Task-specific topographic organization of neural activity in the primate lateral prefrontal cortex

Abstract

Neurons in the primate lateral prefrontal cortex (LPFC) flexibly adapt their activity to support diverse cognitive demands. Whether this flexibility is accompanied by changes in the spatial organization of neural population activity remains unclear. Here, we characterized the functional topography of LPFC neural activity in awake, behaving macaques performing three distinct cognitive tasks. Using chronically implanted multi-electrode arrays and topographic similarity analysis (TSA), we found that LPFC topographies were reproducible within tasks but less consistent across tasks. We then separated neural activity into task-tuned and trial-to-trial residual components to determine the basis of these effects. Task-tuned topographies mirrored the overall pattern: they were less consistent across than within tasks, whereas residual topographies remained comparatively stable across tasks. Moreover, task-tuned and residual topographies showed opposing patterns of consistencies. Within tasks, task-tuned topographies were more consistent than residual topographies; across tasks, the pattern reversed. This dissociation suggests a reproducible spatial organization of task-related activity that reconfigures across tasks. Nevertheless, task-tuned topographies remained significantly correlated across tasks, revealing a shared component of spatial organization. Across all three tasks, topographies exhibited a common spatial scale comparable to that of patterned afferent inputs to LPFC reported in previous anatomical tracing studies. Together, these findings suggest that LPFC functional organization combines a shared spatial scaffold with selective, task-dependent reconfiguration of task-tuned population activity.