In vertebrates, advanced cognitive abilities are associated with a highly developed telencephalic pallium. In mammals, the six-layered neocortex of the pallium is composed of excitatory neurons and inhibitory interneurons, organized across layers into microcircuits. These organizational principles are proposed to support efficient, high-level information processing. Comparative perspectives across vertebrates provide a lens to understand what common features of pallium are important for complex cognition. For non-mammalian vertebrates that exhibit complex cognitive abilities, such as birds, the physiology of identified pallial cell types and their circuit organization are largely unresolved. Using viral tools to target excitatory vs. inhibitory neurons in the zebra finch auditory association pallium, we systematically tested predictions derived from mammalian neocortex. We identify two segregated neuronal populations that exhibit profound physiological and computational similarities with mammalian excitatory and inhibitory neocortical cells. Specifically, despite dissimilarities in gross architecture, avian association pallium exhibits neocortex-typical coding principles, and inhibitory-dependent cortical synchrony, gamma oscillations, and local suppression. Our findings suggest parallel evolution of physiological and network roles for pallial cell types in amniotes with substantially divergent pallial organization.