Dissociable Forms of Uncertainty-Driven Representational Change Across the Human Brain

• Published in: The Journal of neuroscience 2019-02, Vol.39 (9), p.1688-1698
• Main Authors: Nassar, Matthew R, McGuire, Joseph T, Ritz, Harrison, Kable, Joseph W
• Format: Article
• Language: English
• Subjects: Activity patterns; Adult; BASIC (programming language); Brain; Brain mapping; Cortex (cingulate); Cortex (motor); Environmental changes; Female; Firing pattern; Functional magnetic resonance imaging; Humans; Learning; Magnetic Resonance Imaging; Male; Models, Neurological; Neural networks; Perception; Prefrontal cortex; Representations; Sensorimotor Cortex - physiology; Substrates; Uncertainty; Variation; Visual cortex
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.1713-18.2018

Environmental change can lead decision makers to shift rapidly among different behavioral regimes. These behavioral shifts can be accompanied by rapid changes in the firing pattern of neural networks. However, it is unknown what the populations of neurons that participate in such "network reset" phenomena are representing. Here, we investigated the following: (1) whether and where rapid changes in multivariate activity patterns are observable with fMRI during periods of rapid behavioral change and (2) what types of representations give rise to these phenomena. We did so by examining fluctuations in multivoxel patterns of BOLD activity from male and female human subjects making sequential inferences about the state of a partially observable and discontinuously changing variable. We found that, within the context of this sequential inference task, the multivariate patterns of activity in a number of cortical regions contain representations that change more rapidly during periods of uncertainty following a change in behavioral context. In motor cortex, this phenomenon was indicative of discontinuous change in behavioral outputs, whereas in visual regions, the same basic phenomenon was evoked by tracking of salient environmental changes. In most other cortical regions, including dorsolateral prefrontal and anterior cingulate cortex, the phenomenon was most consistent with directly encoding the degree of uncertainty. However, in a few other regions, including orbitofrontal cortex, the phenomenon was best explained by representations of a shifting context that evolve more rapidly during periods of rapid learning. These representations may provide a dynamic substrate for learning that facilitates rapid disengagement from learned responses during periods of change. Brain activity patterns tend to change more rapidly during periods of uncertainty and behavioral adjustment, yet the computational role of such rapid transitions is poorly understood. Here, we identify brain regions with fMRI BOLD activity patterns that change more rapidly during periods of behavioral adjustment and use computational modeling to attribute the phenomenon to specific causes. We demonstrate that the phenomenon emerges in different brain regions for different computational reasons, the most common being the representation of uncertainty itself, but that, in a selective subset of regions including orbitofrontal cortex, the phenomenon was best explained as a shifting latent state signal that