Multimodal 3D atlas of the macaque monkey motor and premotor cortex

Abstract

In the present study we reevaluated the parcellation scheme of the macaque frontal agranular cortex by implementing quantitative cytoarchitectonic and multireceptor analyses, with the purpose to integrate and reconcile the discrepancies between previously published maps of this region.We applied an observer-independent and statistically testable approach to determine the position of cytoarchitectonic borders. Analysis of the regional and laminar distribution patterns of 13 different transmitter receptors confirmed the position of cytoarchitectonically identified borders. Receptor densities were extracted from each area and visualized as its “receptor fingerprint”. Hierarchical and principal components analyses were conducted to detect clusters of areas according to the degree of (dis)similarity of their fingerprints. Finally, functional connectivity pattern of each identified area was analyzed with areas of prefrontal, cingulate, somatosensory and lateral parietal cortex and the results were depicted as “connectivity fingerprints” and seed-to-vertex connectivity maps.We identified 16 cyto- and receptor architectonically distinct areas, including novel subdivisions of the primary motor area 4 (i.e. 4a, 4p, 4m) and of premotor areas F4 (i.e. F4s, F4d, F4v), F5 (i.e. F5s, F5d, F5v) and F7 (i.e. F7d, F7i, F7s). Multivariate analyses of receptor fingerprints revealed three clusters, which first segregated the subdivisions of area 4 with F4d and F4s from the remaining premotor areas, then separated ventrolateral from dorsolateral and medial premotor areas. The functional connectivity analysis revealed that medial and dorsolateral premotor and motor areas show stronger functional connectivity with areas involved in visual processing, whereas 4p and ventrolateral premotor areas presented a stronger functional connectivity with areas involved in somatomotor responses.For the first time, we provide a 3D atlas integrating cyto- and multi-receptor architectonic features of the macaque motor and premotor cortex. This atlas constitutes a valuable resource for the analysis of functional experiments carried out with non-human primates, for modeling approaches with realistic synaptic dynamics, as well as to provide insights into how brain functions have developed by changes in the underlying microstructure and encoding strategies during evolution.HighlightsMultimodal analysis of macaque motor and premotor cortex reveals novel parcellation3D atlas with cyto- and multireceptor architectonic features of 16 (pre)motor areasPrimary motor area 4 is cyto- and receptor architectonically heterogeneous(Pre)motor areas differ in their functional connectivity fingerprints

A dopamine gradient controls access to distributed working memory in the large-scale monkey cortex

“…All anatomical data was mapped to the appropriate parcellations on the Yerkes19 surface. For the present study, we mapped all data to the 40 area Lyon subgraph (Markov et al, 2014b), as the areas in this parcellation were generally larger than those in the Julich Macaque Brain Atlas (Impieri et al, 2019;Niu et al, 2020;Rapan et al, 2021; this paper) and the Queensland (spine count) injection sites (Elston, 2007), and closer to standard areal descriptions than the Vanderbilt (neuronal density) (Collins et al, 2010) sections. The receptor densities were quantified in 109 cortical regions defined by cyto-and receptor-architecture.…”

“…We first analyzed D1 and D2 receptor distribution patterns throughout the macaque brain using in vitro receptor autoradiography (Figure S1). Autoradiography enables quantification of endogenous receptors in the cell membrane through use of radioactive ligands (Niu et al, 2020;Palomero-Gallagher and Zilles, 2018;Rapan et al, 2021). The highest densities (in fmol/ mg protein) of both receptor types were found in the basal ganglia, with the caudate nucleus (D1, 298 ± 28; D2, 188 ± 30) and putamen (D1, 273 ± 40; D2, 203 ± 37) presenting considerably higher values than the internal (D1, 97 ± 34; D2, 22 ± 12) or external (D1, 55 ± 16; D2, 30 ± 11) subdivisions of the globus pallidus.…”

Gradients of receptor expression in the macaque cortex

“…One-hundred-and-nine cortical areas were defined based on their receptor-and cyto-architecture, as described in (Impieri et al, 2019;Niu et al, 2021Niu et al, , 2020Rapan et al, 2020) and upcoming publications on the prefrontal cortex, cingulate and occipital lobe. We call this parcellation the Julich Macaque Brain Atlas.…”

“…Parallel recent advances in in-vivo neuroimaging (Milham et al, 2020(Milham et al, , 2018 and mesoscale connectome mapping (Markov et al, 2014a(Markov et al, , 2014b(Markov et al, , 2013 have increased the translational potential of studies on the macaque brain. Integration of gold-standard neuroanatomy with in-vivo measures of cortical structure and function has great promise to help translation across species and scales of neuroscience, but is still in its infancy (Donahue et al, 2016;, 2020Hayashi et al, 2020;Rapan et al, 2020;Scholtens et al, 2014;Wang et al, 2020). The mapping of precise receptor and anatomical data to a cortical space that is accessible to neuroimaging researchers could dramatically accelerate our understanding across scales of how the brain works, from the synapse to distributed cognitive networks.…”

Functional Architecture of Executive Control and Associated Event-Related Potentials

“…The canonical cortical microcircuit derived from granular sensory areas 18 does not explain agranular frontal areas like SEF 19,20,21,22,23 . Recently we described the laminar microcircuitry of performance monitoring signals in the SEF, and relationship to the ERP indexing error monitoring known as the error-related negativity (ERN) 16 .…”