Interspecies activation correlations reveal functional correspondences between marmoset and human brain areas

The common marmoset has enormous promise as a nonhuman primate model of human brain functions. While resting-state functional MRI (fMRI) has provided evidence for a similar organization of marmoset and human cortices, the technique cannot be used to map the functional correspondences of brain regions between species. This limitation can be overcome by movie-driven fMRI (md-fMRI), which has become a popular tool for noninvasively mapping the neural patterns generated by rich and naturalistic stimulation. Here, we used md-fMRI in marmosets and humans to identify whole-brain functional correspondences between the two primate species. In particular, we describe functional correlates for the well-known human face, body, and scene patches in marmosets. We find that these networks have a similar organization in both species, suggesting a largely conserved organization of higher-order visual areas between New World marmoset monkeys and humans. However, while face patches in humans and marmosets were activated by marmoset faces, only human face patches responded to the faces of other animals. Together, the results demonstrate that higher-order visual processing might be a conserved feature between humans and New World marmoset monkeys but that small, potentially important functional differences exist.

The common marmoset has become an important nonhuman primate model for bridging the translational gap between rodents and humans. Marmosets have a lissencephalic cortex, like rodents, but as primates, they possess a complex visual system (1) and exhibit a similar visuomotor behavior as macaques and humans (2, 3). This, paired with a high reproductive power, small size, and fast maturation rate, make this nonhuman primate (NHP) species particularly interesting for neuroscience.To identify and compare the functional architecture of the primate brain, functional MRI (fMRI) has often been applied because of its noninvasive measures and whole brain coverage (4, 5). In particular, resting-state fMRI (RS-fMRI) has been used 1) to identify homologous large-scale brain networks between marmosets and humans (6, 7), 2) to define functional boundaries based on intrinsic functional connectivity (8, 9), and 3) to use functional connectivity “fingerprints” of brain areas to establish similarities between marmosets, rodents, and humans (10). Because resting-state patterns are state agnostic and spontaneous, however, this technique cannot be used to map the functional correspondences of interspecies blood oxygen level–dependent (BOLD) fluctuations over time. Task-based fMRI is better suited for mapping stimuli-driven fluctuations across species, and, indeed, a few studies have used task-based fMRI in awake marmosets to identify areas related to specific functions [e.g., visuosaccadic orienting (11), processing of faces and bodies (12, 13), looming and receding visual stimuli (14), and tactile processing (15)]. A major drawback of task-based fMRI is that compliance is often poor in NHPs and that each task can only reveal the limited set of functional activations for which it was designed.These limitations can be overcome by employing movie stimuli, which provide rich and naturalistic stimulations. Human studies have shown that movie-driven fMRI (md-fMRI) responses are highly selective between brain regions, engage many brain regions, and are highly reliable between subjects (16–19). Functional correspondences between species can be directly tested by the interspecies activity correlation (ISAC) method, which uses the md-fMRI time course in a seed region in one species to identify functional correspondences across the cortex of the other species. This technique has been successfully employed to identify functional correspondences (analogies) between human and macaque cortical areas (20), but this powerful mapping technique has yet to be applied to the marmoset brain.Here, we used md-fMRI to compare directly the brain activations between marmosets and humans and to establish functional correspondences between cortical areas across the brain in the two species. We focused our analysis on identifying analogies of the well-known human face-, body-, and scene-selective networks in the marmoset brain. Not only do these networks play pivotal roles in complex primate vision, face- and body-selective areas have also been described by a few task-based fMRI studies in marmosets (12, 13), providing an independent validation for some of these results.