Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-17T13:29:18.708Z Has data issue: false hasContentIssue false

A role of serotonin and the insula in vigor: Tracking environmental and physiological resources

Published online by Cambridge University Press:  30 September 2021

Mattie Tops
Affiliation:
Developmental and Educational Psychology Unit, Institute of Psychology, Wassenaarseweg 52, NL-2333 AK Leiden, The Netherlandsm.tops@fsw.leidenuniv.nlhttp://loop.frontiersin.org/people/8492/overview
Maarten A. S. Boksem
Affiliation:
Department of Marketing Management, Rotterdam School of Management, Erasmus University, 3000 DRRotterdam, The Netherlandsmboksem@rsm.nlwww.rsm.nl/people/maarten-boksem/
Jesus Montero-Marin
Affiliation:
Department of Psychiatry, Warneford Hospital, Warneford Ln, Headington, OxfordOX3 7JX, UKjesus.monteromarin@psych.ox.ac.ukhttps://www.psych.ox.ac.uk/team/jesus-montero-marin
Dimitri van der Linden
Affiliation:
Department of Psychology, Education, and Child Studies, Erasmus University Rotterdam, 3000 DRRotterdam, The Netherlandsvanderlinden@essb.eur.nlhttps://www.eur.nl/en/people/dimitri-van-der-linden

Abstract

We describe a neural monitor of environmental and physiological resources that informs effort expenditure. Depending on resources and environmental stability, serotonergic and dopaminergic neuromodulations favor different behavioral controls that are organized in corticostriatal loops. This broader perspective produces some suggestions and questions that may not be covered by the foraging approach to vigor of Shadmehr and Ahmed (2020).

Type
Open Peer Commentary
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ainslie, G. (2020). Willpower with and without effort. Behavioral and Brain Sciences, 44, e30. https://doi.org/10.1017/S0140525X20000357CrossRefGoogle ScholarPubMed
Beeler, J. A., Frazier, C. R., & Zhuang, X. (2012). Putting desire on a budget: Dopamine and energy expenditure, reconciling reward and resources. Frontiers in integrative neuroscience, 6, 49. https://doi.org/10.3389/fnint.2012.00049CrossRefGoogle ScholarPubMed
Berke, J. D. (2018). What does dopamine mean?. Nature neuroscience, 21(6), 787793. https://doi.org/10.1038/s41593-018-0152-yCrossRefGoogle ScholarPubMed
Boksem, M. A. S., & Tops, M. (2008). Mental fatigue: Costs and benefits. Brain Research Reviews, 59, 125139.CrossRefGoogle ScholarPubMed
Buckner, R. L., & Carroll, D. C. (2007) Self-projection and the brain. Trends in Cognitive Sciences, 11, 4957.CrossRefGoogle ScholarPubMed
Carr, L., Iacoboni, M., Dubeau, M. C., Mazziotta, J. C., & Lenzi, G. L. (2003). Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences of the United States of America, 100(9), 54975502. https://doi.org/10.1073/pnas.0935845100AICrossRefGoogle ScholarPubMed
Carter, C. S. (2014). Oxytocin pathways and the evolution of human behavior. Annual review of psychology, 65, 1739. https://doi.org/10.1146/annurev-psych-010213-115110CrossRefGoogle ScholarPubMed
Carver, C. S., Johnson, S. L., & Joormann, J. (2009). Two-mode models of self-regulation as a tool for conceptualizing effects of the serotonin system in normal behavior and diverse disorders. Current Directions of Psychological Science, 18, 195199.CrossRefGoogle ScholarPubMed
Craig, A. D. (2002). How do you feel? Interoception: The sense of the physiological condition of the body. Nature Reviews Neuroscience, 3(8), 655666.CrossRefGoogle Scholar
Damasio, A. R. (1999). The feelings of what happens: Body and emotion in the making of consciousness. Houghton Mifflin Harcourt.Google Scholar
de Graaf, J. B., Gallea, C., Pailhous, J., Anton, J. L., Roth, M., & Bonnard, M. (2004). Awareness of muscular force during movement production: An fMRI study. NeuroImage, 21,13571367.CrossRefGoogle Scholar
Depue, R. A. (1995). Neurobiological factors in personality and depression. European Journal of Personality, 9, 413439.CrossRefGoogle Scholar
Downar, J., Crawley, A. P., Mikulis, D. J., & Davis, K. D. (2002) A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. Journal of Neurophysiology, 87(1), 615620.CrossRefGoogle Scholar
Herbert, B. M., Ulbrich, P., & Schandry, R. (2007) Interoceptive sensitivity and physical effort: Implications for the self-control of physical load in everyday life. Psychophysiology, 44(2), 194202.CrossRefGoogle Scholar
Inzlicht, M., Shenhav, A., & Olivola, C. Y. (2018). The effort paradox: Effort is both costly and valued. Trends in Cognitive Sciences, 22(4), 337349. doi.org/10.1016/j.tics.2018.01.007.CrossRefGoogle ScholarPubMed
Lowry, C. A., Lightman, S. L., & Nutt, D. J. (2009). That warm fuzzy feeling: Brain serotonergic neurons and the regulation of emotion. Journal of Psychopharmacology, 23, 392400.CrossRefGoogle ScholarPubMed
Porat, O., Hassin-Baer, S., Cohen, O. S., Markus, A., & Tomer, R. (2014). Asymmetric dopamine loss differentially affects effort to maximize gain or minimize loss. Cortex, 51, 8291. http://dx.doi.org/10.1016/j.cortex.2013.10.004CrossRefGoogle ScholarPubMed
Russo, S., Kema, I. P., Fokkema, M. R., Boon, J. C., Willemse, P. H. B., de Vries, E. G. E., Korf, J. (2003). Tryptophan as a link between psychopathology and somatic states. Psychosomatic Medicine, 65(4), 665671.CrossRefGoogle ScholarPubMed
Sainburg, R. L. (2014). Convergent models of handedness and brain lateralization. Frontiers in Psychology, 5, 1092.CrossRefGoogle ScholarPubMed
Salamone, J. D., Steinpreis, R. E., McCullough, L. D., Smith, P., Grebel, D., & Mahan, K. (1991). Haloperidol and nucleus accumbens dopamine depletion suppress lever pressing for food but increase free food consumption in a novel food choice procedure. Psychopharmacology (Berl), 104, 515521.CrossRefGoogle Scholar
Schneider, J. E., Wise, J. D., Benton, N. A., Brozek, J. M., & Keen-Rhinehart, E. (2013). When do we eat? Ingestive behavior, survival, and reproductive success. Hormones and Behavior, 64 (4), 702728. http://dx.doi.org/10.1016/j.yhbeh.2013.07.005CrossRefGoogle ScholarPubMed
Shadmehr, R., & Ahmed, A. A. (2020). Vigor. Neuroeconomics of movement control. Massachusetts London, England: MIT Press Cambridge.CrossRefGoogle ScholarPubMed
Shulman, G. L., Astafiev, S. V., Franke, D., Pope, D. L., Snyder, A. Z., McAvoy, M. P., & Corbetta, M. (2009). Interaction of stimulus-driven reorienting and expectation in ventral and dorsal frontoparietal and basal ganglia-cortical networks. Journal of Neuroscience, 29, 43924407.CrossRefGoogle ScholarPubMed
Tanaka, S. C., Schweighofer, N., Asahi, S., Shishida, K., Okamoto, Y., Yamawaki, S. (2007). Serotonin differently regulates short- and long-term prediction of rewards in the ventral and dorsal striatum. PLoS ONE, 2, e1333.CrossRefGoogle Scholar
Tanaka, S. C., Doya, K., Okada, G., Ueda, K., Okamoto, Y., & Yamawaki, S. (2004). Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nature Neuroscience, 7, 887893.CrossRefGoogle ScholarPubMed
Tanaka, S. C., Samejima, K., Okada, G., Ueda, K., Okamoto, Y., Yamawaki, S., & Doya, K. (2006). Brain mechanism of reward prediction under predictable and unpredictable environmental dynamics. Neural Networks, 19, 12331241.CrossRefGoogle ScholarPubMed
Tang, T. L., & West, W. B. (1997). The importance of human needs during peacetime, retrospective peacetime, and the Persian Gulf War. International Journal of Stress Management, 4, 4762. http://dx.doi.org/10.1007/BF02766072Google Scholar
Tinaz, S., Para, K., Vives-Rodriguez, A., Martinez-Kaigi, V., Nalamada, K., Sezgin, M., & Constable, R. T. (2018). Insula as the interface between body awareness and movement: A neurofeedback-guided kinesthetic motor imagery study in Parkinson's disease. Frontiers in Human Neuroscience, 12, 496. https://doi.org/10.3389/fnhum.2018.00496CrossRefGoogle ScholarPubMed
Tops, M., & Boksem, M. A. S. (2011). A potential role of the inferior frontal gyrus and anterior insula in cognitive control, brain rhythms and event-related potentials. Frontiers in Psychology, 2(330), 1–14.CrossRefGoogle ScholarPubMed
Tops, M., Boksem, M. A. S., & Koole, S. (2013). Subjective effort derives from a neurological monitor of performance costs and physiological resources. Behavioral and Brain Sciences, 36(6), 703704.CrossRefGoogle ScholarPubMed
Tops, M., & de Jong, R. (2006). Posing for success: Clenching a fist facilitates approach. Psychonomic Bulletin and Review, 13(2), 229234.CrossRefGoogle ScholarPubMed
Tops, M., IJzerman, H., & Quirin, M. (2021). Personality dynamics in the brain: Individual differences in updating of representations and their phylogenetic roots. In Rauthmann, J. F. (Ed.), The handbook of personality dynamics and processes. (pp. 125–254) Elsevier. https://psyarxiv.com/4yj6rGoogle Scholar
Tops, M., Luu, P., Boksem, M. A. S., & Tucker, D. M. (2010). Brain substrates of behavioral programs associated with self-regulation. Frontiers in Cognition, 1, 152.Google ScholarPubMed
Tops, M., Quirin, M., Boksem, M. A. S., & Koole, S. L. (2017). Large-scale neural networks and the lateralization of motivation and emotion. International Journal of Psychophysiology, 119, 4149. doi: 10.1016/j.ijpsycho.2017.02.004CrossRefGoogle ScholarPubMed
Tops, M., Russo, S., Boksem, M. A., & Tucker, D. M. (2009). Serotonin: Modulator of a drive to withdraw. Brain and Cognition, 71, 427436.CrossRefGoogle ScholarPubMed
Tops, M., Schlinkert, C., Tjew, A., Sin, M., Samur, D., & Koole, S. L. (2015). Protective inhibition of self-regulation and motivation: Extending a classic Pavlovian principle to social and personality functioning. In Gendolla, G. H. E., Tops, M. & Koole, S. L. (Eds.), Handbook of biobehavioral approaches to self-regulation. Springer, pp. 6885. doi: 10.1007/978-1-4939-1236-0Google Scholar
Vatansever, D., Menon, D. K., & Stamatakis, E. A. (2017). Default mode contributions to automated information processing. Proceedings of the National Academy of Sciences USA, 114(48), 1282112826.CrossRefGoogle ScholarPubMed
Yoon, T., Geary, R. B., Ahmed, A. A., & Shadmehr, R. (2018). Control of movement vigor and decision making during foraging. Proceedings of the National Academy of Sciences USA, 115, E10476E10485.CrossRefGoogle ScholarPubMed