Jia Yang¹ (), Haoxuan Yao¹, Kesheng Wang¹, Jingqiu Luo¹, Qianhua Zhu¹, Shiming Tang¹, Zhonglin Lu², Pinglei Bao¹; ¹Peking University, ²New York University Shanghai

Category-selective regions in primate inferotemporal (IT) cortex are defined by strong responses to specific categories. Yet with accumulating experience, familiar stimuli typically elicit reduced responses. This apparent paradox raises a key question: how can visual experience, which often suppresses responses, drive the emergence of highly responsive, category-selective regions? Here, we used longitudinal widefield calcium imaging to track the anterior IT (AIT) cortex in two macaques across approximately 20 sessions of passive exposure to Chinese words. Thirty fixed words, each with 10 exemplars varying in size, position, and rotation, were presented consistently as trained words. In each session, 10 novel words with 10 exemplars were introduced as controls. Additionally, we paired each set of 10 trained words with a distinct reward magnitude of one, two, or three drops of juice. Remarkably, training induced the progressive formation and expansion of a word-selective area. This newly formed region exhibited enhanced selectivity for trained words, characterized by stronger responses and improved decoding performance, including coarse decoding of reward level and finer decoding of character identity within each reward condition. At the population level, learning reorganized representational geometry by increasing inter-word separation, accompanied by expanded yet more elongated individual-word manifolds. Pre- and post-tests further revealed generalization to untrained words, yielding stronger responses and higher decoding accuracy. Critically, these benefits were evident at the start of the post-test, suggesting direct transfer driven by signal enhancement rather than an improved ability to learn new words. Together, these findings indicate that during the early stages of category-selective area formation, experience can operate through signal amplification to rapidly boost selectivity and develop a general and structural representational space for a specific category in the primate IT cortex.

Acknowledgements: This work was supported by National Science and Technology Innovation 2030-Major Project 2022ZD0204803, Natural Science Foundation of China NSFC32230043 to P. B., Natural Science Foundation of China Grant 32200857, China Postdoctoral Science Foundation Grant 2023M740125, 2022T150021to J.Y.