MEBRAINS 1.0: a new population-based macaque atlas
Puiu F Balan,
Qi Zhu,
Xiaolian Li
et al.
Abstract:Due to their fundamental relevance, the number of anatomical macaque brain templates is constantly growing. Novel templates aim to alleviate limitations of previously published atlases and offer the foundation to integrate multiscale multimodal data. Typical limitations of existing templates include their reliance on one subject, their unimodality (usually only T1 or histological images), or lack of anatomical details. The MEBRAINS template overcomes these limitations by using a combination of T1 and T2 images… Show more
“…To address the first question, of anatomical specificity and whether sequence representations were unique to subregions of area 46 within the DLPFC, we used new regions of interest (ROI) that tiled area 46 and replicated previous analyses during the SEQ task (Yusif Rodriguez, et al, 2023). First, to tile area 46 we used the MEBRAINS Multilevel Macaque Brain Atlas (Rapan et al 2023;Balan et al 2024)that parcellated area 46 according to cytoarchitectonic divisions augmented by functional connectivity and neurochemical data. This atlas divides area 46 into eight distinct regions (four anterior and four posterior) that are then divided into dorsal and ventral shoulder and fundus regions (Figure 2A,B).…”
Section: The Fundus Of Monkey Dlpfc Area 46 Represents Abstract Visua...mentioning
Sequential information permeates our daily lives, such as when listening to music. These sequences are potentially abstract in that they do not depend on the exact identity of the stimuli (pitch of the notes), but on the rule that they follow (interval between them). Previously, we showed that a subregion of monkey lateral prefrontal cortex (LPFC), area 46, responds to abstract visual sequences in a manner that parallels human responses. However, area 46 has several mapped subregions and abstract sequences require of multiple stimulus features (such as stimulus and time), leaving open questions as to the specificity of responses in the LPFC. To determine the anatomical and functional specificity of abstract visual sequence responses within area 46 subregions, we used awake functional magnetic resonance imaging in three male macaque monkeys during two no-report visual tasks. One task presented images in an abstract visual sequence; the other used the same timing properties and image variation, but no sequential information. We found, using subdivisions from a multimodal parcellation of area 46, that responses to abstract visual sequences were unique to the posterior fundus of area 46, which did not respond to changes in timing or image alone. In contrast, posterior shoulder regions of area 46 showed selectivity to more concrete stimulus changes (i.e., timing and image). These results align with organizational hierarchies observed in monkeys and humans, and suggest that interactions between adjacent LPFC subregions is key scaffolding for complex daily behaviors.
“…To address the first question, of anatomical specificity and whether sequence representations were unique to subregions of area 46 within the DLPFC, we used new regions of interest (ROI) that tiled area 46 and replicated previous analyses during the SEQ task (Yusif Rodriguez, et al, 2023). First, to tile area 46 we used the MEBRAINS Multilevel Macaque Brain Atlas (Rapan et al 2023;Balan et al 2024)that parcellated area 46 according to cytoarchitectonic divisions augmented by functional connectivity and neurochemical data. This atlas divides area 46 into eight distinct regions (four anterior and four posterior) that are then divided into dorsal and ventral shoulder and fundus regions (Figure 2A,B).…”
Section: The Fundus Of Monkey Dlpfc Area 46 Represents Abstract Visua...mentioning
Sequential information permeates our daily lives, such as when listening to music. These sequences are potentially abstract in that they do not depend on the exact identity of the stimuli (pitch of the notes), but on the rule that they follow (interval between them). Previously, we showed that a subregion of monkey lateral prefrontal cortex (LPFC), area 46, responds to abstract visual sequences in a manner that parallels human responses. However, area 46 has several mapped subregions and abstract sequences require of multiple stimulus features (such as stimulus and time), leaving open questions as to the specificity of responses in the LPFC. To determine the anatomical and functional specificity of abstract visual sequence responses within area 46 subregions, we used awake functional magnetic resonance imaging in three male macaque monkeys during two no-report visual tasks. One task presented images in an abstract visual sequence; the other used the same timing properties and image variation, but no sequential information. We found, using subdivisions from a multimodal parcellation of area 46, that responses to abstract visual sequences were unique to the posterior fundus of area 46, which did not respond to changes in timing or image alone. In contrast, posterior shoulder regions of area 46 showed selectivity to more concrete stimulus changes (i.e., timing and image). These results align with organizational hierarchies observed in monkeys and humans, and suggest that interactions between adjacent LPFC subregions is key scaffolding for complex daily behaviors.
“…Atlases are essential for investigating the structural and functional characteristics of the brain by providing a map in a common space and allowing comparison of results across studies 52 . A series of comparable brain atlases with a uniform parcellation scheme from different species could facilitate efficient comparative studies and provide vital clues about how the human brain evolved 53,54 . However, mapping non-human primate brains is incomplete and relatively preliminary, with previous atlases having been constructed using different modalities and at different scales.…”
Chimpanzees (Pan troglodytes) are humans’ closest living evolutionary relatives, making them the most directly relevant comparison point for understanding human brain evolution. By zeroing in on the differences in brain connectivity between humans and chimpanzees, it can provide key insights into the specific evolutionary changes that occurred along the human lineage. However, conducting fair comparisons of brain connectivity between humans and chimpanzees remains challenging, as cross-species brain atlases established within the same framework are currently lacking. Without the availability of cross-species brain atlases, the region-wise connectivity patterns between humans and chimpanzees cannot be directly compared. To address this gap, we built the first Chimpanzee Brainnetome Atlas (ChimpBNA) by following the well-established connectivity-based parcellation framework. Leveraging this new resource, we found substantial divergence in connectivity patterns across most association cortices, notably in the lateral temporal and dorsolateral prefrontal cortex between the two species. Intriguingly, these patterns significantly deviate from the expected cortical expansion during brain evolution. Additionally, we identified regions displaying connectional asymmetries between species, likely resulting from evolutionary divergence. Genes associated with these divergent connectivities were found to be enriched in cell types crucial for cortical projection circuits and synapse formation. These genes exhibited more pronounced differences in expression patterns in regions with higher connectivity divergence, suggesting a potential foundation for brain connectivity evolution. Therefore, our study not only provides a fine-scale brain atlas of chimpanzees but also highlights the connectivity divergence between humans and chimpanzees in a more rigorous and comparative manner and suggests potential genetic underpinnings for the observed divergence in brain connectivity patterns between the two species. This can help us better understand the origins and development of uniquely human cognitive capabilities.
“…Two rhesus monkeys (Macaca mulatta; 1 female; 5-9 kg), M1 and M2, were used for the high-resolution fMRI study. They had previously participated in several other studies 9,10,32,33 . Another male rhesus monkey, M3 (6.5 kg), was used for the electrophysiological experiments.…”
Segregated networks of columnar-like functional units convey highly specific functional signals within and across early visual areas. It is unknown, however, whether higher-order category-selective areas exhibit a similar mesoscale functional organization, nor whether mesoscale functional units are aggregated in functional networks spanning large distances (e.g. across hemispheres). Using sub-millimeter fMRI and single-cell recordings, we found that neurons with functionally similar tuning properties within face-and body-selective areas are spatially grouped into columnar-like mesoscale functional units, which also show segregated interhemispheric connectivity patterns. Hence, mesoscale functional networks may constitute fundamental architectural features of primate cortex.
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