Causal involvement of dorsomedial prefrontal cortex in learning the predictability of observable actions.

Prefrontal Cortex / physiology Humans Male Female Transcranial Magnetic Stimulation Young Adult Adult Learning / physiology Social Learning / physiology

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
27 Sep 2024
Historique:
received: 04 05 2023
accepted: 11 09 2024
medline: 28 9 2024
pubmed: 28 9 2024
entrez: 27 9 2024
Statut: epublish

Résumé

Social learning is well established across species. While recent neuroimaging studies show that dorsomedial prefrontal cortex (DMPFC/preSMA) activation correlates with observational learning signals, the precise computations that are implemented by DMPFC/preSMA have remained unclear. To identify whether DMPFC/preSMA supports learning from observed outcomes or observed actions, or possibly encodes even a higher order factor (such as the reliability of the demonstrator), we downregulate DMPFC/preSMA excitability with continuous theta burst stimulation (cTBS) and assess different forms of observational learning. Relative to a vertex-cTBS control condition, DMPFC/preSMA downregulation decreases performance during action-based learning but has no effect on outcome-based learning. Computational modeling reveals that DMPFC/preSMA cTBS disrupts learning the predictability, a proxy of reliability, of the demonstrator and modulates the rate of learning from observed actions. Thus, our results suggest that the DMPFC is causally involved in observational action learning, mainly by adjusting the speed of learning about the predictability of the demonstrator.

Identifiants

DOI: 10.1038/s41467-024-52559-0 PMID: 39333062
pubmed: 39333062
doi: 10.1038/s41467-024-52559-0
pii: 10.1038/s41467-024-52559-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

8305

Subventions

Organisme : Universität Zürich (University of Zurich)
ID : K-33151-02-01
Organisme : Universität Zürich (University of Zurich)
ID : URPP AdaBD
Organisme : Universität Zürich (University of Zurich)
ID : K-33151-02-01
Organisme : Knut och Alice Wallenbergs Stiftelse (Knut and Alice Wallenberg Foundation)
ID : KAW 2021.0148
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : SOLAR ERC-2021-STG - 101042529
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 725355
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : BRAINCODES
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : SO 1636/2-1
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : 10001C_188878
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : 100014_165884
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : IZKSZ3_162109

Informations de copyright

© 2024. The Author(s).

Références

Olsson, A., Knapska, E. & Lindström, B. The neural and computational systems of social learning. Nat. Rev. Neurosci. 21, 197–212 (2020).
pubmed: 32221497 doi: 10.1038/s41583-020-0276-4
Tomasello, M., Davis-Dasilva, M., Camak, L. & Bard, K. Observational learning of tool-use by young chimpanzees. Hum. Evol. 2, 175–183 (1987).
doi: 10.1007/BF02436405
Meltzoff, A. N. & Marshall, P. J. Human infant imitation as a social survival circuit. Curr. Opin. Behav. Sci. 24, 130–136 (2018).
doi: 10.1016/j.cobeha.2018.09.006
Bandura, A. & Walters, R. H. Social learning theory. 1 (Englewood cliffs Prentice Hall, 1977).
Heyes, C. M. SOCIAL LEARNING IN ANIMALS: CATEGORIES AND MECHANISMS. Biol. Rev. 69, 207–231 (1994).
pubmed: 8054445 doi: 10.1111/j.1469-185X.1994.tb01506.x
Meltzoff, A. & Gopnik, A. The role of imitation in understanding persons and developing a theory of mind. In Understanding other minds (eds. Baron- Cohen, S., Tager-Flusberg, H. & Cohen, D. J.), (pp. 335–366) (New York: Oxford University Press).
Heyes, C. M. & Dawson, G. R. A Demonstration of Observational Learning in Rats Using a Bidirectional Control. Q. J. Exp. Psychol. Sect. B 42, 59–71 (1990).
Kang, P., Burke, C. J., Tobler, P. N. & Hein, G. Why We Learn Less from Observing Outgroups. J. Neurosci. 41, 144–152 (2021).
pubmed: 33203741 pmcid: 7786220 doi: 10.1523/JNEUROSCI.0926-20.2020
Burke, C. J., Tobler, P. N., Baddeley, M. & Schultz, W. Neural mechanisms of observational learning. Proc. Natl Acad. Sci. 107, 14431–14436 (2010).
pubmed: 20660717 pmcid: 2922583 doi: 10.1073/pnas.1003111107
Suzuki, S. et al. Learning to Simulate Others’ Decisions. Neuron 74, 1125–1137 (2012).
pubmed: 22726841 doi: 10.1016/j.neuron.2012.04.030
Charpentier, C. J., Iigaya, K. & O’Doherty, J. P. A Neuro-computational Account of Arbitration between Choice Imitation and Goal Emulation during Human Observational Learning. Neuron 106, 687–699.e7 (2020).
pubmed: 32187528 pmcid: 7244377 doi: 10.1016/j.neuron.2020.02.028
Jiang, Y., Mi, Q. & Zhu, L. Neurocomputational mechanism of real-time distributed learning on social networks. Nat. Neurosci. 26, 506–516 (2023).
pubmed: 36797365
Yoshida, K., Saito, N., Iriki, A. & Isoda, M. Representation of Others’ Action by Neurons in Monkey Medial Frontal Cortex. Curr. Biol. 21, 249–253 (2011).
pubmed: 21256015 doi: 10.1016/j.cub.2011.01.004
Ridderinkhof, K. R., Ullsperger, M., Crone, E. A. & Nieuwenhuis, S. The role of the medial frontal cortex in cognitive control. Science. 306, 443–447 (2004).
pubmed: 15486290 doi: 10.1126/science.1100301
Selbing, I., Lindström, B. & Olsson, A. Demonstrator skill modulates observational aversive learning. Cognition 133, 128–139 (2014).
pubmed: 25016187 doi: 10.1016/j.cognition.2014.06.010
Selbing, I. & Olsson, A. Beliefs about Others’ Abilities Alter Learning from Observation. Sci. Rep. 7, 1–10 (2017).
doi: 10.1038/s41598-017-16307-3
Biele, G., Rieskamp, J. & Gonzalez, R. Computational models for the combination of advice and individual learning. Cogn. Sci. 33, 206–242 (2009).
pubmed: 21585468 doi: 10.1111/j.1551-6709.2009.01010.x
Corriveau, K. & Harris, P. L. Choosing your informant: Weighing familiarity and recent accuracy. Dev. Sci. 12, 426–437 (2009).
pubmed: 19371367 doi: 10.1111/j.1467-7687.2008.00792.x
Pasquini, E. S., Corriveau, K. H., Koenig, M. & Harris, P. L. Preschoolers Monitor the Relative Accuracy of Informants. Dev. Psychol. 43, 1216–1226 (2007).
pubmed: 17723046 doi: 10.1037/0012-1649.43.5.1216
Behrens, T. E. J., Woolrich, M. W., Walton, M. E. & Rushworth, M. F. S. Learning the value of information in an uncertain world. Nat. Neurosci. 10, 1214–1221 (2007).
pubmed: 17676057 doi: 10.1038/nn1954
Kording, K., Blohm, G., Schrater, P. & Kay, K. Appreciating diversity of goals in computational neuroscience. (2018).
Seo, H., Cai, X., Donahue, C. H. & Lee, D. Neural correlates of strategic reasoning during competitive games. Science. 346, 340–343 (2014).
pubmed: 25236468 pmcid: 4201877 doi: 10.1126/science.1256254
Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S. & Cohen, J. D. Conflict monitoring and cognitive control. Psychol. Rev. 108, 624–652 (2001).
pubmed: 11488380 doi: 10.1037/0033-295X.108.3.624
Holroyd, C. B., Larsen, J. T. & Cohen, J. D. Context dependence of the event‐related brain potential associated with reward and punishment. Psychophysiology 41, 245–253 (2004).
Mahmoodi, A. et al. A frontopolar-temporal circuit determines the impact of social information in macaque decision making. Neuron. 112, 84–92 (2024).
Najar, A., Bonnet, E., Bahrami, B. & Palminteri, S. The actions of others act as a pseudo-reward to drive imitation in the context of social reinforcement learning. PLoS Biol. 18, 1–25 (2020).
doi: 10.1371/journal.pbio.3001028
Golkar, A., Castro, V. & Olsson, A. Social learning of fear and safety is determined by the demonstrator’s racial group. Biol. Lett. 11, 20140817 (2015).
pubmed: 25631229 pmcid: 4321149 doi: 10.1098/rsbl.2014.0817
Buttelmann, D., Zmyj, N., Daum, M. & Carpenter, M. Selective Imitation of In-Group Over Out-Group Members in 14-Month-Old Infants. Child Dev. 84, 422–428 (2013).
pubmed: 23006251 doi: 10.1111/j.1467-8624.2012.01860.x
Venkatraman, V. & Huettel, S. A. Strategic control in decision-making under uncertainty. Eur. J. Neurosci. 35, 1075–1082 (2012).
pubmed: 22487037 pmcid: 3325517 doi: 10.1111/j.1460-9568.2012.08009.x
Ereira, S. et al. Social training reconfigures prediction errors to shape Self-Other boundaries. Nat. Commun. 11, 3030 (2020).
pubmed: 32541779 pmcid: 7295766 doi: 10.1038/s41467-020-16856-8
Wittmann, M. K. et al. Predictive decision making driven by multiple time-linked reward representations in the anterior cingulate cortex. Nat. Commun. 7, 1–13 (2016).
doi: 10.1038/ncomms12327
Wittmann, M. K. et al. Causal manipulation of self-other mergence in the dorsomedial prefrontal cortex. Neuron 109, 2353–2361 (2021).
pubmed: 34171289 pmcid: 8326319 doi: 10.1016/j.neuron.2021.05.027
Wittmann, M. K. et al. Self-other mergence in the frontal cortex during cooperation and competition. Neuron 91, 482–493 (2016).
pubmed: 27477020 pmcid: 4961240 doi: 10.1016/j.neuron.2016.06.022
Sul, S. et al. Spatial gradient in value representation along the medial prefrontal cortex reflects individual differences in prosociality. Proc. Natl Acad. Sci. 112, 201423895 (2015).
doi: 10.1073/pnas.1423895112
Piva, M. et al. The dorsomedial prefrontal cortex computes task-invariant relative subjective value for self and other. Elife 8, e44939 (2019).
pubmed: 31192786 pmcid: 6565363 doi: 10.7554/eLife.44939
Ferrari, C., Vecchi, T., Todorov, A. & Cattaneo, Z. Interfering with activity in the dorsomedial prefrontal cortex via TMS affects social impressions updating. Cogn. Affect. Behav. Neurosci. 16, 626–634 (2016).
pubmed: 27012713 doi: 10.3758/s13415-016-0419-2
Izuma, K. & Adolphs, R. Social manipulation of preference in the human brain. Neuron 78, 563–573 (2013).
pubmed: 23664619 pmcid: 3695714 doi: 10.1016/j.neuron.2013.03.023
Izuma, K. et al. A Causal Role for Posterior Medial Frontal Cortex in Choice-Induced Preference Change. J. Neurosci. 35, 3598–3606 (2015).
pubmed: 25716858 pmcid: 6605562 doi: 10.1523/JNEUROSCI.4591-14.2015
Klucharev, V., Hytönen, K., Rijpkema, M., Smidts, A. & Fernández, G. Reinforcement Learning Signal Predicts Social Conformity. Neuron 61, 140–151 (2009).
pubmed: 19146819 doi: 10.1016/j.neuron.2008.11.027
Klucharev, V., Munneke, M. A. M., Smidts, A. & Fernandez, G. Downregulation of the Posterior Medial Frontal Cortex Prevents Social Conformity. J. Neurosci. 31, 11934–11940 (2011).
pubmed: 21849554 pmcid: 6623179 doi: 10.1523/JNEUROSCI.1869-11.2011
Wilson, R. C. & Collins, A. G. E. Ten simple rules for the computational modeling of behavioral data. Elife 8, 1–33 (2019).
doi: 10.7554/eLife.49547
Silvetti, M., Vassena, E., Abrahamse, E. & Verguts, T. Dorsal anterior cingulate-midbrain ensemble as a reinforcement. PLoS Comput. Biol. 14, e1006370 (2018).
pubmed: 30142152 pmcid: 6126878 doi: 10.1371/journal.pcbi.1006370
Soutschek, A., Taylo, P. C. J., Müller, H. J. & Schubert, T. Dissociable networks control conflict during perception and response selection: A transcranial magnetic stimulation study. J. Neurosci. 33, 5647–5654 (2013).
pubmed: 23536079 pmcid: 6705084 doi: 10.1523/JNEUROSCI.4768-12.2013
Cavanagh, J. F., Cohen, M. X. & Allen, J. J. B. Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring. J. Neurosci. 29, 98–105 (2009).
pubmed: 19129388 pmcid: 2742325 doi: 10.1523/JNEUROSCI.4137-08.2009
Kerns, J. G. et al. Anterior Cingulate Conflict Monitoring and Adjustments in Control. Science. 303, 1023–1026 (2004).
pubmed: 14963333 doi: 10.1126/science.1089910
Danielmeier, C., Eichele, T., Forstmann, B. U., Tittgemeyer, M. & Ullsperger, M. Posterior Medial Frontal Cortex Activity Predicts Post-Error Adaptations in Task-Related Visual and Motor Areas. J. Neurosci. 31, 1780–1789 (2011).
pubmed: 21289188 pmcid: 6623722 doi: 10.1523/JNEUROSCI.4299-10.2011
Soutschek, A., Ruff, C. C., Strombach, T., Kalenscher, T. & Tobler, P. N. Brain stimulation reveals crucial role of overcoming self-centeredness in self-control. Sci. Adv. 2, 2–10 (2016).
doi: 10.1126/sciadv.1600992
Rossi, S. et al. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 120, 2008–2039 (2009).
pubmed: 19833552 pmcid: 3260536 doi: 10.1016/j.clinph.2009.08.016
Ebner, N. C., Riediger, M. & Lindenberger, U. FACES-a database of facial expressions in young, middle-aged, and older women and men: Development and validation. Behav. Res. Methods 42, 351–362 (2010).
pubmed: 20160315 doi: 10.3758/BRM.42.1.351
Davis, M. H. Measuring individual differences in empathy: Evidence for a multidimensional approach. J. Pers. Soc. Psychol. 44, 113–126 (1983).
doi: 10.1037/0022-3514.44.1.113
Christie, R. & Geis, F. L. Studies in machiavellianism. (Academic Press, 2013).
Raven, J. C. Guide to the standard progressive matrices: Sets A, B, C, D and E. (HK Lewis, 1960).
Huang, Y. Z., Edwards, M. J., Rounis, E., Bhatia, K. P. & Rothwell, J. C. Theta burst stimulation of the human motor cortex. Neuron 45, 201–206 (2005).
pubmed: 15664172 doi: 10.1016/j.neuron.2004.12.033
Stokes, M. G. et al. Distance-adjusted motor threshold for transcranial magnetic stimulation. Clin Neurophysiol. 118, 1617–1625 (2007).
Huang, Y. Z., Edwards, M. J., Rounis, E., Bhatia, K. P. & Rothwell, J. C. Theta burst stimulation of the human motor cortex. Neuron. 45, 201–206 (2005).
Wagenmakers, E. J. A practical solution to the pervasive problems of p values. Psychon. Bull. Rev. 14, 779–804 (2007).
pubmed: 18087943 doi: 10.3758/BF03194105
Wunderlich, K., Smittenaar, P. & Dolan, R. J. Dopamine Enhances Model-Based over Model-Free Choice Behavior. Neuron 75, 418–424 (2012).
pubmed: 22884326 pmcid: 3417237 doi: 10.1016/j.neuron.2012.03.042
Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423 (1948).
doi: 10.1002/j.1538-7305.1948.tb01338.x
Steingroever, H., Wetzels, R., Horstmann, A., Neumann, J. & Wagenmakers, E. J. Performance of healthy participants on the Iowa Gambling Task. Psychol Assess. 25, 180 (2013).
Hill, C. A. et al. A causal account of the brain network computations underlying strategic social behavior. Nat Neurosci. 20, 1142–1149 (2017).
Su, Y. S. & Yajima, M. R2jags: A Package for Running jags from R. R package version 0.03-08, http://CRAN.R-project.org/package=R2jags . (2012).
Spiegelhalter, D. J., Best, N. G., Carlin, B. P., & Van Der Linde, A. Bayesian measures of model complexity and fit. J. R. Statist. Soc. B 64, 583–639 (2002).

Auteurs

Pyungwon Kang (P)

Zurich Center for Neuroeconomics, Department of Economics, University of Zurich, Zurich, Switzerland. pyungwon.kang@gmail.com.
ORCID: 0009-0006-7116-5904

Marius Moisa (M)

Zurich Center for Neuroeconomics, Department of Economics, University of Zurich, Zurich, Switzerland.
ORCID: 0000-0001-9789-3383

Björn Lindström (B)

Department of Clinical Neuroscience, Division for Psychology, Karolinska Institute, Stockholm, Sweden.
ORCID: 0000-0002-2121-8370

Alexander Soutschek (A)

Ludwig Maximilian University Munich, Department for Psychology, Munich, Germany.
ORCID: 0000-0001-8438-7721

Christian C Ruff (CC)

Zurich Center for Neuroeconomics, Department of Economics, University of Zurich, Zurich, Switzerland.
ORCID: 0000-0002-3964-2364

Philippe N Tobler (PN)

Zurich Center for Neuroeconomics, Department of Economics, University of Zurich, Zurich, Switzerland.
Neuroscience Center Zurich, ETH Zurich and University of Zurich, Zurich, Switzerland.
ORCID: 0000-0002-4915-9448

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Classifications MeSH

questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Lobe frontal › Cortex préfrontal › Causal involvement of dorsomedial prefrontal...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Causal involvement of dorsomedial prefrontal...
questionsmedicales.fr › Thérapeutique › Magnétothérapie › Stimulation magnétique transcrânienne › Causal involvement of dorsomedial prefrontal...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Jeune adulte › Causal involvement of dorsomedial prefrontal...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Causal involvement of dorsomedial prefrontal...
questionsmedicales.fr › Phénomènes psychologiques › Psychologie appliquée › Apprentissage › Causal involvement of dorsomedial prefrontal...
questionsmedicales.fr › Phénomènes psychologiques › Psychologie appliquée › Apprentissage › Apprentissage social › Causal involvement of dorsomedial prefrontal...