Dual-format attentional template during preparation in human visual cortex

Chen, Yilin; Liu, Taosheng; Jia, Ke; Theeuwes, Jan; Gong, Mengyuan · 2025 · DOAJ

DOI: 10.7554/eLife.103425

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Summary

This study investigates the neural representation of attentional templates during the preparatory phase of visual attention, addressing a debate over whether these templates are sensory-like (veridical) or non-sensory (abstract). While previous research has shown that attentional templates resemble sensory responses during stimulus processing, their format during preparation remains controversial. The authors propose a dual-format mechanism, hypothesizing that the brain maintains a predominantly non-sensory template alongside a latent, sensory-like template during preparation. This latent template is suggested to be stored in an activity-silent state, becoming accessible only when needed for prospective stimulus processing. To test this hypothesis, the researchers employed functional magnetic resonance imaging (fMRI) combined with multivariate pattern analysis (MVPA) and a novel “pinging” technique. Participants performed an orientation cueing task where they prepared to attend to a specific orientation (45° or 135°) during a delay period before discriminating a compound stimulus. The experiment included two conditions: a “No-Ping” session with no visual disturbance during preparation, and a “Ping” session where a high-contrast, task-irrelevant visual impulse was presented during the delay to perturb neural activity. This impulse was designed to retrieve information from latent brain states. The study analyzed neural activity in primary visual cortex (V1), extrastriate visual cortex (EVC), intraparietal sulcus (IPS), and prefrontal cortex (PFC). In the No-Ping condition, MVPA revealed that neural patterns during preparation contained decodable information about the attended orientation but were distinct from patterns evoked by actual perception, indicating a non-sensory format. Cross-task generalization from perception to preparation failed, confirming the lack of a sensory-like template. However, in the Ping condition, the visual impulse caused preparatory activity patterns in V1 and EVC to resemble those associated with perceiving the orientations. This impulse-driven activation significantly increased decoding accuracy and pattern similarity between preparation and perception in visual areas, but not in frontoparietal regions. Furthermore, the emergence of this sensory-like template was associated with enhanced informational connectivity between V1 and frontoparietal areas (IPS and PFC) and correlated with faster reaction times, though not improved accuracy. The findings provide compelling evidence for a dual-format representation of attention during preparation. The brain appears to maintain a default, non-sensory template for initial guidance and a latent, sensory-like template in visual cortex for prospective processing. The “pinging” technique successfully revealed this latent state, demonstrating that it can be activated to enhance network connectivity and facilitate behavioral performance. This work reconciles conflicting accounts of attentional templates by showing that both formats coexist, offering a flexible mechanism for adaptive attentional control. The study highlights the functional relevance of latent neural states in visual cortex and their role in coordinating with frontoparietal networks to optimize stimulus selection.

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• perceptual processing