Independent and interacting value systems for reward and information in the human brain
Abstract
Theories of Prefrontal Cortex (PFC) as optimizing reward value have been widely deployed to explain its activity in a diverse range of contexts, with substantial empirical support in neuroeconomics and decision neuroscience. Similar neural circuits, however, have also been associated with information processing. By using computational modeling, model-based fMRI analysis, and a novel experimental paradigm, we aim at establishing whether a dedicated and independent value system for information exists in the human PFC. We identify two regions in the human PFC which independently encode reward and information. Our results provide empirical evidence for PFC as an optimizer of independent information and reward signals during decision-making under realistic scenarios, with potential implications for the interpretation of PFC activity in both healthy and clinical populations.
Data availability
Behavioral data is available on OSF, https://osf.io/e3rp6/.
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Indipendent and interacting value system for reward and information in the human brainOSF, DOI 10.17605/OSF.IO/E3RP6.
Article and author information
Author details
Funding
FWO-Flanders Odysseus 2 (G.OC44.13N)
- William H Alexander
F.R.S.-fNRS
- Irene Cogliati Dezza
FWO
- Irene Cogliati Dezza
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: The experiment was approved by the Ethical Committee of the Ghent University Hospital and conducted according to the Declaration of Helsinki. Informed consent was obtained from all participants prior to the experiment.
Copyright
© 2022, Cogliati Dezza et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
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- Neuroscience
Human-specific cognitive abilities depend on information processing in the cerebral cortex, where the neurons are significantly larger and their processes longer and sparser compared to rodents. We found that, in synaptically connected layer 2/3 pyramidal cells (L2/3 PCs), the delay in signal propagation from soma to soma is similar in humans and rodents. To compensate for the longer processes of neurons, membrane potential changes in human axons and/or dendrites must propagate faster. Axonal and dendritic recordings show that the propagation speed of action potentials (APs) is similar in human and rat axons, but the forward propagation of excitatory postsynaptic potentials (EPSPs) and the backward propagation of APs are 26 and 47% faster in human dendrites, respectively. Experimentally-based detailed biophysical models have shown that the key factor responsible for the accelerated EPSP propagation in human cortical dendrites is the large conductance load imposed at the soma by the large basal dendritic tree. Additionally, larger dendritic diameters and differences in cable and ion channel properties in humans contribute to enhanced signal propagation. Our integrative experimental and modeling study provides new insights into the scaling rules that help maintain information processing speed albeit the large and sparse neurons in the human cortex.