Celine Amiez: Sulcal organization in medial frontal cortex and insights into primate brain evolution
Channel: Brain Web
Date: 2021-07-14

Sulcal organization in the medial frontal cortex provides insights into primate brain evolution

Although the relative expansion of the frontal cortex in primate evolution is generally accepted, the nature of its scaling and inter-species anatomo-functional comparisons of the frontal areas remain controversial. For this symposium, I will present novel results showing how the Medial Frontal Cortical (MFC) sulcal organization has evolved through the primate order. This region has been neglected by evolutionary studies, despite its key role in cognitive functions often thought to be uniquely human, such as mentalizing or counterfactual thinking.

Our between-species comparison of sulcal morphology using magnetic resonance imaging (MRI) provides evidence for a novel interpretation of the evolution of the MFC from Old-world monkeys (80 macaques and 88 baboons) to Hominoidea (225 chimpanzees and 197 humans). To start, we found that chimpanzees do possess a paracingulate sulcus (PCGS), a feature previously thought to be unique to the human brain(1,2). Both the cytoarchitectonic and the functional organization of the PCGS at the level of the mid-cingulate cortex (MCC) are similar in chimpanzee and in human(3). However, we did observe species differences regarding the probability of occurrence of this sulcus and its lateralization across the two hemispheres. Additionally, these two species differed with regard to the organization of the MFC rostral to the genu of the corpus callosum. There is no evidence from cytoarchitectonic(4) and neuroimaging(5) studies that these changes are associated with new cortical areas, suggesting instead a differential expansion of the rostral MFC and the medial frontopolar cortex, two brain regions that have been considered important for high-order socio-cognitive processing, and the ventral-medial frontal cortex, which is implicated in value-based decisions.

In Old-world monkeys, the organization of the MFC posterior to the genu of the corpus callosum (i.e. the MCC) has all the basic features of the human sulcal organization and reaches a similar organization across Hominoidea. Specifically, Old-world monkeys display precursors of the four vertical sulci of this region. Importantly, these sulci appear to be located at specific anatomical landmarks that are common to all primates. These results, in combination with functional imaging data that I will present, provide evidence that the MCC is comparable, anatomically and functionally, from macaque to human(6).

The above results demonstrate an evolutionarily conserved organizational principle from Old-world monkeys to Hominoidea species, providing a new framework to compare sulcal morphology, cytoarchitectonic areal distribution, connectivity, and function across the primate order. The data presented here can be used to generate clear predictions about how other primate brains might be anatomo-functionally organized(7).

1. Cole, M. et al. (2009). Cingulate cortex: Diverging data from humans and monkeys. Trends in Neurosciences, 32, 566-574.
2. Vogt, B. A. (2016). Midcingulate cortex: Structure, connections, homologies, functions and diseases. Journal of Chemical Neuroanatomy, 74, 28-46.
3. Amiez C. et al. (in press). Chimpanzee histology and functional brain imaging show that the paracingulate sulcus is not human specific. Communication Biology.
4. Petrides, M. et al. (2012). The prefrontal cortex: Comparative architectonic organization in the human and the macaque monkey brains. Cortex, 48, 46-57.
5. Sallet, J. et al. (2013). The organization of dorsal frontal cortex in humans and macaques. Journal of Neuroscience, 33, 12255-12274.
6. Procyk, E. et al. (2016). Midcingulate motor map and feedback detection: Converging data from humans and monkeys. Cerebral Cortex, 26, 467-476.
7. Amiez, C. et al. (2019). Sulcal organization in the medial frontal cortex provides insights into primate brain evolution. Nature Communications, 10, 3437. https://doi.org/10.1038/s41467-019-11347-x.