Aperiodic neural timescales in prefrontal cortex dilate with increased task abstraction

Abstract

Navigating everyday environments requires that the brain perform information processing at multiple different timescales. For example, while watching a movie we use sensory information from every video frame to construct the current movie scene, which itself is continuously integrated into the narrative arc of the film. This critical function is supported by sensory inputs propagating from dynamic sensory cortices to association cortices, where neural activity remains more stable over time. The hierarchical organization of cortex is therefore reflected in a gradient of neural timescales. While this propagation of inputs up the cortical hierarchy is facilitated by both rhythmic (oscillatory) and non-rhythmic (aperiodic) neural activity, traditional measures of oscillations are often confounded by the influence of aperiodic signals. The reverse is also true: traditional measures of aperiodic neural timescales are influenced by oscillations. This makes it difficult to distinguish between oscillatory and timescale effects in cognition. Here, we analyzed electroencephalography (EEG) data from participants performing a cognitive control task that manipulated the amount of task-relevant contextual information, called task abstraction. Critically, we separated aperiodic neural timescales from the confounding influence of oscillatory power. We hypothesized that neural timescales would increase during the task, and more so in high-abstraction conditions. We found that task abstraction dilated the aperiodic neural timescale, as estimated from the autocorrelation function, over prefrontal cortical regions. Our findings suggests that neural timescales are a dynamic feature of the cerebral cortex that change to meet task demands. Significance StatementThough often thought of as indexing anatomical brain structure, neural timescales have recently come under the spotlight for their variability across different task conditions. Here, we investigated whether neural timescales dynamically change during cognitive tasks that require a greater level of contextual control. Previous work quantified neural timescales using the autocorrelation function, but this approach conflates oscillatory and aperiodic contributions to the timescale. Thus, we decomposed the neural timescale into oscillatory and aperiodic components, and found that aperiodic-derived timescale measures dynamically change with contextual control. Oscillatory power also exhibits change in response to task demands, reaffirming previous findings. These results together suggest that both established oscillatory and novel aperiodic measures of neural timescales can dynamically change to meet task demands.