Reversible Fronto-occipitotemporal Signaling Complements Task Encoding and Switching under Ambiguous Cues

Adaptation to changing environments involves the appropriate extraction of environmental information to achieve a behavioral goal. It remains unclear how behavioral flexibility is guided under situations where the relevant behavior is ambiguous. Using functional brain mapping of machine learning decoders and directional functional connectivity, we show that brain-wide reversible neural signaling underpins task encoding and behavioral flexibility in ambiguously changing environments. When relevant behavior is cued ambiguously during behavioral shifting, neural coding is attenuated in distributed cortical regions, but top-down signals from the prefrontal cortex complement the coding. When behavioral shifting is cued more explicitly, modality-specialized occipitotemporal regions implement distinct neural coding about relevant behavior, and bottom-up signals from the occipitotemporal region to the prefrontal cortex supplement the behavioral shift. These results suggest that our adaptation to an ever-changing world is orchestrated by the alternation of top-down and bottom-up signaling in the fronto-occipitotemporal circuit depending on the availability of environmental information.

Two Measures of Dependence

Two families of dependence measures between random variables are introduced. They are based on the Rényi divergence of order α and the relative α -entropy, respectively, and both dependence measures reduce to Shannon’s mutual information when their order α is one. The first measure shares many properties with the mutual information, including the data-processing inequality, and can be related to the optimal error exponents in composite hypothesis testing. The second measure does not satisfy the data-processing inequality, but appears naturally in the context of distributed task encoding.

Representational organization of novel task sets during proactive encoding

Recent multivariate analyses of brain data have boosted our understanding of the organizational principles that shape neural coding. However, most of this progress has focused on perceptual visual regions (Connolly et al., 2012), whereas far less is known about the organization of more abstract, action-oriented representations. In this study, we focused on humans’ remarkable ability to turn novel instructions into actions. While previous research shows that instruction encoding is tightly linked to proactive activations in fronto-parietal brain regions, little is known about the structure that orchestrates such anticipatory representation. We collected fMRI data while participants (both males and females) followed novel complex verbal rules that varied across control-related variables (integrating within/across stimuli dimensions, response complexity, target category) and reward expectations. Using Representational Similarity Analysis (Kriegeskorte et al., 2008) we explored where in the brain these variables explained the organization of novel task encoding, and whether motivation modulated these representational spaces. Instruction representations in the lateral prefrontal cortex were structured by the three control-related variables, while intraparietal sulcus encoded response complexity and the fusiform gyrus and precuneus organized its activity according to the relevant stimulus category. Reward exerted a general effect, increasing the representational similarity among different instructions, which was robustly correlated with behavioral improvements. Overall, our results highlight the flexibility of proactive task encoding, governed by distinct representational organizations in specific brain regions. They also stress the variability of motivation-control interactions, which appear to be highly dependent on task attributes such as complexity or novelty.Significance StatementIn comparison with other primates, humans display a remarkable success in novel task contexts thanks to our ability to transform instructions into effective actions. This skill is associated with proactive task-set reconfigurations in fronto-parietal cortices. It remains yet unknown, however, how the brain encodes in anticipation the flexible, rich repertoire of novel tasks that we can achieve. Here we explored cognitive control and motivation-related variables that might orchestrate the representational space for novel instructions. Our results showed that different dimensions become relevant for task prospective encoding depending on the brain region, and that the lateral prefrontal cortex simultaneously organized task representations following different control-related variables. Motivation exerted a general modulation upon this process, diminishing rather than increasing distances among instruction representations.

Encoding Variability: When Pattern Reactivation Does Not Benefit Context Memory

A growing body of evidence suggests that neural pattern reactivation supports successful memory formation across multiple study episodes. Previous studies investigating the beneficial effects of repeated encoding typically presented the same stimuli repeatedly under the same encoding task instructions. In contrast, repeating stimuli in different contexts is associated with superior item memory, but poorer memory for contextual features varying across repetitions. In the present functional magnetic-resonance imaging (fMRI) study, we predicted dissociable mechanisms to underlie the successful formation of context memory when the context in which stimuli are repeated is either held constant or varies at each stimulus presentation. Twenty participants studied names of famous people four times, either in the same task repeatedly, or in four different encoding tasks. This was followed by a surprise recognition memory test, including a source judgement about the encoding task. Behaviourally, different task encoding compared to same task encoding was associated with fewer correct context memory judgements but also better item memory, as reflected in fewer misses. Searchlight representational similarity analysis revealed fMRI pattern reactivation in the posterior cingulate cortex to be higher for correct compared to incorrect source memory judgements in the same task condition, with the opposite pattern being observed in the different task condition. It was concluded that higher levels of pattern reactivation in the posterior cingulate cortex index generalisation across context information, which in turn may improve item memory performance during encoding variability but at the cost of contextual features.

Frontal Cortex Supports the Early Structuring of Multiple Solution Steps in Symbolic Problem-solving

problem-solving relies on a sequence of cognitive steps involving phases of task encoding, the structuring of solution steps, and their execution. On the neural level, metabolic neuroimaging studies have associated a frontal-parietal network with various aspects of executive control during numerical and nonnumerical problem-solving. We used EEG–MEG to assess whether frontal cortex contributes specifically to the early structuring of multiple solution steps. Basic multiplication (“3 × 4” vs. “3 × 24”) was compared with an arithmetic sequence rule (“first add the two digits, then multiply the sum with the smaller digit”) on two complexity levels. This allowed dissociating demands of early solution step structuring from early task encoding demands. Structuring demands were high for conditions that required multiple steps, that is, complex multiplication and the two arithmetic sequence conditions, but low for easy multiplication that mostly relied on direct memory retrieval. Increased right frontal activation in time windows between 300 and 450 msec was observed only for conditions that required multiple solution steps. General task encoding demands, operationalized by problem size (one-digit vs. two-digit numbers), did not predict these early frontal effects. In contrast, parietal effects occurred as a function of problem size irrespectively of structuring demands in early phases of task encoding between 100 and 300 msec. We here propose that frontal cortex subserves domain-general processes of problem-solving, such as the structuring of multiple solution steps, whereas parietal cortex supports number-specific early encoding processes that vary as a function of problem size.