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A brain network supporting social influences in human decision-making.

ABSTRACT: Humans learn from their own trial-and-error experience and observing others. However, it remains unknown how brain circuits compute expected values when direct learning and social learning coexist in uncertain environments. Using a multiplayer reward learning paradigm with 185 participants (39 being scanned) in real time, we observed that individuals succumbed to the group when confronted with dissenting information but observing confirming information increased their confidence. Leveraging computational modeling and functional magnetic resonance imaging, we tracked direct valuation through experience and vicarious valuation through observation and their dissociable, but interacting neural representations in the ventromedial prefrontal cortex and the anterior cingulate cortex, respectively. Their functional coupling with the right temporoparietal junction representing instantaneous social information instantiated a hitherto uncharacterized social prediction error, rather than a reward prediction error, in the putamen. These findings suggest that an integrated network involving the brain's reward hub and social hub supports social influence in human decision-making.

SUBMITTER: Zhang L

PROVIDER: S-EPMC7438106 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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A brain network supporting social influences in human decision-making.

Zhang Lei L Gläscher Jan J

Science advances 20200819 34

Humans learn from their own trial-and-error experience and observing others. However, it remains unknown how brain circuits compute expected values when direct learning and social learning coexist in uncertain environments. Using a multiplayer reward learning paradigm with 185 participants (39 being scanned) in real time, we observed that individuals succumbed to the group when confronted with dissenting information but observing confirming information increased their confidence. Leveraging comp ...[more]

PMID: 32875112

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Project description:Social living animals need to adjust the expression of their behavior to their status within the group and to changes in social context and this ability (social plasticity) has an impact on their Darwinian fitness. At the proximate level social plasticity must rely on neuroplasticity in the brain social decision-making network (SDMN) that underlies the expression of social behavior, such that the same neural circuit may underlie the expression of different behaviors depending on social context. Here we tested this hypothesis in zebrafish by characterizing the gene expression response in the SDMN to changes in social status of a set of genes involved in different types of neural plasticity: bdnf, involved in changes in synaptic strength; npas4, involved in contextual learning and dependent establishment of GABAergic synapses; neuroligins (nlgn1 and nlgn2) as synaptogenesis markers; and genes involved in adult neurogenesis (wnt3 and neurod). Four social phenotypes were experimentally induced: Winners and Losers of a real-opponent interaction; Mirror-fighters, that fight their own image in a mirror and thus do not experience a change in social status despite the expression of aggressive behavior; and non-interacting fish, which were used as a reference group. Our results show that each social phenotype (i.e., Winners, Losers, and Mirror-fighters) present specific patterns of gene expression across the SDMN, and that different neuroplasticity genes are differentially expressed in different nodes of the network (e.g., BDNF in the dorsolateral telencephalon, which is a putative teleost homolog of the mammalian hippocampus). Winners expressed unique patterns of gene co-expression across the SDMN, whereas in Losers and Mirror-fighters the co-expression patterns were similar in the dorsal regions of the telencephalon and in the supracommissural nucleus of the ventral telencephalic area, but differents in the remaining regions of the ventral telencephalon. These results indicate that social plasticity relies on multiple neuroplasticity mechanisms across the SDMN, and that there is not a single neuromolecular module underlying this type of behavioral flexibility.

Project description:ObjectivesDespite significant public health emphasis on unintended pregnancy prevention among adolescent girls and young women in Sub-Saharan Africa, there is a gap in understanding how adolescents' own reproductive priorities and the social influences on their decision-making align and compete. We examined the social context of contraceptive decision-making among Kenyan female adolescents.MethodsUsing community-based sampling, we conducted 40 in-depth interviews and 6 focus group discussions among sexually-active or partnered adolescent girls and young women aged 15-19 in the Nyanza region of Kenya. We analyzed the data in Dedoose using an inductive, grounded theory approach, and developed a conceptual model from the data illustrating social influences on adolescent contraceptive decision-making.ResultsParticipants viewed adolescent pregnancy as unacceptable, and described severe social, financial, and health consequences of unintended pregnancy, including abortion under unsafe conditions. Yet, their contraceptive behaviors often did not reflect their desire to delay pregnancy. Contraceptive decision-making was influenced by multiple social factors, centering on the intersecting stigmas of adolescent female sexuality, pregnancy, and contraceptive use, as well as unequal power in sexual relationships. To prioritize pregnancy prevention, adolescents must navigate conflicting social norms and power dynamics, and put their perceived future fertility at risk.ConclusionsContraceptive decision-making among Kenyan female adolescents is strongly influenced by opposing social norms within families, communities, and sexual relationships, which compel them to risk stigma whether they use a contraceptive method or become pregnant as adolescents. These findings put into perspective adolescents' seemingly incongruent pregnancy preferences and contraceptive behaviors. Interventions to address adolescent unintended pregnancy should focus on supporting adolescent decision-making agency, addressing fertility-related contraceptive concerns, and promoting innovative contraceptive access points rather than increasing contraceptive prevalence.

Project description:Social living animals have to adjust their behavior to rapid changes in the social environment. It has been hypothesized that the expression of social behavior is better explained by the activity pattern of a diffuse social decision-making network (SDMN) in the brain than by the activity of a single brain region. In this study, we tested the hypothesis that it is the assessment that individuals make of the outcome of the fights, rather than the expression of aggressive behavior per se, that triggers changes in the pattern of activation of the SDMN which are reflected in socially driven behavioral profiles (e.g., dominant vs. subordinate specific behaviors). For this purpose, we manipulated the perception of the outcome of an agonistic interaction in an African cichlid fish (Oreochromis mossambicus) and assessed if either the perception of outcome or fighting by itself was sufficient to trigger rapid changes in the activity of the SDMN. We have used the expression of immediate early genes (c-fos and egr-1) as a proxy to measure the neuronal activity in the brain. Fish fought their own image on a mirror for 15 min after which they were allocated to one of three conditions for the two last minutes of the trial: (1) they remained fighting the mirror image (no outcome treatment); (2) the mirror was lifted and a dominant male that had just won a fight was presented behind a transparent partition (perception of defeat treatment); and (3) the mirror was lifted and a subordinate male that had just lost a fight was presented behind a transparent partition (perception of victory treatment). Results show that these short-term social interactions elicit distinct patterns in the SDMN and that the perception of the outcome was not a necessary condition to trigger a SDMN response as evidenced in the second treatment (perception of defeat treatment). We suggest that the mutual assessment of relative fighting behavior drives these acute changes in the state of the SDMN.

Project description:Although aggression is more prevalent in males, females also express aggressive behaviors and in specific ecological contexts females can be more aggressive than males. The aim of this work is to assess sex differences in aggression and to characterize the patterns of neuronal activation of the social-decision making network (SDMN) in response to intra-sexual aggression in both male and female zebrafish. Adult fish were exposed to social interaction with a same-sex opponent and all behavioral displays, latency, and time of resolution were quantified. After conflict resolution, brains were sampled and sex differences on functional connectivity throughout the SDMN were assessed by immunofluorescence of the neuronal activation marker pS6. Results suggest that both sexes share a similar level of motivation for aggression, but female encounters show shorter conflict resolution and a preferential use of antiparallel displays instead of overt aggression, showing a reduction of putative maladaptive effects. Although there are no sex differences in the neuronal activation in any individual brain area from the SDMN, agonistic interactions increased neuronal activity in most brain areas in both sexes. Functional connectivity was assessed using bootstrapped adjacency matrices that capture the co-activation of the SDMN nodes. Male winners increased the overall excitation and showed no changes in inhibition across the SDMN, whereas female winners and both male and female losers showed a decrease in both excitation and inhibition of the SDMN in comparison to non-interacting control fish. Moreover, network centrality analysis revealed both shared hubs, as well as sex-specific hubs, between the sexes for each social condition in the SDMN. In summary, a distinct neural activation pattern associated with social experience during fights was found for each sex, suggesting a sex-specific differential activation of the social brain as a consequence of social experience. Overall, our study adds insights into sex differences in agonistic behavior and on the neuronal architecture of intrasexual aggression in zebrafish.

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A brain network supporting social influences in human decision-making.

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A brain network supporting social influences in human decision-making.

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