Within-Individual Organization of the Human Cerebral Cortex: Networks, Global Topography, and Function

Abstract

The human cerebral cortex is populated by specialized regions that are organized into networks. Here we estimated networks using a Multi-Session Hierarchical Bayesian Model (MS-HBM) applied to intensively sampled within-individual functional MRI (fMRI) data. The network estimation procedure was initially developed and tested in two participants (each scanned 31 times) and then prospectively applied to 15 new participants (each scanned 8 to 11 times). Detailed analysis of the networks revealed a global organization. Locally organized first-order sensory and motor networks were surrounded by spatially adjacent second-order networks that also linked to distant regions. Third-order networks each possessed regions distributed widely throughout association cortex. Moreover, regions of distinct third-order networks displayed side-by-side juxtapositions with a pattern that repeated similarly across multiple cortical zones. We refer to these as Supra-Areal Association Megaclusters (SAAMs). Within each SAAM, two candidate control regions were typically adjacent to three separate domain-specialized regions. Independent task data were analyzed to explore functional response properties. The somatomotor and visual first-order networks responded to body movements and visual stimulation, respectively. A subset of the second-order networks responded to transients in an oddball detection task, consistent with a role in orienting to salient or novel events. The third-order networks, including distinct regions within each SAAM, showed two levels of functional specialization. Regions linked to the putative control networks responded to working memory load across multiple stimulus domains. The remaining regions within each SAAM did not track working memory load but rather dissociated across language, social, and spatial / episodic processing domains. These results support a model of the cerebral cortex in which progressively higher-order networks nest outwards from primary sensory and motor cortices. Within the apex zones of association cortex there is specialization of large-scale networks that divides domain-flexible from domain-specialized regions repeatedly across parietal, temporal, and prefrontal cortices. We discuss implications of these findings including how repeating organizational motifs may emerge during development.

Specialization of the Human Hippocampal Long Axis Revisited

“…In a major advance using within-individual precision neuroimaging, Zheng et al (2021) found that two distinct cerebral networks possess differential coupling to the anterior and posterior hippocampus. The first network, correlated with the anterior hippocampus, is topographically similar to canonical groupbased estimates of the hippocampal-cortical network mentioned above and has been functionally associated with autobiographical remembering and scene construction (e.g., Svoboda et al 2006;Hassabis and Maguire 2007;Schacter et al 2007;Andrews-Hanna et al 2014;DiNicola et al 2020DiNicola et al , 2023aDiNicola et al , 2023bDu et al 2023). This network has also been identified within individuals using high-field fMRI from seed regions placed in the subiculum (Braga et al 2019) and parahippocampal area TH (Reznik et al 2023).…”

“…Adding nuance to inferring functions of the hippocampal subregions, the network coupled to the posterior hippocampus includes regions resembling another network extensively studied in the literature, generally referred to as the Salience Network (SAL; Seeley et al 2007;Seeley 2019). By our estimation, the SAL and PMN networks may be the same network historically described by two different literatures (referred to as SAL / PMN; see Du et al 2023). The observation that the posterior hippocampus may be coupled to a network which responds to transient events raises the possibility that the posterior hippocampus itself may support the detection of salience or novelty (e.g.…”

“…English-speaking adults (ages 18-34) without neurological or psychiatric illness completed MRI scanning sessions (data from Du et al 2023). After exclusions to ensure data quality, the MRI data set included 11 participants with a mean age of 22.4 yr (SD = 4.1; 11 right-handed; 8 women).…”

“…Scanning was conducted at the Harvard Center for Brain Science using a 3T Siemens MAGNETOM Prisma fit MRI scanner as described in Du et al (2023). For P2, a 64-channel phase-arrayed head-neck coil (Siemens Healthcare, Erlangen, Germany) was used for 2 sessions, and a 32-channel phase-arrayed head coil (Siemens Healthcare, Erlangen, Germany) was used for the remaining 6 sessions.…”

Social cognitive regions of human association cortex are selectively connected to the amygdala

“…This provided another replication of the separation between the networks. 20,70,86,[115][116][117][118] Surface-based analysis allows easy observation of the cortical mantle, making it convenient for identifying the networks based on anatomical characteristics (see detailed descriptions in Braga and Buckner 66 and Braga et al 70 ), but does not well-capture the anatomy of the MTL. Therefore, we re-defined DN-A and DN-B in the volume using manually selected seed voxels from left dorsal prefrontal cortex, and projected the volume-defined maps to the surface for comparison with surface-defined estimates to confirm that both approaches were targeting the same networks (Fig.…”