Een kopje voor het geheugen, twee voor de smaak
Wat als we allemaal sneller konden leren? En wat als de sleutel naar sneller leren in iedereens keuken ligt? Het klinkt moeilijk te geloven, maar één enkele kopje koffie na een leersessie kan je geheugen een meetbare boost geven!
Wat er in je hoofd gebeurt als je leert
Onze hersenen worden vaak gezien als indrukwekkende computers, in staat om een enorme hoeveelheid aan informatie te verwerken en op te slaan. Wanneer we iets leren, slaan we nieuwe informatie op doordat hersencellen nieuwe verbindingen met elkaar maken, wat leidt tot een complex netwerk van verbonden hersencellen. Dit is grotendeels een chemisch proces dat berust op neurotransmitters, chemische signaalstoffen in het lichaam die zorgen voor de communicatie tussen zenuwcellen. Belangrijk hierbij is dat dit proces zich verderzet nadat een herinnering is gevormd, een verschijnsel dat geheugenconsolidatie wordt genoemd. Bijvoorbeeld, als je een nieuwe melodie op de piano leert, blijven jouw hersenen nog lang bezig met deze nieuwe informatie te verankeren in het langetermijngeheugen, zelfs nadat je gestopt bent met oefenen. Maar wat heeft dit nu allemaal met koffie te maken?
Breng mij een koffie voordat ik in een geit verander
Cafeïne is de meest verbruikte psychoactieve stof ter wereld. Dat zal voor de meesten geen verrassend weetje zijn, 80% van de wereldbevolking verbruikt namelijk elke dag een cafeïne houdend product. Denk bijvoorbeeld maar aan hoe je tegenwoordig overal wel een koffiezaak kan vinden. Daarnaast is cafeïne van nature aanwezig in vele producten zoals koffie, thee, of chocolade, en wordt het vaak toegevoegd aan frisdranken, energiedranken, en zelfs pijnstillers.
Het wijdverspreid gebruik van cafeïne is zeker geen modern fenomeen, zelfs Bach componeerde al tussen 1732 en 1735 zijn beroemde "Kaffeekantate" waarin hij dramatisch waarschuwt: "Als ik niet driemaal daags mijn kopje koffie mag drinken, verander ik tot mijn verdriet in een verdord stukje geitenvlees".
De psychoactieve effecten van cafeïne zijn daarom ook al eeuwenlang bekend: meer energie, verhoogde concentratie, verbeterde stemming. Deze effecten ontstaan doordat cafeïne voornamelijk de werking van adenosine blokkeert. Omdat adenosine een neurotransmitter is die vermoeidheid opwekt, voelen we ons energiek als de werking van adenosine wordt tegengehouden. Anders gezegd: “een beetje moe, drink Nalu”.
Naast de directe werking op adenosine, heeft cafeïne ook een indirecte werking op de vrijgave van andere neurotransmitters, waaronder glutamaat, dopamine, en noradrenaline. Deze neurotransmitters, en vooral glutamaat, spelen een essentiële rol bij het vormen van nieuwe herinneringen. Omdat cafeïne de vrijgave van deze stoffen verhoogt in hersenregio’s die sterk geassocieerd worden met het geheugen, zouden we verwachten dat cafeïne een invloed heeft op het opslaan van nieuwe informatie. Toch heeft eerder onderzoek getoond dat cafeïne geen effect heeft op het geheugen. Echter, bij bijna alle eerdere studies werd cafeïne toegediend vóór of tijdens een leersessie. Met andere woorden, de invloed van cafeïne op het consolidatieproces was tot nu toe nauwelijks bestudeerd, en dat is juist wat ik tijdens mijn thesis heb onderzocht.
Liever een cappuccino dan een dubbele espresso
Om eindelijk achter te komen of al die kopjes koffie tijdens de examenperiodes meer goed dan kwaad deden, heb ik 30 participanten verzameld voor een experiment. De participanten leerden een specifieke volgorde toetsen op een toetsenbord en kregen daarna een capsule met 0mg (placebo), 80mg (ongeveer één kopje koffie) of 240mg cafeïne (ongeveer drie kopjes). Een dag later voerden ze de sequentie opnieuw uit. Door te kijken hoe hun reactietijden veranderden tussen de twee dagen, kon ik meten hoe goed de geleerde sequentie was blijven hangen. Het sneller kunnen voltooien van de sequentie betekent namelijk dat de volgorde beter werd onthouden. Belangrijker nog, de verschillen tussen de groepen toonden of cafeïne het consolideren van deze nieuwe informatie beïnvloedde.
In het kort, ja cafeïne kan helpen met nieuwe informatie beter te onthouden! Het effect is echter subtiel, maar statistisch significant, en geldt bovendien enkel voor kleine porties. De 80mg cafeïnegroep was namelijk ongeveer 2% sneller tussen dagen vergeleken met placebo, maar de grote portie van 240mg bood geen extra voordeel. Als het gaat om de interactie tussen cafeïne en geheugen, blijkt minder uiteindelijk dus meer te zijn. Hoewel het verschil klein is, zou het effect zich mogelijks kunnen opstapelen. Bijvoorbeeld, iemand die telkens na het leren een kopje koffie neemt, bouwt stukje bij beetje een voordeel op, en 2% per keer kan na een paar sessies een opvallend verschil creëren. Daarnaast is zo’n laagdrempelige interventie makkelijk toe te passen en kan in theorie zelfs een kleine steun bieden bij fysiek of cognitief herstel.
Gemiddelde reactietijden per groep en dag. Een grotere daling tussen dag 1 en 2 bij de 80mg groep laat zien dat één kopje koffie na het leren het geheugen subtiel kan versterken
Of je nu studeert, een instrument oefent, of een nieuwe vaardigheid onder de knie probeert te krijgen, dit eenvoudig trucje kan je dus een subtiele boost geven. De volgende keer dat je een moeilijke melodie of een complex concept moet leren: wacht tot na het leren en drink dan pas die espresso, je geheugen zal je dankbaar zijn!
Bibliografie
Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19(6), 716–723. https://doi.org/10.1109/tac.1974.1100705
Albouy, G., King, B. R., Maquet, P., & Doyon, J. (2013). Hippocampus and striatum: Dynamics and interaction during acquisition and sleep‐related motor sequence memory consolidation. Hippocampus, 23(11), 985–1004. https://doi.org/10.1002/hipo.22183
Allain, H., Lieury, A., Quemener, V., Thomas, V., Reymann, J., & Gandon, J. (1995). Procedural memory and Parkinson’s Disease. Dementia and Geriatric Cognitive Disorders, 6(3), 174–178. https://doi.org/10.1159/000106942
Allison, P. (2012, September 10). When can you safely ignore multicollinearity? Statistical Horizons. Retrieved August 27, 2024, from https://statisticalhorizons.com/multicollinearity/
Anderson, E. N. (2003). Caffeine and culture. In W. Jankowiak & D. Bradburd (Eds.), Drugs, labor and colonial expansion (1st ed., pp. 159–177). The University of Arizona Press. https://doi.org/10.2307/j.ctv2rcnqn9
Angelucci, M., Cesário, C., Hiroi, R., Rosalen, P., & Da Cunha, C. (2002). Effects of caffeine on learning and memory in rats tested in the Morris water maze. Brazilian Journal of Medical and Biological Research, 35(10), 1201–1208. https://doi.org/10.1590/s0100-879x2002001000013
Arab, L., & Blumberg, J. B. (2008). Introduction to the proceedings of the Fourth International Scientific Symposium on Tea and Human Health. The Journal of Nutrition, 138(8), 1526S-1528S. https://doi.org/10.1093/jn/138.8.1526s
Arnaud, M. J. (2010). Pharmacokinetics and metabolism of natural methylxanthines in animal and man. In B. B. Fredholm (Ed.), Methylxanthines. Handbook of experimental pharmacology (Vol. 200, pp. 33–91). Springer. https://doi.org/10.1007/978-3-642-13443-2_3
Avissar, M., Powell, F., Ilieva, I., Respino, M., Gunning, F. M., Liston, C., & Dubin, M. J. (2017). Functional connectivity of the left DLPFC to striatum predicts treatment response of depression to TMS. Brain Stimulation, 10(5), 919–925. https://doi.org/10.1016/j.brs.2017.07.002
Baird, A., & Samson, S. (2009). Memory for music in Alzheimer’s disease: Unforgettable? Neuropsychology Review, 19(1), 85–101. https://doi.org/10.1007/s11065-009-9085-2
Banakar, M., Moayedi, S., Shamsoddin, E., Vahedi, Z., Banakar, M. H., Mousavi, S. M., Rokaya, D., & Lankarani, K. B. (2022). Chewing gums as a drug delivery approach for oral health. International Journal of Dentistry, 2022, 1–10. https://doi.org/10.1155/2022/9430988
Barone, J. J., & Roberts, H. (1984). Human consumption of caffeine. In P. B. Dews (Ed.), Caffeine: Perspectives from recent research (1st ed., pp. 59–60). Springer. https://doi.org/10.1007/978-3-642-69823-1
Barone, J. J., & Roberts, H. R. (1996). Caffeine consumption. Food and Chemical Toxicology, 34(1), 119–129. https://doi.org/10.1016/0278-6915(95)00093-3
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models usinglme4. Journal of Statistical Software, 67(1). https://doi.org/10.18637/jss.v067.i01
Blacker, K. J., Hamilton, J., Roush, G., Pettijohn, K. A., & Biggs, A. T. (2018). Cognitive training for military application: A review of the literature and practical guide. Journal of Cognitive Enhancement, 3(1), 30–51. https://doi.org/10.1007/s41465-018-0076-1
Borota, D., Murray, E., Keceli, G., Chang, A. X., Watabe, J., Ly, M., Toscano, J. P., & Yassa, M. A. (2014). Post-study caffeine administration enhances memory consolidation in humans. Nature Neuroscience, 17(2), 201–203. https://doi.org/10.1038/nn.3623
Brainard, D. H. (1997). The Psychophysics toolbox. Spatial Vision, 10(4), 433–436. https://doi.org/10.1163/156856897x00357
Brunyé, T. T., Mahoney, C. R., Lieberman, H. R., & Taylor, H. A. (2010). Caffeine modulates attention network function. Brain and Cognition, 72(2), 181–188. https://doi.org/10.1016/j.bandc.2009.07.013
Burdan, F. (2015). Pharmacology of caffeine: The main active compound of coffee. In V. R. Preedy (Ed.), Coffee in health and disease prevention (pp. 823–829). Academic Press. https://doi.org/10.1016/b978-0-12-409517-5.00090-5
Bylsma, F., Brandt, J., & Strauss, M. E. (1990). Aspects of procedural memory are differentially impaired in Huntington’s disease. Archives of Clinical Neuropsychology, 5(3), 287–297. https://doi.org/10.1016/0887-6177(90)90027-m
Caragea, V., Méndez-Couz, M., & Manahan-Vaughan, D. (2024). Dopamine receptors of the rodent fastigial nucleus support skilled reaching for goal-directed action. Brain Structure and Function, 229(3), 609–637. https://doi.org/10.1007/s00429-023-02685-0
Carrillo, J. A., & Benitez, J. (2000). Clinically significant pharmacokinetic interactions between dietary caffeine and medications. Clinical Pharmacokinetics, 39(2), 127–153. https://doi.org/10.2165/00003088-200039020-00004
Cavaco, S., Feinstein, J. S., Van Twillert, H., & Tranel, D. (2012). Musical memory in a patient with severe anterograde amnesia. Journal of Clinical and Experimental Neuropsychology, 34(10), 1089–1100. https://doi.org/10.1080/13803395.2012.728568
Cayzac, S., Delcasso, S., Paz, V., Jeantet, Y., & Cho, Y. H. (2011). Changes in striatal procedural memory coding correlate with learning deficits in a mouse model of Huntington disease. Proceedings of the National Academy of Sciences, 108(22), 9280–9285. https://doi.org/10.1073/pnas.1016190108
Childs, E., & De Wit, H. (2006). Subjective, behavioral, and physiological effects of acute caffeine in light, nondependent caffeine users. Psychopharmacology, 185, 514–523. https://doi.org/10.1007/s00213-006-0341-3
Cohen, M. D., & Bacdayan, P. (1994). Organizational routines are stored as procedural memory: Evidence from a laboratory study. Organization Science, 5(4), 554–568. https://doi.org/10.1287/orsc.5.4.554
Corkin, S. (1968). Acquisition of motor skill after bilateral medial temporal-lobe excision. Neuropsychologia, 6(3), 255–265. https://doi.org/10.1016/0028-3932(68)90024-9
Craig, C. L., Marshall, A. L., Sjöström, M., Bauman, A. E., Booth, M. L., Ainsworth, B. E., Pratt, M., Ekelund, U., Yngve, A., Sallis, J. F., & Oja, P. (2003). International Physical Activity Questionnaire: 12-Country reliability and validity. Medicine and Science in Sports and Exercise, 35(8), 1381–1395. https://doi.org/10.1249/01.mss.0000078924.61453.fb
Cysneiros, R. M., Farkas, D., Harmatz, J. S., Von Moltke, L. L., & Greenblatt, D. J. (2007). Pharmacokinetic and pharmacodynamic interactions between zolpidem and caffeine. Clinical Pharmacology & Therapeutics, 82(1), 54–62. https://doi.org/10.1038/sj.clpt.6100211
Dayan, E., & Cohen, L. G. (2011). Neuroplasticity subserving motor skill learning. Neuron, 72(3), 443–454. https://doi.org/10.1016/j.neuron.2011.10.008
De Vries, M. H., Ulte, C., Zwitserlood, P., Szymanski, B., & Knecht, S. (2010). Increasing dopamine levels in the brain improves feedback-based procedural learning in healthy participants: An artificial-grammar-learning experiment. Neuropsychologia, 48(11), 3193–3197. https://doi.org/10.1016/j.neuropsychologia.2010.06.024
Debas, K., Carrier, J., Orban, P., Barakat, M., Lungu, O., Vandewalle, G., Tahar, A. H., Bellec, P., Karni, A., Ungerleider, L. G., Benali, H., & Doyon, J. (2010). Brain plasticity related to the consolidation of motor sequence learning and motor adaptation. Proceedings of the National Academy of Sciences, 107(41), 17839–17844. https://doi.org/10.1073/pnas.1013176107
Di Filippo, M., & Calabresi, P. (2016). Regulation of corticostriatal synaptic plasticity in physiological and pathological conditions. In Handbook of behavioral neuroscience (pp. 459–476). https://doi.org/10.1016/b978-0-12-802206-1.00023-4
Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007). The temporal dynamics model of emotional memory processing: A synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson Law. Neural Plasticity, 2007, 1–33. https://doi.org/10.1155/2007/60803
Doyle, T. P., Lutz, R. S., Pellegrino, J. K., Sanders, D. J., & Arent, S. M. (2016). The effects of caffeine on arousal, response time, accuracy, and performance in division I collegiate fencers. Journal of Strength and Conditioning Research, 30(11), 3228–3235. https://doi.org/10.1519/jsc.0000000000001602
Doyon, J., Gabitov, E., Vahdat, S., Lungu, O., & Boutin, A. (2018). Current issues related to motor sequence learning in humans. Current Opinion in Behavioral Sciences, 20, 89–97. https://doi.org/10.1016/j.cobeha.2017.11.012
Dudai, Y. (2004). The neurobiology of consolidations, or, how stable is the engram? Annual Review of Psychology, 55(1), 51–86. https://doi.org/10.1146/annurev.psych.55.090902.142050
Einöther, S. J., & Giesbrecht, T. (2012). Caffeine as an attention enhancer: Reviewing existing assumptions. Psychopharmacology, 225(2), 251–274. https://doi.org/10.1007/s00213-012-2917-4
Elkin, L. A., Kay, M., Higgins, J. J., & Wobbrock, J. O. (2021). An aligned rank transform procedure for multifactor contrast tests. The 34th Annual ACM Symposium on User Interface Software and Technology, 754–768. https://doi.org/10.1145/3472749.3474784
Engelen, U., De Peuter, S., Victoir, A., Van Diest, I., & Van Den Bergh, O. (2006). Verdere validering van de Positive and Negative Affect Schedule (PANAS) en vergelijking van twee Nederlandstalige versies. Gedrag En Gezondheid, 34(2), 61–70. https://doi.org/10.1007/bf03087979
Farkas, B. C., Krajcsi, A., Janacsek, K., & Nemeth, D. (2024). The complexity of measuring reliability in learning tasks: An illustration using the Alternating Serial Reaction Time Task. Behavior Research Methods, 56(1), 301–317. https://doi.org/10.3758/s13428-022-02038-5
Ferré, S. (2008). An update on the mechanisms of the psychostimulant effects of caffeine. Journal of Neurochemistry, 105(4), 1067–1079. https://doi.org/10.1111/j.1471-4159.2007.05196.x
Ferré, S. (2010). Role of the central ascending neurotransmitter systems in the psychostimulant effects of caffeine. Journal of Alzheimer S Disease, 20(s1), S35–S49. https://doi.org/10.3233/jad-2010-1400
Ferré, S., Fuxé, K., Fredholm, B. B., Morelli, M., & Popoli, P. (1997). Adenosine–dopamine receptor–receptor interactions as an integrative mechanism in the basal ganglia. Trends in Neurosciences, 20(10), 482–487. https://doi.org/10.1016/s0166-2236(97)01096-5
Fischer, S., Nitschke, M. F., Melchert, U. H., Erdmann, C., & Born, J. (2005). Motor memory consolidation in sleep shapes more effective neuronal representations. Journal of Neuroscience, 25(49), 11248–11255. https://doi.org/10.1523/jneurosci.1743-05.2005
Fisone, G., Borgkvist, A., & Usiello, A. (2004). Caffeine as a psychomotor stimulant: Mechanism of action. Cellular and Molecular Life Sciences, 61(7–8), 857–872. https://doi.org/10.1007/s00018-003-3269-3
Fox, G., Wu, A., Liang, Y., & Force, L. E. (2013). Variation in caffeine concentration in single coffee beans. Journal of Agricultural and Food Chemistry, 61(45), 10772–10778. https://doi.org/10.1021/jf4011388
Fredholm, B. B. (1995). Adenosine, adenosine receptors and the actions of caffeine. Pharmacology & Toxicology, 76(2), 93–101. https://doi.org/10.1111/j.1600-0773.1995.tb00111.x
Fredholm, B. B. (2011). Methylxanthines. In Handbook of experimental pharmacology. https://doi.org/10.1007/978-3-642-13443-2
Fredholm, B. B., Bättig, K., Holmén, J., Nehlig, A., & Zvartau, E. E. (1999). Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacological Reviews, 51(1), 83–133. https://pubmed.ncbi.nlm.nih.gov/10049999
Gais, S., Rasch, B., Wagner, U., & Born, J. (2008). Visual–Procedural memory consolidation during sleep blocked by glutamatergic receptor antagonists. Journal of Neuroscience, 28(21), 5513–5518. https://doi.org/10.1523/jneurosci.5374-07.2008
Gardiner, C., Weakley, J., Burke, L. M., Roach, G. D., Sargent, C., Maniar, N., Townshend, A. D., & Halson, S. L. (2023). The effect of caffeine on subsequent sleep: A systematic review and meta-analysis. Sleep Medicine Reviews, 69, 101764. https://doi.org/10.1016/j.smrv.2023.101764
Gracia-Lor, E., Rousis, N. I., Zuccato, E., Bade, R., Baz-Lomba, J. A., Castrignanò, E., Causanilles, A., Hernández, F., Kasprzyk-Hordern, B., Kinyua, J., McCall, A., Van Nuijs, A. L., Plósz, B. G., Ramin, P., Ryu, Y., Santos, M. M., Thomas, K. V., De Voogt, P., Yang, Z., & Castiglioni, S. (2017). Estimation of caffeine intake from analysis of caffeine metabolites in wastewater. Science of the Total Environment, 609, 1582–1588. https://doi.org/10.1016/j.scitotenv.2017.07.258
Green, P., & MacLeod, C. J. (2015). SIMR: an R package for power analysis of generalized linear mixed models by simulation. Methods in Ecology and Evolution, 7(4), 493–498. https://doi.org/10.1111/2041-210x.12504
Hair, J. F., Black, W. C., Babin, B. J., Anderson, R. E., & Tatham, R. L. (2005). Multivariate data analysis (6th ed.). Pearson Prentice Hall.
Hasselmo, M. E. (2006). The role of acetylcholine in learning and memory. Current Opinion in Neurobiology, 16(6), 710–715. https://doi.org/10.1016/j.conb.2006.09.002
Heckman, M. A., Weil, J., & De Mejia, E. G. (2010). Caffeine (1, 3, 7-trimethylxanthine) in foods: A comprehensive review on consumption, functionality, safety, and regulatory matters. Journal of Food Science, 75(3). https://doi.org/10.1111/j.1750-3841.2010.01561.x
Hikosaka, O., Nakamura, K., Sakai, K., & Nakahara, H. (2002). Central mechanisms of motor skill learning. Current Opinion in Neurobiology, 12(2), 217–222. https://doi.org/10.1016/s0959-4388(02)00307-0
Hollingworth, H. L. (1912). The influence of caffein on mental and motor efficiency. The Science Press. https://doi.org/10.1037/10936-000
Hopkins, M., Davis, F., VanTieghem, Whalen, P., & Bucci, D. (2012). Differential effects of acute and regular physical exercise on cognition and affect. Neuroscience, 215, 59–68. https://doi.org/10.1016/j.neuroscience.2012.04.056
Iglesias, D., Moreno, M. P., Santos-Rosa, F. J., Cervelló, E., & Del Villar, F. (2005). Cognitive expertise in sport: relationships between procedural knowledge, experience and performance in youth basketball. Journal of Human Movement Studies, 49(1), 0306-7297/05/0700-0065 515.00. https://www.researchgate.net/publication/270217082_Cognitive_expertise_…
Jacobson, B. H., & Edgley, B. M. (1987). Effects of caffeine on simple reaction time and movement time. PubMed, 58(12), 1153–1156. https://pubmed.ncbi.nlm.nih.gov/3426488
James, J. E. (1997). Understanding caffeine: A biobehavioral analysis. SAGE Publications, Incorporated. https://archive.org/details/understandingcaf0000jame/mode/2up
James, J. E., & Rogers, P. J. (2005). Effects of caffeine on performance and mood: Withdrawal reversal is the most plausible explanation. Psychopharmacology, 182(1), 1–8. https://doi.org/10.1007/s00213-005-0084-6
Jay, T. M. (2003). Dopamine: A potential substrate for synaptic plasticity and memory mechanisms. Progress in Neurobiology, 69(6), 375–390. https://doi.org/10.1016/s0301-0082(03)00085-6
Jetté, M., Sidney, K., & Blümchen, G. (1990). Metabolic equivalents (METS) in exercise testing, exercise prescription, and evaluation of functional capacity. Clinical Cardiology, 13(8), 555–565. https://doi.org/10.1002/clc.4960130809
Kamimori, G. H., Karyekar, C. S., Otterstetter, R., Cox, D. S., Balkin, T. J., Belenky, G., & Eddington, N. D. (2002). The rate of absorption and relative bioavailability of caffeine administered in chewing gum versus capsules to normal healthy volunteers. International Journal of Pharmaceutics, 234(1–2), 159–167. https://doi.org/10.1016/s0378-5173(01)00958-9
Kaplan, G. B., Greenblatt, D. J., Ehrenberg, B. L., Goddard, J., Cotreau, M. M., Harmatz, J. S., & Shader, R. I. (1997). Dose-Dependent pharmacokinetics and psychomotor effects of caffeine in humans. The Journal of Clinical Pharmacology, 37(8), 693–703. https://doi.org/10.1002/j.1552-4604.1997.tb04356.x
Kelley, A. E., Andrzejewski, M. E., Baldwin, A. E., Hernandez, P. J., & Pratt, W. E. (2003). Glutamate‐Mediated plasticity in corticostriatal networks. Annals of the New York Academy of Sciences, 1003(1), 159–168. https://doi.org/10.1196/annals.1300.061
Kerr, G. (2021). A short history of coffee. Oldcastle Books.
Kingston, N., & Tiemann, G. (2010). Spearman–Brown Prophecy Formula. In N. J. Salkind (Ed.), Encyclopedia of research design (pp. 1403–1404). SAGE Publications, Inc. https://doi.org/10.4135/9781412961288.n427
Kleiner, M., Brainard, D., Pelli, D., & Ingling, A. (2007). What’s new in Psychtoolbox-3? Perception, 36(14), 1–16. https://doi.org/10.1068/v070821
Knopman, D., & Nissen, M. J. (1991). Procedural learning is impaired in Huntington’s disease: Evidence from the serial reaction time task. Neuropsychologia, 29(3), 245–254. https://doi.org/10.1016/0028-3932(91)90085-m
Knowlton, B. J., & Schorn, J. M. (2024). Procedural and motor learning. In M. J. Kahana & A. D. Wagner (Eds.), The Oxford handbook of human memory, two volume pack: Foundations and applications (pp. 244–267). Oxford Library of Psychology. https://doi.org/10.1093/oxfordhb/9780190917982.013.9
LaLumiere, R. T., McGaugh, J. L., & McIntyre, C. K. (2017). Emotional modulation of learning and memory: Pharmacological implications. Pharmacological Reviews, 69(3), 236–255. https://doi.org/10.1124/pr.116.013474
Lara, B., Ruiz-Moreno, C., Salinero, J. J., & Del Coso, J. (2019). Time course of tolerance to the performance benefits of caffeine. PLoS ONE, 14(1), e0210275. https://doi.org/10.1371/journal.pone.0210275
Lee, A. Y., & Sternthal, B. (1999). The effects of positive mood on memory. Journal of Consumer Research, 26(2), 115–127. https://doi.org/10.1086/209554
Liguori, A., Hughes, J. R., & Grass, J. A. (1997). Absorption and subjective effects of caffeine from coffee, cola and capsules. Pharmacology, Biochemistry and Behavior, 58(3), 721–726. https://doi.org/10.1016/s0091-3057(97)00003-8
Little, R. J. A. (1988). Missing-Data adjustments in large surveys. Journal of Business and Economic Statistics, 6(3), 287–296. https://doi.org/10.1080/07350015.1988.10509663
Lo, S., & Andrews, S. (2015). To transform or not to transform: Using generalized linear mixed models to analyse reaction time data. Frontiers in Psychology, 6. https://doi.org/10.3389/fpsyg.2015.01171
Loprinzi, P. D., Roig, M., Etnier, J. L., Tomporowski, P. D., & Voss, M. (2021). Acute and chronic exercise effects on human memory: What we know and where to go from here. Journal of Clinical Medicine, 10(21), 4812. https://doi.org/10.3390/jcm10214812
Lorist, M. M., & Tops, M. (2003). Caffeine, fatigue, and cognition. Brain and Cognition, 53(1), 82–94. https://doi.org/10.1016/s0278-2626(03)00206-9
Ludwig, I. A., Mena, P., Calani, L., Cid, C., Del Rio, D., Lean, M. E. J., & Crozier, A. (2014). Variations in caffeine and chlorogenic acid contents of coffees: What are we drinking? Food & Function, 5(8), 1718–1726. https://doi.org/10.1039/c4fo00290c
McCoy, J. G., & Strecker, R. E. (2011). The cognitive cost of sleep lost. Neurobiology of Learning and Memory, 96(4), 564–582. https://doi.org/10.1016/j.nlm.2011.07.004
McCusker, R. R., Fuehrlein, B., Goldberger, B. A., Gold, M. S., & Cone, E. J. (2006). Caffeine content of decaffeinated coffee. Journal of Analytical Toxicology, 30(8), 611–613. https://doi.org/10.1093/jat/30.8.611
McCusker, R. R., Goldberger, B. A., & Cone, E. J. (2003). Caffeine content of specialty coffees. Journal of Analytical Toxicology, 27(7), 520–522. https://doi.org/10.1093/jat/27.7.520
McLellan, T. M., Caldwell, J. A., & Lieberman, H. R. (2016). A review of caffeine’s effects on cognitive, physical and occupational performance. Neuroscience & Biobehavioral Reviews, 71, 294–312. https://doi.org/10.1016/j.neubiorev.2016.09.001
Misto, Alawiyah, K., Rohman, L., Supriyadi, S., Mutmainnah, & Purwandari, E. (2021). Spectrophotometric analysis of caffeine in local product of Arabica: Observed at different roasted temperatures. IOP Conference Series: Materials Science and Engineering, 1173(1), 012012. https://doi.org/10.1088/1757-899x/1173/1/012012
Muellbacher, W., Ziemann, U., Wissel, J., Dang, N., Kofler, M., Facchini, S., Boroojerdi, B., Poewe, W., & Hallett, M. (2002). Early consolidation in human primary motor cortex. Nature, 415(6872), 640–644. https://doi.org/10.1038/nature712
Muratori, L. M., Lamberg, E. M., Quinn, L., & Duff, S. V. (2013). Applying principles of motor learning and control to upper extremity rehabilitation. Journal of Hand Therapy, 26(2), 94–103. https://doi.org/10.1016/j.jht.2012.12.007
Natick. (2024). MATLAB (24.1 R2024A) [Software]. The MathWorks Inc. https://www.mathworks.com
Nehlig, A., Daval, J., & Debry, G. (1992). Caffeine and the central nervous system: Mechanisms of action, biochemical, metabolic and psychostimulant effects. Brain Research Reviews, 17(2), 139–170. https://doi.org/10.1016/0165-0173(92)90012-b
Neves, B. S., Del Rosso Barbosa, G. P., De Souza Rosa, A. C., Picua, S. S., Gomes, G. M., Sosa, P. M., & Mello-Carpes, P. B. (2020). On the role of the dopaminergic system in the memory deficits induced by maternal deprivation. Neurobiology of Learning and Memory, 173, 107272. https://doi.org/10.1016/j.nlm.2020.107272
Oliveira, C. M., Hayiou-Thomas, M. E., & Henderson, L. M. (2024). Reliability of the serial reaction time task: If at first you don’t succeed, try, try, try again. Quarterly Journal of Experimental Psychology, 77(11), 2256–2282. https://doi.org/10.1177/17470218241232347
Parsons, O. (2015). Serial-reaction-time-task [Software]. https://github.com/autism-research-centre/serial-reaction-time-task
Pauly, L., Pauly, C., Hansen, M., Schröder, V. E., Rauschenberger, A., Leist, A. K., & Krüger, R. (2022). Retrograde procedural memory in Parkinson’s disease: A cross-sectional, case-control study. Journal of Parkinson S Disease, 12(3), 1013–1022. https://doi.org/10.3233/jpd-213081
Pelli, D. G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision, 10(4), 437–442. https://doi.org/10.1163/156856897x00366
Porkka‐Heiskanen, T., Alanko, L., Kalinchuk, A. V., & Stenberg, D. (2002). Adenosine and sleep. Sleep Medicine Reviews, 6(4), 321–332. https://doi.org/10.1053/smrv.2001.0201
Posit Team. (2025). RStudio: Integrated Development Environment for R (2024.12.1.563) [Software]. Posit Software, PBC. http://www.posit.co/
Prestori, F., Bonardi, C., Mapelli, L., Lombardo, P., Goselink, R., De Stefano, M. E., Gandolfi, D., Mapelli, J., Bertrand, D., Schonewille, M., De Zeeuw, C., & D’Angelo, E. (2013). Gating of long-term potentiation by nicotinic acetylcholine receptors at the cerebellum input stage. PLoS ONE, 8(5), e64828. https://doi.org/10.1371/journal.pone.0064828
Quadra, G. R., Paranaíba, J. R., Vilas–Boas, J. A., Roland, F., Amado, A. M., Barros, N., Dias, R. J. P., & Cardoso, S. J. (2020). A global trend of caffeine consumption over time and related-environmental impacts. Environmental Pollution, 256, 113343. https://doi.org/10.1016/j.envpol.2019.113343
R Core Team. (2024). R: A Language and Environment for Statistical Computing (4.4.0, Vol. 1, Issue 1) [Software]. R Foundation for Statistical Computing. https://www.r-project.org/
Rammsayer, T. H., Rodewald, S., & Groh, D. (2000). Dopamine-Antagonistic, anticholinergic, and GABAergic effects on declarative and procedural memory functions. Cognitive Brain Research, 9(1), 61–71. https://doi.org/10.1016/s0926-6410(99)00045-2
Reber, P. J., & Squire, L. R. (1994). Parallel brain systems for learning with and without awareness. Learning & Memory, 1(4), 217–229. https://doi.org/10.1101/lm.1.4.217
Reddy, V. S., Shiva, S., Manikantan, S., & Ramakrishna, S. (2024). Pharmacology of caffeine and its effects on the human body. European Journal of Medicinal Chemistry Reports, 10, 100138. https://doi.org/10.1016/j.ejmcr.2024.100138
Ribeiro, J. A., & Sebastião, A. M. (2010). Caffeine and adenosine. Journal of Alzheimer’s Disease, 20(s1), S3–S15. https://doi.org/10.3233/jad-2010-1379
Rioult-Pedotti, M., Friedman, D., & Donoghue, J. P. (2000). Learning-Induced LTP in neocortex. Science, 290(5491), 533–536. https://doi.org/10.1126/science.290.5491.533
Rioult-Pedotti, M.-., Friedman, D., Hess, G., & Donoghue, J. P. (1998). Strengthening of horizontal cortical connections following skill learning. Nature Neuroscience, 1(3), 230–234. https://doi.org/10.1038/678
Robertson, E. M. (2009). From creation to consolidation: A novel framework for memory processing. PLoS Biology, 7(1), e1000019. https://doi.org/10.1371/journal.pbio.1000019
Rubin, D. B. (1986). Statistical matching using file concatenation with adjusted weights and multiple imputations. Journal of Business and Economic Statistics, 4(1), 87–94. https://doi.org/10.1080/07350015.1986.10509497
Ryan, L., Hatfield, C., & Hofstetter, M. (2002). Caffeine reduces time-of-day effects on memory performance in older adults. Psychological Science, 13(1), 68–71. https://doi.org/10.1111/1467-9280.00412
Santos, V. G. F., Santos, V. R. F., Felippe, L. C., Almeida, J. W. L., De Moraes Bertuzzi, R. C., Kiss, M. a. P. D., & Lima‐Silva, A. E. (2014). Caffeine reduces reaction time and improves performance in simulated-contest of taekwondo. Nutrients, 6(2), 637–649. https://doi.org/10.3390/nu6020637
Schapiro, A. C., Reid, A. G., Morgan, A., Manoach, D. S., Verfaellie, M., & Stickgold, R. (2019). The hippocampus is necessary for the consolidation of a task that does not require the hippocampus for initial learning. Hippocampus, 29(11), 1091–1100. https://doi.org/10.1002/hipo.23101
Schimidt, H. L., Carpes, P. B. M., & Carpes, F. P. (2016). The role of regular physical exercise for enhancement of long-term memory in the elderly: A review of recent evidences. PAJAR - Pan American Journal of Aging Research, 3(2), 60. https://doi.org/10.15448/2357-9641.2015.2.21786
Schönauer, M., Geisler, T., & Gais, S. (2014). Strengthening procedural memories by reactivation in sleep. Journal of Cognitive Neuroscience, 26(1), 143–153. https://doi.org/10.1162/jocn_a_00471
Schwarb, H., & Schumacher, E. H. (2012). Generalized lessons about sequence learning from the study of the serial reaction time task. Advances in Cognitive Psychology, 8(2), PMID: 22723815. https://doi.org/10.2478/v10053-008-0113-1
Shallice, T. (1988). From neuropsychology to mental structure. Cambridge University Press. https://archive.org/details/fromneuropsychol0000shal
Sherman, S. M., Buckley, T. P., Baena, E., & Ryan, L. (2016). Caffeine enhances memory performance in young adults during their non-optimal time of day. Frontiers in Psychology, 7. https://doi.org/10.3389/fpsyg.2016.01764
Siengsukon, C. F., & Boyd, L. A. (2009). Does sleep promote motor learning? Implications for physical rehabilitation. Physical Therapy, 89(4), 370–383. https://doi.org/10.2522/ptj.20080310
Sjöström, M., Ainsworth, B., Bauman, A., Bull, F., Hamilton-Craig, C., & Sallis, J. (2005). Guidelines for data processing analysis of the International Physical Activity Questionnaire (IPAQ) - Short and long forms. CiNii Articles. https://sites.google.com/view/ipaq/score
Smit, H., & Rogers, P. (2000). Effects of low doses of caffeine on cognitive performance, mood and thirst in low and higher caffeine consumers. Psychopharmacology, 152, 167–173. https://doi.org/10.1007/s002130000506
Smith, C., & Macneill, C. (1994). Impaired motor memory for a pursuit rotor task following stage 2 sleep loss in college students. Journal of Sleep Research, 3(4), 206–213. https://doi.org/10.1111/j.1365-2869.1994.tb00133.x
Snel, J., & Lorist, M. M. (2011). Effects of caffeine on sleep and cognition. In H. P. A. Van Dongen & G. A. Kerkhof (Eds.), Progress in brain research (Vol. 190, pp. 105–117). Elsevier. https://doi.org/10.1016/b978-0-444-53817-8.00006-2
Southward, K., Rutherfurd-Markwick, K. J., & Ali, A. (2018). The effect of acute caffeine ingestion on endurance performance: A systematic review and meta-analysis. Sports Medicine, 48(8), 1913–1928. https://doi.org/10.1007/s40279-018-0939-8
Squire, L. R. (2004). Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory, 82(3), 171–177. https://doi.org/10.1016/j.nlm.2004.06.005
Sridhar, S., Khamaj, A., & Asthana, M. K. (2023). Cognitive neuroscience perspective on memory: Overview and summary. Frontiers in Human Neuroscience, 17. https://doi.org/10.3389/fnhum.2023.1217093
Stanley, J. A., Burgess, A., Khatib, D., Ramaseshan, K., Arshad, M., Wu, H., &
Diwadkar, V. A. (2017). Functional dynamics of hippocampal glutamate during associative learning assessed with in vivo 1H functional magnetic resonance spectroscopy. NeuroImage, 153, 189–197. https://doi.org/10.1016/j.neuroimage.2017.03.051
Stavrić, B., Klassen, R., Watkinson, B., Karpinski, K., Stapley, R., & Fried, P. A. (1988). Variability in caffeine consumption from coffee and tea: Possible significance for epidemiological studies. Food and Chemical Toxicology, 26(2), 111–118. https://doi.org/10.1016/0278-6915(88)90107-x
Stefanello, N., Spanevello, R. M., Passamonti, S., Porciúncula, L., Bonan, C. D., Olabiyi, A. A., Da Rocha, J. B. T., Assmann, C. E., Morsch, V. M., & Schetinger, M. R. C. (2019). Coffee, caffeine, chlorogenic acid, and the purinergic system. Food and Chemical Toxicology, 123, 298–313. https://doi.org/10.1016/j.fct.2018.10.005
Stefaniak, N., Baltazart, V., & Declercq, C. (2021). Processing verb meanings and the declarative/procedural model: A developmental study. Frontiers in Psychology, 12. https://doi.org/10.3389/fpsyg.2021.714523
Stevans, J., & Hall, K. G. (1998). Motor skill acquisition strategies for rehabilitation of low back pain. Journal of Orthopaedic and Sports Physical Therapy, 28(3), 165–167. https://doi.org/10.2519/jospt.1998.28.3.165
Stickgold, R., James, L., & Hobson, J. A. (2000). Visual discrimination learning requires sleep after training. Nature Neuroscience, 3(12), 1237–1238. https://doi.org/10.1038/81756
Stickgold, R., & Walker, M. P. (2007). Sleep-dependent memory consolidation and reconsolidation. Sleep Medicine, 8(4), 331–343. https://doi.org/10.1016/j.sleep.2007.03.011
Superior Health Council. (2012). The use of caffeine in foodstuffs (No. 8689). FPS Public Health, Food Chain Safety and Environment. Retrieved August 6, 2024, from https://www.hgr-css.be/en/report/8689/caffeine
Temple, J. L., Bernard, C., Lipshultz, S. E., Czachor, J. D., Westphal, J. A., & Mestre, M. A. (2017). The safety of ingested caffeine: A comprehensive review. Frontiers in Psychiatry, 8. https://doi.org/10.3389/fpsyt.2017.00080
Thielen, J., Hong, D., Rankouhi, S. R., Wiltfang, J., Fernández, G., Norris, D. G., & Tendolkar, I. (2018). The increase in medial prefrontal glutamate/glutamine concentration during memory encoding is associated with better memory performance and stronger functional connectivity in the human medial prefrontal–thalamus–hippocampus network. Human Brain Mapping, 39(6), 2381–2390. https://doi.org/10.1002/hbm.24008
Thomas, R., Beck, M. M., Lind, R. R., Johnsen, L. K., Geertsen, S. S., Christiansen, L., Ritz, C., Roig, M., & Lundbye-Jensen, J. (2016). Acute exercise and motor memory consolidation: The role of exercise timing. Neural Plasticity, 2016(1), 1–11. https://doi.org/10.1155/2016/6205452
Thompson, E. R. (2007). Development and validation of an internationally reliable short-form of the Positive and Negative Affect Schedule (PANAS). Journal of Cross-Cultural Psychology, 38(2), 227–242. https://doi.org/10.1177/0022022106297301
Titulaer, J., Björkholm, C., Feltmann, K., Malmlöf, T., Mishra, D., Gonzales, C. B., Schilström, B., & Konradsson-Geuken, Å. (2021). The importance of ventral hippocampal dopamine and norepinephrine in recognition memory. Frontiers in Behavioral Neuroscience, 15. https://doi.org/10.3389/fnbeh.2021.667244
Ullman, M. T. (2013). The role of declarative and procedural memory in disorders of language. Linguistic Variation, 13(2), 133–154. https://doi.org/10.1075/lv.13.2.01ull
Van Buuren, S., & Groothuis-Oudshoorn, K. (2011). mice: Multivariate imputation by chained equations in R. Journal of Statistical Software, 45(3). https://doi.org/10.18637/jss.v045.i03
Van Der Heijden, M. E., Hipolito, A. G. R., Kim, L. H., Kizek, D. J., Perez, R. M., Lin, T., & Sillitoe, R. V. (2023). Glutamatergic cerebellar neurons differentially contribute to the acquisition of motor and social behaviors. Nature Communications, 14(1). https://doi.org/10.1038/s41467-023-38475-9
Van Schalkwijk, F. J., Sauter, C., Hoedlmoser, K., Heib, D. P. J., Klösch, G., Moser, D., Gruber, G., Anderer, P., Zeitlhofer, J., & Schabus, M. (2017). The effect of daytime napping and full‐night sleep on the consolidation of declarative and procedural information. Journal of Sleep Research, 28(1). https://doi.org/10.1111/jsr.12649
Vanlessen, N., De Raedt, R., Koster, E. H., & Pourtois, G. (2016). Happy heart, smiling eyes: A systematic review of positive mood effects on broadening of visuospatial attention. Neuroscience & Biobehavioral Reviews, 68, 816–837. https://doi.org/10.1016/j.neubiorev.2016.07.001
Walker, M. P., Brakefield, T., Hobson, J. A., & Stickgold, R. (2003). Dissociable stages of human memory consolidation and reconsolidation. Nature, 425(6958), 616–620. https://doi.org/10.1038/nature01930
Weinberg, B. A., & Bealer, B. K. (2001). The world of caffeine: The science and culture of the world’s most popular drug (1st ed.). Routledge.
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer-Verlag. https://ggplot2.tidyverse.org
Wickham, H., François, R., Henry, L., Müller, K., & Vaughan, D. (2023). dplyr: A grammar of data manipulation (1.1.4) [Software]. https://doi.org/10.32614/cran.package.dplyr
Wobbrock, J. O., Findlater, L., Gergle, D., & Higgins, J. J. (2011). The aligned rank transform for nonparametric factorial analyses using only anova procedures. Proceedings of the International Conference on Human Factors in Computing Systems, 143–146. https://doi.org/10.1145/1978942.1978963
Yang, L., Yu, X., Zhang, Y., Liu, N., Xue, X., & Fu, J. (2021). Encephalopathy in preterm infants: Advances in neuroprotection with caffeine. Frontiers in Pediatrics, 9. https://doi.org/10.3389/fped.2021.724161
Yerkes, R. M., & Dodson, J. D. (1908). The relation of strength of stimulus to rapidity of habit‐formation. Journal of Comparative Neurology and Psychology, 18(5), 459–482. https://doi.org/10.1002/cne.920180503
