Organization of parietoprefrontal and temporoprefrontal networks in the macaque.

Abstract

The connectivity among architectonically defined areas of the frontal, parietal, and temporal cortex of the macaque has been extensively mapped through tract-tracing methods. To investigate the statistical organization underlying this connectivity, and identify its underlying architecture, we performed a hierarchical cluster analysis on 69 cortical areas based on their anatomically defined inputs. We identified 10 frontal, four parietal, and five temporal hierarchically related sets of areas (clusters), defined by unique sets of inputs and typically composed of anatomically contiguous areas. Across the cortex, clusters that share functional properties were linked by dominant information processing circuits in a topographically organized manner that reflects the organization of the main fiber bundles in the cortex. This led to a dorsal-ventral subdivision of the frontal cortex, where dorsal and ventral clusters showed privileged connectivity with parietal and temporal areas, respectively. Ventrally, temporofrontal circuits encode information to discriminate objects in the environment, their value, emotional properties, and functions such as memory and spatial navigation. Dorsal parietofrontal circuits encode information for selecting, generating, and monitoring appropriate actions based on visual-spatial and somatosensory information. This organization may reflect evolutionary antecedents, in which the vertebrate pallium, which is the ancestral cortex, was defined by a ventral and lateral olfactory region and a medial hippocampal region.NEW & NOTEWORTHY The study of cortical connectivity is crucial for understanding brain function and disease. We show that temporofrontal and parietofrontal networks in the macaque can be described in terms of circuits among clusters of areas that share similar inputs and functional properties. The resulting overall architecture described a dual subdivision of the frontal cortex, consistent with the main cortical fiber bundles and an evolutionary trend that underlies the organization of the cortex in the macaque.