The effects of pramipexole on motivational vigour during a saccade task: a placebo-controlled study in healthy adults.
Dopamine
Eye movement
Eye tracking
Motivation
Pramipexole
Reward
Saccade
Vigour
Journal
Psychopharmacology
ISSN: 1432-2072
Titre abrégé: Psychopharmacology (Berl)
Pays: Germany
ID NLM: 7608025
Informations de publication
Date de publication:
18 Mar 2024
18 Mar 2024
Historique:
received:
13
02
2023
accepted:
28
02
2024
medline:
18
3
2024
pubmed:
18
3
2024
entrez:
18
3
2024
Statut:
aheadofprint
Résumé
Motivation allows us to energise actions when we expect reward and is reduced in depression. This effect, termed motivational vigour, has been proposed to rely on central dopamine, with dopaminergic agents showing promise in the treatment of depression. This suggests that dopaminergic agents might act to reduce depression by increasing the effects of reward or by helping energise actions. The aim of the current study was to investigate whether the dopamine agonist pramipexole enhanced motivational vigour during a rewarded saccade task. In addition, we asked whether the effects of pramipexole on vigour differ between reward contingent on performance and guaranteed reward. Healthy adult participants were randomised to receive either pramipexole (n = 19) or placebo (controls n = 18) for 18 days. The vigour of saccades was measured twice, once before the administration of study medication (Time 1) and after taking it for 12-15 days (Time 2). To separate motivation by contingency vs. reward, saccadic vigour was separately measured when (1) rewards were contingent on performance (2) delivered randomly with matched frequency, (3) when reward was guaranteed, (4) when reward was not present at all. Motivation increased response vigour, as expected. Relative to placebo, pramipexole also increased response vigour. However, there was no interaction, meaning that the effects of reward were not modulated by drug, and there was no differential drug effect on contingent vs. guaranteed rewards. The effect of pramipexole on vigour could not be explained by a speed/accuracy trade-off, nor by autonomic arousal as indexed by pupillary dilation. Chronic D2 stimulation increases general vigour, energising movements in healthy adults irrespective of extrinsic reward.
Identifiants
pubmed: 38494550
doi: 10.1007/s00213-024-06567-z
pii: 10.1007/s00213-024-06567-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Institute for Health and Care Research
ID : National Institute for Health and Care Research
Informations de copyright
© 2024. The Author(s).
Références
American Psychological Association (2013) Diagnostic and statistical Manual of Mental Disorder (DSM-5). American Psychological Association, Arlington
doi: 10.1176/appi.books.9780890425596
Bahill AT, Clark MR, Stark L (1975) The main sequence, a tool for studying human eye movements. Math Biosci 24:191–204. https://doi.org/10.1016/0025-5564(75)90075-9
doi: 10.1016/0025-5564(75)90075-9
Beck AT, Steer RA, Brown GK (1996) Manual for the Beck Depression Inventory-II. Psychological Corporation, San Antonio, TX
Beierholm U, Guitart-Masip M, Economides M et al (2013) Dopamine modulates reward-related Vigor. Neuropsychopharmacology 38:1495–1503. https://doi.org/10.1038/npp.2013.48
doi: 10.1038/npp.2013.48
pubmed: 23419875
pmcid: 3682144
Bodi N, Keri S, Nagy H et al (2009) Reward-learning and the novelty-seeking personality: a between- and within-subjects study of the effects of dopamine agonists on young Parkinson’s patients. Brain 132:2385–2395. https://doi.org/10.1093/brain/awp094
doi: 10.1093/brain/awp094
pubmed: 19416950
pmcid: 2766178
Chernoloz O, Mansari ME, Blier P (2009) Sustained Administration of Pramipexole modifies the spontaneous firing of dopamine, Norepinephrine, and serotonin neurons in the rat brain. Neuropsychopharmacology 34:651–661. https://doi.org/10.1038/npp.2008.114
doi: 10.1038/npp.2008.114
pubmed: 18688211
Chernoloz O, El Mansari M, Blier P (2012) Long-term administration of the dopamine D3/2 receptor agonist pramipexole increases dopamine and serotonin neurotransmission in the male rat forebrain. J Psychiatry Neurosci 37:113–121. https://doi.org/10.1503/jpn.110038
doi: 10.1503/jpn.110038
pubmed: 22023785
pmcid: 3297071
Chiew KS, Braver TS (2014) Dissociable influences of reward motivation and positive emotion on cognitive control. Cogn Affect Behav Neurosci 14:509–529. https://doi.org/10.3758/s13415-014-0280-0
doi: 10.3758/s13415-014-0280-0
pubmed: 24733296
pmcid: 4072919
Dooley M, Markham A (1998) Pramipexole: a review of its use in the management of early and advanced Parkinson’s Disease. Drugs Aging 12:495–514. https://doi.org/10.2165/00002512-199812060-00007
doi: 10.2165/00002512-199812060-00007
pubmed: 9638397
First MB, Williams JBW, Karg RS, Spitzer RL (2015) Structured clinical interview for DSM-5—Research Version (SCID-5 for DSM-5, Research Version; SCID-5-RV). American Psychiatric Association, Arlington
Gallant H, Vo A, Seergobin KN, MacDonald PA (2016) Pramipexole impairs stimulus-response learning in healthy young adults. Front Neurosci 10. https://doi.org/10.3389/fnins.2016.00374
Ghez C, Krakauer JW (2006) Back 33. The Organization of Movement
Grogan JP, Sandhu TR, Hu MT, Manohar SG (2020) Dopamine promotes instrumental motivation, but reduces reward-related vigour. eLife 9:e58321. https://doi.org/10.7554/eLife.58321
doi: 10.7554/eLife.58321
pubmed: 33001026
pmcid: 7599069
Haith AM, Pakpoor J, Krakauer JW (2016) Independence of Movement Preparation and Movement Initiation. J Neurosci 36:3007–3015. https://doi.org/10.1523/JNEUROSCI.3245-15.2016
doi: 10.1523/JNEUROSCI.3245-15.2016
pubmed: 26961954
pmcid: 6601759
Halahakoon DC, Kaltenboeck A, Martens M et al (2022) Pramipexole enhances reward learning by preserving Value estimates. Psychiatry and Clinical Psychology
Höflich A, Michenthaler P, Kasper S, Lanzenberger R (2019) Circuit Mechanisms of Reward, Anhedonia, and Depression. Int J Neuropsychopharmacol 22:105–118. https://doi.org/10.1093/ijnp/pyy081
doi: 10.1093/ijnp/pyy081
pubmed: 30239748
Horne SJ, Topp TE, Quigley L (2021) Depression and the willingness to expend cognitive and physical effort for rewards: a systematic review. Clin Psychol Rev 88:102065. https://doi.org/10.1016/j.cpr.2021.102065
doi: 10.1016/j.cpr.2021.102065
pubmed: 34274800
Kaltenboeck A, Halahakoon DC, Harmer CJ et al (2022) Enhanced taste recognition following Subacute Treatment with the dopamine D2/D3 receptor agonist pramipexole in healthy volunteers. Int J Neuropsychopharmacol 25:720–726. https://doi.org/10.1093/ijnp/pyac030
doi: 10.1093/ijnp/pyac030
pubmed: 35605609
pmcid: 9515131
Liberg B, Rahm C (2015) The functional anatomy of Psychomotor disturbances in Major Depressive Disorder. Front Psychiatry 6. https://doi.org/10.3389/fpsyt.2015.00034
Manohar SG, Chong TT-J, Apps MAJ et al (2015) Reward pays the cost of noise reduction in Motor and Cognitive Control. Curr Biol 25:1707–1716. https://doi.org/10.1016/j.cub.2015.05.038
doi: 10.1016/j.cub.2015.05.038
pubmed: 26096975
pmcid: 4557747
Manohar SG, Finzi RD, Drew D, Husain M (2017) Distinct Motivational effects of Contingent and noncontingent rewards. Psychol Sci 28:1016–1026. https://doi.org/10.1177/0956797617693326
doi: 10.1177/0956797617693326
pubmed: 28488927
Martens MAG, Kaltenboeck A, Halahakoon DC et al (2021) An Experimental Medicine Investigation of the effects of Subacute Pramipexole Treatment on Emotional Information Processing in healthy volunteers. Pharmaceuticals 14:800. https://doi.org/10.3390/ph14080800
doi: 10.3390/ph14080800
pubmed: 34451897
pmcid: 8401454
Mazzoni P, Hristova A, Krakauer JW (2007) Why don’t we move faster? Parkinson’s Disease, Movement Vigor, and Implicit Motivation. J Neurosci 27:7105–7116. https://doi.org/10.1523/JNEUROSCI.0264-07.2007
doi: 10.1523/JNEUROSCI.0264-07.2007
pubmed: 17611263
pmcid: 6794577
Niv Y, Daw ND, Joel D, Dayan P (2007) Tonic dopamine: opportunity costs and the control of response vigor. Psychopharmacology 191:507–520. https://doi.org/10.1007/s00213-006-0502-4
doi: 10.1007/s00213-006-0502-4
pubmed: 17031711
Norbury A, Manohar S, Rogers RD, Husain M M (2013) Dopamine modulates risk-taking as a function of baseline sensation-seeking trait. J Neurosci 33:12982–12986. https://doi.org/10.1523/jneurosci.5587-12.2013
doi: 10.1523/jneurosci.5587-12.2013
pubmed: 23926253
pmcid: 3735881
Pizzagalli DA, Evins AE, Schetter EC et al (2008) Single dose of a dopamine agonist impairs reinforcement learning in humans: behavioral evidence from a laboratory-based measure of reward responsiveness. Psychopharmacology 196:221–232. https://doi.org/10.1007/s00213-007-0957-y
doi: 10.1007/s00213-007-0957-y
pubmed: 17909750
Reppert TR, Lempert KM, Glimcher PW, Shadmehr R (2015) Modulation of Saccade Vigor during Value-based decision making. J Neurosci 35:15369–15378. https://doi.org/10.1523/JNEUROSCI.2621-15.2015
doi: 10.1523/JNEUROSCI.2621-15.2015
pubmed: 26586823
pmcid: 4649007
Riba J, Krämer UM, Heldmann M, Richter S, Münte TF (2008) Dopamine agonist increases risk taking but blunts reward-related brain activity. PLoS ONE 3:e2479. https://doi.org/10.1371/journal.pone.0002479
doi: 10.1371/journal.pone.0002479
pubmed: 18575579
pmcid: 2423613
Santesso DL, Evins AE, Frank MJ et al (2009) Single dose of a dopamine agonist impairs reinforcement learning in humans: evidence from event-related potentials and computational modeling of striatal-cortical function. Hum Brain Mapp 30:1963–1976. https://doi.org/10.1002/hbm.20642
doi: 10.1002/hbm.20642
pubmed: 18726908
Satterthwaite TD, Green L, Myerson J et al (2007) Dissociable but inter-related systems of cognitive control and reward during decision making: evidence from pupillometry and event-related fMRI. NeuroImage 37:1017–1031. https://doi.org/10.1016/j.neuroimage.2007.04.066
doi: 10.1016/j.neuroimage.2007.04.066
pubmed: 17632014
Schück S, Bentué-Ferrer D, Kleinermans D, Reymann J-M, Polard E, Gandon J-M, Allain H (2002) Psychomotor and cognitive effects of piribedil, a dopamine agonist, in young healthy volunteers. Fundam Clin Pharmacol 16:57–65. https://doi.org/10.1046/j.1472-8206.2002.00070.x
doi: 10.1046/j.1472-8206.2002.00070.x
pubmed: 11903513
Shelton RC, Tomarken AJ (2001) Can Recovery from Depression be Achieved? Psychiatr Serv 52:1469–1478. https://doi.org/10.1176/appi.ps.52.11.1469
doi: 10.1176/appi.ps.52.11.1469
pubmed: 11684742
Takikawa Y, Kawagoe R, Hikosaka O (2002) Reward-dependent spatial selectivity of anticipatory activity in Monkey Caudate neurons. J Neurophysiol 87:508–515. https://doi.org/10.1152/jn.00288.2001
doi: 10.1152/jn.00288.2001
pubmed: 11784766
Tundo A, Filippis R, De Crescenzo F (2019) Pramipexole in the treatment of unipolar and bipolar depression. A systematic review and meta-analysis. Acta Psychiatr Scand 140:116–125. https://doi.org/10.1111/acps.13055
doi: 10.1111/acps.13055
pubmed: 31111467
Whitton AE, Reinen JM, Slifstein M et al (2020) Baseline reward processing and ventrostriatal dopamine function are associated with pramipexole response in depression. Brain 143:701–710. https://doi.org/10.1093/brain/awaa002
doi: 10.1093/brain/awaa002
pubmed: 32040562
pmcid: 7009463