Reduced effects of social feedback on learning in Turner syndrome.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
22 09 2023
22 09 2023
Historique:
received:
31
03
2023
accepted:
12
09
2023
medline:
25
9
2023
pubmed:
23
9
2023
entrez:
22
9
2023
Statut:
epublish
Résumé
Turner syndrome is a genetic condition caused by a complete or partial loss of one of the X chromosomes. Previous studies indicate that Turner syndrome is associated with challenges in social skills, but the underlying mechanisms remain largely unexplored. A possible mechanism is a reduced social influence on learning. The current study examined the impact of social and non-social feedback on learning in women with Turner syndrome (n = 35) and a sex- and age-matched control group (n = 37). Participants were instructed to earn points by repeatedly choosing between two stimuli with unequal probabilities of resulting in a reward. Mastering the task therefore required participants to learn through feedback which of the two stimuli was more likely to be rewarded. Data were analyzed using computational modeling and analyses of choice behavior. Social feedback led to a more explorative choice behavior in the control group, resulting in reduced learning compared to non-social feedback. No effects of social feedback on learning were found in Turner syndrome. The current study thus indicates that women with Turner syndrome may be less sensitive to social influences on reinforcement learning, than the general population.
Identifiants
pubmed: 37739980
doi: 10.1038/s41598-023-42628-7
pii: 10.1038/s41598-023-42628-7
pmc: PMC10516979
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
15858Informations de copyright
© 2023. Springer Nature Limited.
Références
Berglund, A. et al. Changes in the cohort composition of turner syndrome and severe non-diagnosis of Klinefelter, 47, XXX and 47, XYY syndrome: A nationwide cohort study. Orphanet J. Rare Dis. 14, 16. https://doi.org/10.1186/s13023-018-0976-2 (2019).
doi: 10.1186/s13023-018-0976-2
pubmed: 30642344
pmcid: 6332849
Nielsen, J. & Wohlert, M. Chromosome abnormalities found among 34,910 newborn children: Results from a 13-year incidence study in Arhus, Denmark. Hum. Genet. 87, 81–83 (1991).
doi: 10.1007/BF01213097
pubmed: 2037286
Ye, M., Yeh, J., Kosteria, I. & Li, L. Progress in fertility preservation strategies in Turner syndrome. Front. Med. (Lausanne) 7, 3. https://doi.org/10.3389/fmed.2020.00003 (2020).
doi: 10.3389/fmed.2020.00003
pubmed: 32039223
Gravholt, C. H. et al. The changing face of Turner syndrome. Endocr. Rev. https://doi.org/10.1210/endrev/bnac016 (2022).
doi: 10.1210/endrev/bnac016
Gravholt, C. H., Viuff, M. H., Brun, S., Stochholm, K. & Andersen, N. H. Turner syndrome: Mechanisms and management. Nat. Rev. Endocrinol. 15, 601–614. https://doi.org/10.1038/s41574-019-0224-4 (2019).
doi: 10.1038/s41574-019-0224-4
pubmed: 31213699
Hong, D. S. & Reiss, A. L. Cognitive and neurological aspects of sex chromosome aneuploidies. Lancet Neurol. 13, 306–318. https://doi.org/10.1016/S1474-4422(13)70302-8 (2014).
doi: 10.1016/S1474-4422(13)70302-8
pubmed: 24556008
Hong, D. S., Scaletta Kent, J. & Kesler, S. Cognitive profile of Turner syndrome. Dev. Disabil. Res. Rev. 15, 270–278 (2009).
doi: 10.1002/ddrr.79
pubmed: 20014362
pmcid: 3114458
Björlin Avdic, H. et al. Cognitive profile in adult women with turner syndrome: IQ split and associations with ADHD and ASD. Cogn. Neuropsychiatry 28, 207–225. https://doi.org/10.1080/13546805.2023.2209312 (2023).
doi: 10.1080/13546805.2023.2209312
pubmed: 37165648
Green, T. et al. Effect of sex chromosome number variation on attention-deficit/hyperactivity disorder symptoms, executive function, and processing speed. Dev. Med. Child Neurol. 64, 331–339. https://doi.org/10.1111/dmcn.15020 (2022).
doi: 10.1111/dmcn.15020
pubmed: 34431088
Hutaff-Lee, C., Bennett, E., Howell, S. & Tartaglia, N. Clinical developmental, neuropsychological, and social-emotional features of Turner syndrome. Am. J. Med. Genet. Part C-Semin. Med. Genet. 181, 126–134. https://doi.org/10.1002/ajmg.c.31687 (2019).
doi: 10.1002/ajmg.c.31687
pubmed: 30767374
Green, T. et al. Elucidating X chromosome influences on attention deficit hyperactivity disorder and executive function. J. Psychiatr. Res. 68, 217–225. https://doi.org/10.1016/j.jpsychires.2015.06.021 (2015).
doi: 10.1016/j.jpsychires.2015.06.021
pubmed: 26228422
pmcid: 4528918
Mccauley, E., Feuillan, P., Kushner, H. & Ross, J. L. Psychosocial development in adolescents with Turner syndrome. J. Dev. Behav. Pediatr. 22, 360–365 (2001).
doi: 10.1097/00004703-200112000-00003
pubmed: 11773800
Wolstencroft, J. & Skuse, D. Social skills and relationships in Turner syndrome. Curr. Opin. Psychiatry 32, 85–91. https://doi.org/10.1097/yco.0000000000000472 (2019).
doi: 10.1097/yco.0000000000000472
pubmed: 30407217
Liedmeier, A. et al. Psychosocial well-being and quality of life in women with Turner syndrome. Psychoneuroendocrinology 113, 104548. https://doi.org/10.1016/j.psyneuen.2019.104548 (2020).
doi: 10.1016/j.psyneuen.2019.104548
pubmed: 31923612
Wolstencroft, J., Mandy, W. & Skuse, D. Mental health and neurodevelopment in children and adolescents with Turner syndrome. Womens Health (Lond) 18, 17455057221133636. https://doi.org/10.1177/17455057221133635 (2022).
doi: 10.1177/17455057221133635
pubmed: 36472167
Hong, D. S., Dunkin, B. & Reiss, A. L. Psychosocial functioning and social cognitive processing in girls with Turner syndrome. J. Dev. Behav. Pediatr. 32, 512–520. https://doi.org/10.1097/DBP.0b013e3182255301 (2011).
doi: 10.1097/DBP.0b013e3182255301
pubmed: 21743350
pmcid: 3179767
Lepage, J. F., Dunkin, B., Hong, D. S. & Reiss, A. L. Impact of cognitive profile on social functioning in prepubescent females with Turner syndrome. Child Neuropsychol. 19, 161–172. https://doi.org/10.1080/09297049.2011.647900 (2013).
doi: 10.1080/09297049.2011.647900
pubmed: 22372383
Wolstencroft, J., Mandy, W. & Skuse, D. Experiences of social interaction in young women with Turner syndrome: A qualitative study. Child Care Health Dev. 46, 46–55. https://doi.org/10.1111/cch.12710 (2020).
doi: 10.1111/cch.12710
pubmed: 31322282
Noordman, I. D. et al. Socioeconomic status in patients with Turner syndrome. Compr. Psychoneuroendocrinol. 5, 100030. https://doi.org/10.1016/j.cpnec.2021.100030 (2021).
doi: 10.1016/j.cpnec.2021.100030
pubmed: 35754454
pmcid: 9216711
Suzigan, L. Z., de Paiva e Silva, R. B., Guerra-Júnior, G., Marini, S. H. & Maciel-Guerra, A. T. Social skills in women with Turner Syndrome. Scand. J. Psychol. 52, 440–447. https://doi.org/10.1111/j.1467-9450.2011.00887.x (2011).
doi: 10.1111/j.1467-9450.2011.00887.x
pubmed: 21534980
Lawrence, K., Kuntsi, J., Coleman, M., Campbell, R. & Skuse, D. Face and emotion recognition deficits in Turner syndrome: A possible role for X-linked genes in amygdala development. Neuropsychology 17, 39–49 (2003).
doi: 10.1037/0894-4105.17.1.39
pubmed: 12597072
Mazzola, F. et al. Eye tracking and fear recognition deficits in Turner syndrome. Soc. Neurosci. 1, 259–269. https://doi.org/10.1080/17470910600989912 (2006).
doi: 10.1080/17470910600989912
pubmed: 18633792
Hong, D. S., Bray, S., Haas, B. W., Hoeft, F. & Reiss, A. L. Aberrant neurocognitive processing of fear in young girls with Turner syndrome. Soc. Cogn. Affect. Neurosci. 9, 255–264. https://doi.org/10.1093/scan/nss133 (2014).
doi: 10.1093/scan/nss133
pubmed: 23171616
Anaki, D., Zadikov Mor, T., Gepstein, V. & Hochberg, Z. Face perception in women with Turner syndrome and its underlying factors. Neuropsychologia 90, 274–285. https://doi.org/10.1016/j.neuropsychologia.2016.08.024 (2016).
doi: 10.1016/j.neuropsychologia.2016.08.024
pubmed: 27565637
Olsson, A., Knapska, E. & Lindström, B. The neural and computational systems of social learning. Nat. Rev. Neurosci. 21, 197–212. https://doi.org/10.1038/s41583-020-0276-4 (2020).
doi: 10.1038/s41583-020-0276-4
pubmed: 32221497
Frith, C. D. & Frith, U. Mechanisms of social cognition. Annu. Rev. Psychol. 63, 287–313 (2012).
doi: 10.1146/annurev-psych-120710-100449
pubmed: 21838544
Sanders, G. S. Driven by distraction: An integrative review of social facilitation theory and research. J. Exp. Soc. Psychol. 17, 227–251 (1981).
doi: 10.1016/0022-1031(81)90024-X
Kendal, R. L. et al. Social learning strategies: Bridge-building between fields. Trends Cogn. Sci. 22, 651–665 (2018).
doi: 10.1016/j.tics.2018.04.003
pubmed: 29759889
Laland, K. N. Social learning strategies. Anim. Learn. Behav. 32, 4–14 (2004).
doi: 10.3758/BF03196002
Anaki, D., Zadikov-Mor, T., Gepstein, V. & Hochberg, Z. Normal performance in non-visual social cognition tasks in women with Turner syndrome. Front. Endocrinol. (Lausanne) 9, 171. https://doi.org/10.3389/fendo.2018.00171 (2018).
doi: 10.3389/fendo.2018.00171
pubmed: 29780353
Zhang, L., Lengersdorff, L., Mikus, N., Gläscher, J. & Lamm, C. Using reinforcement learning models in social neuroscience: Frameworks, pitfalls and suggestions of best practices. Soc. Cogn. Affect. Neurosci. 15, 695–707. https://doi.org/10.1093/scan/nsaa089 (2020).
doi: 10.1093/scan/nsaa089
pubmed: 32608484
pmcid: 7393303
Lee, D., Seo, H. & Jung, M. W. Neural basis of reinforcement learning and decision making. Annu. Rev. Neurosci. 35, 287–308. https://doi.org/10.1146/annurev-neuro-062111-150512 (2012).
doi: 10.1146/annurev-neuro-062111-150512
pubmed: 22462543
pmcid: 3490621
Mehlhorn, K. et al. Unpacking the exploration–exploitation tradeoff: A synthesis of human and animal literatures. Decision 2, 191 (2015).
doi: 10.1037/dec0000033
Rmus, M., McDougle, S. D. & Collins, A. G. The role of executive function in shaping reinforcement learning. Curr. Opin. Behav. Sci. 38, 66–73 (2021).
doi: 10.1016/j.cobeha.2020.10.003
pubmed: 35194556
Lindström, B., Golkar, A., Jangard, S., Tobler, P. N. & Olsson, A. Social threat learning transfers to decision making in humans. Proc. Natl. Acad. Sci. U. S. A. 116, 4732–4737. https://doi.org/10.1073/pnas.1810180116 (2019).
doi: 10.1073/pnas.1810180116
pubmed: 30760585
pmcid: 6410767
Flores, A., Münte, T. F. & Donamayor, N. Event-related EEG responses to anticipation and delivery of monetary and social reward. Biol. Psychol. 109, 10–19 (2015).
doi: 10.1016/j.biopsycho.2015.04.005
pubmed: 25910956
Lin, A., Adolphs, R. & Rangel, A. Social and monetary reward learning engage overlapping neural substrates. Soc. Cogn. Affect. Neurosci. 7, 274–281 (2012).
doi: 10.1093/scan/nsr006
pubmed: 21427193
Garg, K., Kello, C. T. & Smaldino, P. E. Individual exploration and selective social learning: Balancing exploration–exploitation trade-offs in collective foraging. J. R. Soc. Interface 19, 20210915 (2022).
doi: 10.1098/rsif.2021.0915
pubmed: 35472271
pmcid: 9042579
Yechiam, E., Arshavsky, O., Shamay-Tsoory, S. G., Yaniv, S. & Aharon, J. Adapted to explore: Reinforcement learning in autistic spectrum conditions. Brain Cogn. 72, 317–324. https://doi.org/10.1016/j.bandc.2009.10.005 (2010).
doi: 10.1016/j.bandc.2009.10.005
pubmed: 19913345
Espinosa, L. et al. Enhanced social learning of threat in adults with autism. Mol. Autism 11, 71. https://doi.org/10.1186/s13229-020-00375-w (2020).
doi: 10.1186/s13229-020-00375-w
pubmed: 32962741
pmcid: 7510115
Frey, A. L., Frank, M. J. & McCabe, C. Social reinforcement learning as a predictor of real-life experiences in individuals with high and low depressive symptomatology. Psychol. Med. 51, 408–415. https://doi.org/10.1017/s0033291719003222 (2021).
doi: 10.1017/s0033291719003222
pubmed: 31831095
Pike, A. C. & Robinson, O. J. Reinforcement learning in patients with mood and anxiety disorders vs control individuals: A systematic review and meta-analysis. JAMA Psychiatry 79, 313–322. https://doi.org/10.1001/jamapsychiatry.2022.0051 (2022).
doi: 10.1001/jamapsychiatry.2022.0051
pubmed: 35234834
pmcid: 8892374
Guath, M., Willfors, C., Avdic, H. B., Nordgren, A. & Kleberg, J. L. Pupillary response in reward processing in adults with major depressive disorder in remission. J. Int. Neuropsychol. Soc. 29, 306–315 (2023).
doi: 10.1017/S1355617722000224
pubmed: 35545874
Kleberg, J. L. et al. Social feedback enhances learning in Williams syndrome. Sci. Rep. 13, 164. https://doi.org/10.1038/s41598-022-26055-8 (2023)
doi: 10.1038/s41598-022-26055-8
pubmed: 36599864
pmcid: 9813264
Brown, W. E. et al. A volumetric study of parietal lobe subregions in Turner syndrome. Dev. Med. Child Neurol. 46, 607–609 (2004).
doi: 10.1111/j.1469-8749.2004.tb01024.x
pubmed: 15344520
pmcid: 3051360
Knickmeyer, R. C. & Hooper, S. R. The deep biology of cognition: Moving toward a comprehensive neurodevelopmental model of Turner syndrome. Am. J. Med. Genet. 181, 91–99. https://doi.org/10.1002/ajmg.c.31679 (2019).
doi: 10.1002/ajmg.c.31679
pubmed: 30741475
Wilson, R. C. & Ten Collins, A. G. E. simple rules for the computational modeling of behavioral data. eLife 8, e49547. https://doi.org/10.7554/eLife.49547 (2019).
doi: 10.7554/eLife.49547
pubmed: 31769410
pmcid: 6879303
Lee, D., Seo, H. & Jung, M. W. Neural basis of reinforcement learning and decision making. Annu. Rev. Neurosci. 35, 287–308 (2012).
doi: 10.1146/annurev-neuro-062111-150512
pubmed: 22462543
pmcid: 3490621
Sutton, R. S. & Barto, A. G. Reinforcement Learning: An Introduction (MIT Press, 2018).
Pike, A. C. & Robinson, O. J. Reinforcement learning in patients with mood and anxiety disorders vs control individuals: A systematic review and meta-analysis. JAMA Psychiatry (2022).
Manning, C., Kilner, J., Neil, L., Karaminis, T. & Pellicano, E. Children on the autism spectrum update their behaviour in response to a volatile environment. Dev. Sci. 20, e12435 (2017).
doi: 10.1111/desc.12435
pubmed: 27496590
Insel, T. et al. Research domain criteria (RDoC): Toward a new classification framework for research on mental disorders. Am. J. Psychiatry. 167, 748–751. https://doi.org/10.1176/appi.ajp.2010.09091379 (2010).
doi: 10.1176/appi.ajp.2010.09091379
pubmed: 20595427
Wechsler, D. Wechsler adult intelligence scale–fourth edition, Swedish version. Pearson Assessment (2010).
Bridges, D., Pitiot, A., MacAskill, M. R. & Peirce, J. W. The timing mega-study: Comparing a range of experiment generators, both lab-based and online. PeerJ 8, e9414 (2020).
doi: 10.7717/peerj.9414
pubmed: 33005482
pmcid: 7512138
Lenth, R. V. Estimated marginal means, aka least-squares means [R Package Emmeans Version 1.6. 0]. Comprehensive R Archive Network (CRAN) (2021).
Bates, D., Maechler, M. & Bolker, B. Walker., S. Fitting linear mixed-effects models using lme4. J Stat Softw 67, 1–48 (2015).
doi: 10.18637/jss.v067.i01
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. Package ‘lmertest’. R package version 2, 734 (2015).
Green, P. & MacLeod, C. J. SIMR: An R package for power analysis of generalized linear mixed models by simulation. Methods Ecol. Evol. 7, 493–498 (2016).
doi: 10.1111/2041-210X.12504
Villano, W. J. et al. Individual differences in naturalistic learning link negative emotionality to the development of anxiety. Sci. Adv. 9, eadd2976 (2023).
doi: 10.1126/sciadv.add2976
pubmed: 36598977
pmcid: 9812386
Huys, Q. J., Russek, E. M., Abitante, G., Kahnt, T. & Gollan, J. K. Components of behavioral activation therapy for depression engage specific reinforcement learning mechanisms in a pilot study. Comput. Psychiatry 6 (2022).
Frith, C. D. & Frith, U. Mechanisms of social cognition. Annu. Rev. Psychol. 63, 287–313 (2012).
doi: 10.1146/annurev-psych-120710-100449
pubmed: 21838544
Feinberg, J. M. & Aiello, J. R. Social facilitation: A test of competing theories 1. J. Appl. Soc. Psychol. 36, 1087–1109 (2006).
doi: 10.1111/j.0021-9029.2006.00032.x
Tschida, J. E. & Yerys, B. E. A systematic review of the positive valence system in autism spectrum disorder. Neuropsychol. Rev. 31, 58–88 (2021).
doi: 10.1007/s11065-020-09459-z
pubmed: 33174110