Projection Motifs and Wiring Logic of Medial Pulvinar Thalamocortical Axons in the Marmoset Monkey

The medial pulvinar thalamic nucleus (MPu) is an evolutionary novelty of the primate thalamus, prominently expanded in humans. Piecemeal data from studies in various monkey species indicate that MPu axons reach prefrontal, inferior parietal, cingulate, insular, or temporal areas; however, the precise wiring and functional logic of such brain-wide connections remain obscure. In marmoset monkeys (<i>Callithrix jacchus</i>) of both sexes, we visualized the axons originated from specific pulvinar domains by means of biotinylated dextran amine microinjections and compared them across multiple cases. In addition, by injecting retrograde tracers in the cortical areas targeted by the pulvinar axons, we investigated the organization of projection cells within MPu and the existence of long-range branched axons. Specific projection motifs reveal a caudal MPu subnucleus that innervates inferior and ventral temporal areas and a rostral MPu subnucleus that innervates temporal, ventral prefrontal, premotor, inferior posterior parietal, and cingulate areas. We demonstrate numerous MPu neurons that innervate through branched axons prefrontal and parietal or prefrontal and temporal areas; other cells with different projection patterns are closely intermingled with them. Our findings support the notion that MPu is a hub of the brain-wide networks that support complex visual and social cognition, sensory-guided reaching, working memory, and attention. Moreover, the finding of long-range branching MPu axons and dense terminal arborizations suggest that MPu cells may regulate functional connectivity among high-level cortical areas at different spatial scales. Besides, the anatomical "ground truth" provided by our study is relevant for functional imaging and distributed network modeling studies.