Inferotemporal Cortex Collaborates Before It Codes: Non-Serial Inter-Area Synergy in the Macaque Ventral Stream

The ventral visual stream is widely modeled as a serial feedforward hierarchy in which V1, V4, and IT population codes develop sequentially during object recognition. We ask whether a second, concurrent coding mode exists—one organized not by anatomical order but by joint population structure across areas. Using Partial Information Decomposition applied to simultaneous multielectrode spiking recordings across all three areas at millisecond resolution—the first simultaneous three-area spiking PID analysis of the primate ventral stream—in two macaque monkeys viewing 25,000+ natural images, we decompose population coding into serial (unique per area) and synergistic (joint across areas) components at 5 ms resolution across five CNN target representations spanning low-level spatial features to high-level object identity. Three findings replicate across both animals and all five representations. First, synergistic inter-area coupling emerges before IT carries any unique object-related information—a dissociation of 15–65 ms that replicates in direction without exception across both animals—such that the joint population integrates before the apex encodes; moreover, V1–IT synergy persists for over 120 ms after V1’s unique information reaches zero. Second, although V1↔IT and V1↔V4 coupling emerge simultaneously and rise in parallel, V1↔IT exhibits stronger peak synergy at mid-to-high-level targets in both animals, suggesting a dominant role for non-serial joint coding. Third, when V1 and V4 are treated as an integrated feedforward block, their synergistic coupling with IT emerges last across all tested conditions—the feedforward foundation is the final component to join the synergistic mode, not the first. Together, these results show that serial and synergistic population codes co-occur in the same recordings, overlap in time, but follow different organizational principles, Providing a new level of nuance in our understanding of the primate ventral stream and introducing concrete constraints for biologically grounded models of vision.