Time Course of Orientation Ensemble Representation in the Human Brain.

Abstract

Natural scenes are filled with groups of similar items. Humans employ ensemble coding to extract the summary statistical information of the environment, thereby enhancing the efficiency of information processing, something particularly useful when observing natural scenes. However, the neural mechanisms underlying the representation of ensemble information in the brain remain elusive. In particular, whether ensemble representation results from the mere summation of individual item representations or it engages other specific processes remains unclear. In this study, we utilized a set of orientation ensembles wherein none of the individual item orientations were the same as the ensemble orientation. We recorded magnetoencephalography (MEG) signals from human participants (both sexes) when they performed an ensemble orientation discrimination task. Time-resolved multivariate pattern analysis (MVPA) and the inverted encoding model (IEM) were employed to unravel the neural mechanisms of the ensemble orientation representation and track its time course. First, we achieved successful decoding of the ensemble orientation, with a high correlation between the decoding and behavioral accuracies. Second, the IEM analysis demonstrated that the representation of the ensemble orientation differed from the sum of the representations of individual item orientations, suggesting that ensemble coding could further modulate orientation representation in the brain. Moreover, using source reconstruction, we showed that the representation of ensemble orientation manifested in early visual areas. Taken together, our findings reveal the emergence of the ensemble representation in the human visual cortex and advance the understanding of how the brain captures and represents ensemble information.Significance Statement Ensemble coding, a cognitive process of extracting summary statistical information from groups of similar items, stands as a pivotal strategy enabling humans to efficiently process complex natural scenes with limited sensory capacities. However, the neural mechanisms of ensemble coding remain largely unknown. Recent modeling studies have predominantly highlighted the importance of the summed activation across all items in ensemble coding. Intriguingly, here, we show that ensemble orientation representation differed from the summed representation of all component item orientations, suggesting that ensemble coding incorporates additional processes beyond mere summation. Additionally, we explore how the ensemble orientation representation per se evolved in the human visual cortex. Our findings significantly extend our understanding of ensemble coding.