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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.

SUBMITTER: Giarrocco F

PROVIDER: S-EPMC8560415 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Primates have specialized domains in inferior temporal (IT) cortex that are responsive to particular image categories. Though IT traditionally has been regarded as lacking retinotopy, several recent studies in monkeys have shown that retinotopic maps extend to face patches along the lower bank of the superior temporal sulcus (STS) and neighboring regions of IT cortex. Here, we used fMRI to map the retinotopic organization of medial ventral temporal cortex in four monkeys (2 male and 2 female). We confirm the presence of visual field maps within and around the lower bank of the STS and extend these prior findings to scene-selective cortex in the ventral-most regions of IT. Within the occipitotemporal sulcus (OTS), we identified two retinotopic areas, OTS1 and OTS2. The polar angle representation of OTS2 was a mirror reversal of the OTS1 representation. These regions contained representations of the contralateral periphery and were selectively active for scene versus face, body, or object images. The extent of this retinotopy parallels that in humans and shows that the organization of the scene network is preserved across primate species. In addition retinotopic maps were identified in dorsal extrastriate, posterior parietal, and frontal cortex as well as the thalamus, including both the lateral geniculate nucleus and pulvinar. Together, it appears that most, if not all, of the macaque visual system contains organized representations of visual space.SIGNIFICANCE STATEMENT Primates have specialized domains in inferior temporal (IT) cortex that are responsive to particular image categories. Though retinotopic maps are considered a fundamental organizing principle of posterior visual cortex, IT traditionally has been regarded as lacking retinotopy. Recent imaging studies have demonstrated the presence of several visual field maps within the lateral IT. Using neuroimaging, we found multiple representations of visual space within ventral IT cortex of macaques that included scene-selective cortex. Scene domains were biased toward the peripheral visual field. These data demonstrate the prevalence of visual field maps throughout the primate visual system, including late stages in the ventral visual hierarchy, and support the idea that domains representing different categories are biased toward different parts of the visual field.

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Organization of parietoprefrontal and temporoprefrontal networks in the macaque.

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