering depressed patients’ social be-
havior and by improving mood; and I propose that the role of serotonin and other neuro-
transmitters in regulating real-life social behavior deserves more attention in the fields of
psychiatry and clinical psychology.
Samenvatting
155
SAMENVATTING
Dit Proefschrift beschrijft de rol van de neurotransmitter serotonine in de regulering van
sociaal gedrag. Bij het bestuderen van de literatuur constateerde ik dat eerdere experi-
mentele studies naar de effecten van serotonine manipulaties op humaan sociaal gedrag
voornamelijk in het laboratorium plaatsvonden. De resultaten van deze studies suggere-
ren dat veranderingen in serotonine in de hersenen leiden tot veranderingen in aspecten
van sociaal functioneren, maar de relevantie voor dagelijkse interacties blijft vaak ondui-
delijk. Slechts twee eerdere studies hebben serotonine manipulatie gecombineerd met de
ecologische momentane assessment van dagelijkse sociale interacties. Beide studies,
uitgevoerd bij gezonde niet-depressieve individuen, vonden dat inname van tryptofaan
om serotonine te verhogen, onvriendelijk gedrag verlaagde en vriendelijk gedrag kon
verhogen. Aangezien depressie geassocieerd wordt met veranderingen in serotonine in de
hersenen en in sociaal functioneren, hebben laboratorium- en ecologische momentane
assessment studies naar de effecten van serotonine manipulaties op het sociaal functione-
ren mogelijk implicaties voor individuen met een verhoogd risico op depressie. Ik breid-
de eerder onderzoek uit door (a) studies te doen bij individuen met een familie geschie-
denis van depressie en (b) door gebruik te maken van methodes met verbeterde ecolo-
gische validiteit.
Ik heb een laboratorium studie uitgevoerd bij niet-depressieve individuen met
(FH+) en zonder (FH-) een familie geschiedenis van depressie over de effecten van acute
tryptofaan depletie (ATD), wat voor een tijdelijke verlaging van serotonine in de herse-
nen zorgt, op meerdere maten van sociaal functioneren met hoge ecologische validiteit
(Studie 1). Bij FH+ individuen heb ik daarnaast een ecologische momentane assessment-
studie uitgevoerd naar de effecten van tryptofaantoediening op onvriendelijk, vriendelijk,
dominant en onderdanig gedrag in het dagelijks leven (Studie 2).
In Studie 1 verkortte ATD de tijd waarin individuen wachtten alvorens te spre-
ken, maar had verder geen significante effecten op sociale spraak. Ook veroorzaakte
ATD geen significante veranderingen in empathische nauwkeurigheid, mimiek van ge-
drag of stemming. In Studie 2 verbeterde tryptofaantoediening de stemming tijdens socia-
le interacties. Verder zorgde het nemen van tryptofaan voor een toename in onvriendelijk
gedrag en een afname in vriendelijk gedrag, specifiek tijdens sociale interacties die thuis
plaatsvonden. Verder bleken negatieve sociale cognities (zoals ‘niemand begrijpt me’) in
de loop van de studie af te nemen. Kortom, een acute afname van serotonine in de herse-
nen had weinig invloed op het sociaal functioneren (gemeten met ecologisch meer valide
Samenvatting
156
methoden ten opzichte van eerdere studies)en een toename van serotonine over langere
tijd had effecten op sociaal gedrag die onverwacht waren.
De bevindingen van Studie 1 impliceren dat een acute verlaging van serotonine
weinig of geen invloed heeft op het sociaal functioneren van individuen zonder persoon-
lijke geschiedenis van depressie. De bevindingen van Studie 2 wijzen op de mogelijkheid
dat een toename van serotonine mogelijk onvriendelijkheid verhoogt en vriendelijkheid
verlaagt bij sommige depressieve patiënten, zelfs als het onvriendelijkheid kan verlagen
en vriendelijkheid kan verhogen in andere patiënten, en in beide groepen geassocieerd is
met een verbetering van de stemming. In dit Proefschrift beargumenteer ik dat een acute
verlaging van serotonine in de hersenen mogelijk geen direct effect heeft op het sociaal
functioneren in patiënten met een geschiedenis van depressie; ik bouw voort op het idee
dat antidepressiva mogelijk werken door sociaal gedrag van depressieve patiënten te
veranderen en stemming te verbeteren; en ik stel voor dat de rol van serotonine en andere
neurotransmitters in het reguleren van dagelijks sociaal gedrag meer aandacht verdient in
de psychiatrie en klinische psychologie.
Dankwoord
157
DANKWOORD
Het beginnen en doorzetten van een promotieonderzoek en het afronden ervan in de vorm
van een proefschrift vervult me met trots. Het is een bijzonder en zeer leerzaam avontuur,
met vele memorabele momenten.
Promoveren kan nogal solitair zijn, wat tegen mijn natuur is en enigszins iro-
nisch, gezien het onderwerp van dit proefschrift. Maar door samen te werken (essentieel
gezien het interdisciplinaire karakter van mijn onderzoek) en de juiste begeleiding kom je
tot een goed eindresultaat. Daarnaast was voor mij ontspanning met vrienden en familie
erg belangrijk. Een dankwoord aan collega’s, vrienden en familie is dan ook zeer op zijn
plaats.
Op de eerste plaats wil ik mijn begeleidster Marije aan het Rot bedanken. Beste Marije,
jij hebt me de kans geboden om te promoveren. Ik besef me dat ik geluk heb gehad met je
deskundigheid, je toegankelijkheid en je duidelijkheid. Je bent integer, gemotiveerd en
staat stevig in je onderzoeksschoenen. Hoewel het voor mij niet altijd eenvoudig was,
heeft je strakke begeleiding significant bijgedragen aan dit proefschrift. Bovenal hebben
je vele adviezen, inzichten en stimulansen me laten leren en groeien als wetenschapper en
ben ik erkentelijk voor de verantwoordelijkheid en het vertrouwen dat je me al die tijd
hebt gegeven.
Mijn promotoren Peter de Jong en Robert Schoevers wil ik uiteraard ook bedanken. Pe-
ter, net als vele collega’s sta ik versteld van je scherpte, snelheid waarmee je stukken
leest en becommentarieert (zelfs al is het enigszins buiten je eigen onderzoeksgebied) en
je passie voor je vak. Ik ben dankbaar voor je openheid en de inhoudelijke discussies die
we hebben gehad en waardeer je vriendelijke en optimistische persoonlijkheid. Robert,
ook jij was vaak optimistisch en als een soort mentor voor me, iets wat ik in ieder geval
zeer op prijs stelde. Je was betrokken en ik heb onze gesprekken altijd als erg aangenaam
ervaren, waarin ik veel geleerd heb van je wetenschappelijke en klinisch inzicht.
I would further like to express my appreciation to the assessment committee, prof. dr.
Catherine Harmer, prof. dr. Willem van der Does and prof. dr. Johan (Hans) Ormel, for
taking the time to read, assess, and comment on my thesis.
I would also like to thank my co-authors for some of the chapters. Tassos, it was a great
pleasure getting to know you, discussing my project with you, designing a way to tackle
Dankwoord
158
the speech analysis part, and write a paper together. Pontus and Barbara, I appreciate our
discussions about the assessment of mimicry as well as your comments on the paper.
Ido en Fred, bedankt voor jullie bijdrage aan dit proefschrift in de vorm van bio-
chemische expertise, laboratorium analyses en advies voor de beschrijving van deze ana-
lyses in de papers (hoofdstukken 5 en 6).
Ook wil ik graag alle deelnemers aan de studies bedanken. Voor een aantal van jullie was
deelname niet altijd even makkelijk, maar ik ben zeer dankbaar dat jullie allen dat deden.
Tijdens mijn promotieonderzoek heb ik met veel plezier een aantal studenten begeleid.
Als masterstudent hebben Annika, Kristina en Beatrice een belangrijke bedrage geleverd
aan het verzamelen dan wel verwerken van de data. Als bachelor student hebben Minita,
Lisanne, Elise, Sophie, Pia en Sofie me geholpen met studie opzet, data verzameling en
verwerking. Allemaal hartelijk dank voor jullie inzet. Het overdragen van kennis heb ik
altijd leuk gevonden en gaf mij het inzicht hoeveel ik heb geleerd tijdens mijn opleiding
en promotie-traject.
Dan de ‘stille’ krachten. Zoals ze in het voetbal zeggen: “je ziet hem nauwelijks, maar
zonder hem merk je pas hoe onmisbaar hij is”. Dat geldt zeker voor een aantal personen
waarvan ik technische ondersteuning heb gehad. Eise Hoekstra, bedankt voor je vele uren
aan programmeerwerk. Het was altijd leuk om bij je langs te komen. Mark Span, je R
scripts voor de EAT waren goud waard. Verder blijft me vooral je eigenaardigheid en
genialiteit bij. Pieter Zandbergen, hoeveel mailtjes met verzoeken voor apparatuur ik jou
wel niet heb gestuurd. Altijd was je vriendelijk en behulpzaam. Rock on! Verder wil ik
Remco en Bert bedanken voor de altijd vriendelijke technische ondersteuning en Jaap
voor de ontwikkeling van de BluesClues website. Judith, bedankt voor je hulp bij de
werving van deelnemers. Ingrid, Jolanda, Josje en Lucia, bedankt voor de ondersteuning
vanuit het secretariaat. Voor het meten van hartslag had ik niet zonder Harriëte en Ben
gekund, dank daarvoor. Tot slot wil ik Kor bedanken voor de samenwerking met de prik-
dienst van het UMCG, Albert voor de coördinatie van alle bloedsamples en Barbara als
verantwoordelijke van de apotheek.
Graag wil ik alle KP collega’s bedanken voor de inhoudelijke discussies, fijne borrels in
de minnaar, de avondjes met gezelschapsspellen, de quizzen en de afdelingsuitjes. Op de
afdeling heerst een zeer prettige sfeer, dat besef je des te meer als je er niet meer bent.
Mijn paranimfen, Renate en Charmaine. Twee hele leuke, knappe en slimme
dames. Jullie reactie toen ik vroeg of jullie mijn paranimfen wilden zijn zal ik nooit verg-
eten. Renate, we begonnen samen op één kamer. Het klikte meteen, de humor zat er goed
Dankwoord
159
in en er werd een spaarplan voor de Librije opgezet. Ik denk met veel plezier terug aan
onze kantoorhumor. Ook deelden we smart als er iets tegenzat. Soms heb je gewoon een
heel zwaar leven. En dan Charmaine, waar zal ik beginnen. Ruim een jaar deelden we een
kantoor. We konden het daarvoor al goed vinden en dat werd alleen maar beter. Je hebt
een heel groot (sociaal) hart met ruimte voor iedereen lijkt het. Ook werk je erg hard om
succesvol te zijn, en met resultaat. Ik heb veel aan je gehad op wetenschappelijk gebied.
Daarnaast waardeer ik de ‘interessante’ gesprekken op maandagochtend. Bovenal vind ik
het bijzonder dat ik je altijd om advies of hulp kan vragen. En dan is Johan er nog. Johan,
je bent uniek en een fijne collega en bedankt voor je brede rug zodat ik uit de wind kon
fietsen als ik weer eens stuk zat.
Buiten de afdeling zijn er nog een aantal collega-vrienden die mijn tijd in Groningen
extra kleur hebben gegeven. Gert, jij verleidde me weer naar Groningen te komen, atten-
deerde me op een promotie-plek en bent altijd bereid om te helpen (het inspringen als
derde paranimf is slechts een van je vele daden). We hebben vele mooie avonden beleefd.
Vaak was Wouter dan ook van de partij. Wouter, ik heb je leren kennen als een hele toffe
en sociale jongen met als hoogtepunt het samen beleven van de Stones op Pinkpop! Een
derde topper is Jan, met wie ik vaak onder het genot van een goed glas bier een gesprek
van man tot man had over vrouwen, voetbal en andere belangrijke zaken.
Het afronden van een promotieonderzoek is de kroon op mijn lerende en studerende le-
vensfase. In dat licht wil ik me richten tot Jos en Betty. Pap en Mam, dat ik dit heb be-
reikt heb ik toch ook in grote mate aan jullie te danken. Jullie hebben mij, Rik en Wout
een fijne en stabiele opvoeding gegeven en altijd gezegd dat als je ‘de hersens’ hebt, je er
wat mee moet doen. We nemen het vaak voor lief, maar het getuigt van veel onzelfzuch-
tigheid, doorzettingsvermogen en liefde dat jullie alles in het werk zetten om, in tegen-
stelling tot jullie eigen opvoeding, ons de mogelijkheden te bieden om te ontwikkelen
zoals we dat willen. Muito obrigado!
Het beste bewaar ik voor het laatst. Marijn, wat ben je lief, wijs, bijzonder en perfect voor
mij. Bedankt dat je me altijd zo gesteund hebt tijdens mijn promotie traject, door te luis-
teren, geduldig te zijn, constructief mee te denken en te helpen relativeren. Het was heer-
lijk om je elk weekend weer te zien, maar tegelijkertijd was het afscheid nemen niet leuk
en reizen vermoeiend. Gelukkig wonen we nu samen en ik vind het geweldig. Dat heeft
me het afgelopen jaar, waarin het nog behoorlijk doorzetten was, veel energie gegeven. Ik
wil met jou geen wetenschappelijke discussies, ik wil je liefhebben, samen plezier ma-
ken, de wereld zien en lekker eten. Ik vind het geweldig hoe je bent en dat je er bent.
About the author
161
ABOUT THE AUTHOR
Curriculum vitae
Koen Hogenelst was born on June 7th
1985 in Winterswijk, the
Netherlands. After completing high school in 2003 he moved to
Groningen to study Human Movement Sciences at the University
of Groningen. During the bachelor his fascination for the brain and
neurobiology emerged. Thus, after receiving his BSc degree in the
summer of 2006, he started the Research Master Behavioural and
Cognitive Neurosciences (BCN) (Track: clinical and molecular
neuroscience). In his first internship, he studied the effect of sleep
deprivation on memory in mice, under the supervision of Robert Havekes and Peter
Meerlo, resulting in his first scientific co-authorship. For a second internship, supported
by several funds including the Dutch Brain Foundation, Koen went to Prof. Klaus Miczek
at Tufts University in Boston, MA, USA. In Boston, Koen studied stress-sensitization,
drug abuse, and drug addiction in rats, which led to a second scientific co-authorship.
After graduating the Research Master in 2008, Koen moved to Amsterdam and worked at
a contract research organization for a year. This helped to realize his travel plans for East-
Africa (sept 2009-jan 2010). In spring 2010, Koen applied for the PhD position entitled:
Mood, Serotonin, and Social Behavior, and was hired to start in September 2010 under
the supervision of Dr. Marije aan het Rot. For over four years, Koen studied the role of
serotonin in social behavior in individuals at familial risk for depression (this Thesis). He
won the BCN poster prize in 2013 and presented his research to the public at the Night of
Arts and Science, June 2013, Groningen. Next to his PhD work, Koen was involved in
education of Psychology students at the University of Groningen and guided many bache-
lor and master students. Now, he lives with his girlfriend in Utrecht, the Netherlands.
Since January 2015 he works at TNO, a Dutch applied science institute, where he is in-
volved in several applied science projects related to stress-monitoring, personalized
health advice, and nutrition & cognition.
About the author
162
List of publications
Hogenelst, K., Sarampalis, A., Leander, N.P., Müller, B.C.N., Schoevers, R.A., aan het Rot, M.
(2015). The effects of acute tryptophan depletion on speech and behavioral mimicry in indi-
viduals at familial risk for depression. Journal of Psychopharmacology. Accepted
Hogenelst, K., Schoevers, R.A., Kema, I.P., Sweep, F.C., aan het Rot, M. (2015). Empathic accura-
cy and oxytocin after tryptophan depletion in adults at risk for depression. Psychopharmaco-
logy. doi:10.1007/s00213-015-4093-9
Hogenelst, K., Schoevers, R. A., & aan het Rot, M. (2015). The effects of tryptophan on everyday
interpersonal encounters and social cognitions in individuals with a family history of depres-
sion. The International Journal of Neuropsychopharmacology / Official Scientific Journal of
the Collegium Internationale Neuropsychopharmacologicum (CINP), 18(8). doi:pyv012
Hogenelst, K., Schoevers, R. A., & aan het Rot, M. (2015). Studying the neurobiology of human
social interaction: Making the case for ecological validity. Social Neuroscience 10(3), 219-
229. doi:10.1080/17470919.2014.994786
aan het Rot, M., & Hogenelst, K. (2014). The influence of affective empathy and autism spectrum
traits on empathic accuracy. PloS One, 9(6), e98436. doi:10.1371/journal.pone.0098436
aan het Rot, M., Hogenelst, K., & Gesing, C. M. (2014). Communal and agentic behaviour in re-
sponse to facial emotion expressions. British Journal of Psychology, 105(2), 173-186.
doi:10.1111/bjop.12029
aan het Rot, M., Hogenelst, K., & Moskowitz, D. S. (2013). Comparability of the social behavior
inventory in English and Dutch. Journal of Personality Assessment, 95(5), 500-505.
doi:10.1080/00223891.2013.775138
aan het Rot, M., Hogenelst, K., & Schoevers, R. A. (2012). Mood disorders in everyday life: A
systematic review of experience sampling and ecological momentary assessment studies.
Clinical Psychology Review, 32(6), 510-523. 10.1016/j.cpr.2012.05.007
Cruz, F. C., Quadros, I. M., Hogenelst, K., Planeta, C. S., & Miczek, K. A. (2011). Social defeat
stress in rats: Escalation of cocaine and "speedball" binge self-administration, but not heroin.
Psychopharmacology, 215(1), 165-175. 10.1007/s00213-010-2139-6
Hagewoud, R., Havekes, R., Tiba, P. A., Novati, A., Hogenelst, K., Weinreder, P., ... Meerlo, P.
(2010). Coping with Sleep Deprivation: Shifts in Regional Brain Activity and Learning Strat-
egy. Sleep, 33(11), 1465-1473.
