Jepma, M. | Search bioRxiv

bioRxiv2020

Evoked pain intensity representation is distributed across brain systems: A multistudy mega-analysis

Information is coded in the brain at different scales for different phenomena: locally, distributed across regions and networks, and globally. For pain, the scale of representation is controversial. Although generally believed to be an integrated cognitive and sensory phenomenon implicating diverse brain systems, quantitative characterizations of which regions and networks are sufficient to represent pain are lacking. In this meta-analysis (or mega-analysis) using data from 289 participants across 10 studies, we use model comparison combined with multivariate predictive models to investigate the spatial scale and location of acute pain representation. We compare models based on (a) a single most pain-predictive module, either previously identified elementary regions or a single best large-scale cortical resting-state network module; (b) selected cortical-subcortical systems related to evoked pain in prior literature ( multi-system models); and (c) a model spanning the full brain. We estimate the accuracy of pain intensity predictions using cross validation (7 studies) and subsequently validate in three independent holdout studies. All spatial scales convey information about pain intensity, but distributed, multi-system models better characterize pain representations than any individual region or network (e.g. multisystem models explain >20% more of individual subject pain ratings than the best elementary region). Full brain models showed no predictive advantage over multi-system models. These findings quantify the extent that representation of evoked pain experience is distributed across multiple cortical and subcortical systems, show that pain representation is not circumscribed by any elementary region or conical network, and provide a blueprint for identifying the spatial scale of information in other domains. Significance StatementWe define modular, multisystem and global views of brain function, use multivariate fMRI decoding to characterize pain representations at each level, and provide evidence for a multisystem representation of evoked pain. We further show that local views necessarily exclude important components of pain representation, while a global full brain representation is superfluous, even though both are viable frameworks for representing pain. These findings quantitatively juxtapose and reconcile divergent conclusions from evoked pain studies within a generalized neuroscientific framework, and provide a blueprint for investigating representational architecture for diverse brain processes.

neuroscience↗

bioRxiv2020

Uncertainty-driven regulation of learning and exploration in adolescents: A computational account

Healthy adults flexibly adapt their learning strategies to ongoing changes in uncertainty, a key feature of adaptive behaviour. However, the developmental trajectory of this ability is yet unknown, as developmental studies have not incorporated trial-to-trial variation in uncertainty in their analyses or models. To address this issue, we compared adolescents and adults trial-to-trial dynamics of uncertainty, learning rate, and exploration in two tasks that assess learning in noisy but otherwise stable environments. In an estimation task--which provides direct indices of trial-specific learning rate--both age groups reduced their learning rate over time, as self-reported uncertainty decreased. Accordingly, the estimation data in both groups was better explained by a Bayesian model with dynamic learning rate (Kalman filter) than by conventional reinforcement-learning models. Furthermore, adolescents learning rates asymptoted at a higher level, reflecting an over-weighting of the most recent outcome, and the estimated Kalman-filter parameters suggested that this was due to an overestimation of environmental volatility. In a choice task, both age groups became more likely to choose the higher-valued option over time, but this increase in choice accuracy was smaller in the adolescents. In contrast to the estimation task, we found no evidence for a Bayesian expectation-updating process in the choice task, suggesting that estimation and choice tasks engage different learning processes. However, our modeling results of the choice task suggested that both age groups reduced their degree of exploration over time, and that the adolescents explored overall more than the adults. Finally, age-related differences in exploration parameters from fits to the choice data were mediated by participants volatility parameter from fits to the estimation data. Together, these results suggest that adolescents overestimate the rate of environmental change, resulting in elevated learning rates and increased exploration, which may help understand developmental changes in learning and decision-making. Author SummaryTo successfully learn the value of stimuli and actions, people should take into account their current (un)certainty about these values: Learning rates and exploration should be high when ones value estimates are highly uncertain (in the beginning of learning), and decrease over time as evidence accumulates and uncertainty decreases. Recent studies have shown that healthy adults flexibly adapt their learning strategies based on ongoing changes in uncertainty, consistent with normative learning. However, the development of this ability prior to adulthood is yet unknown, as developmental learning studies have not considered trial-to-trial changes in uncertainty. Here, we show that adolescents, as compared to adults, showed a smaller decrease in both learning rate and exploration over time. Computational modeling revealed that both of these effects were due to adolescents overestimating the amount of environmental volatility, which made them more sensitive to recent relative to older evidence. The overestimation of volatility during adolescence may represent the rapidly changing environmental demands during this developmental period, and can help understand the surge in real-life risk taking and exploratory behaviours characteristic of adolescents.

neuroscience↗