The origin of human speech capabilities remains one of the most hotly debated questions in neuroscience. The prevailing theories—whether they invoke laryngeal position or neurogenetic adaptations—have been progressively set aside, and it has long been held that most of the neural infrastructure dedicated to speech in the frontal cortex, including the classical Broca's area, was already present, in a nascent form, in non-human primates. Yet voluntary control of speech remains, to this day, unique to the human species, without current models being able to account for it.
This work builds on the identification, in the adult human brain, of a singular anatomical feature: the prefrontal operculum (PFO), a region located in immediate proximity and medial to Broca's area. This structure results from the expansion of the prefrontal cortex—particularly areas 9 and 10—which pushes the anatomical boundary between the prefrontal and premotor cortices backward. In Old World monkeys, including the macaque and the baboon, the frontal operculum remains exclusively at the level of the premotor/motor cortex, so that this prefrontal extension is lacking. The aim was twofold: to characterize the anatomo-functional organization of the PFO on the basis of its whole-brain connectivity, and to determine whether it has a counterpart in the macaque.
Analysis of functional connectivity in humans reveals that the PFO subdivides into two distinct regions, anterior (aPFO) and posterior (pPFO). These two subregions interact strongly with each other but display markedly different whole-brain connectivity profiles: the posterior part is preferentially associated with the language network, whereas the anterior part is linked to the cognitive control network. This organization suggests that the PFO plays an important role in the cognitive control of speech. To search for possible homologs in the non-human primate, the researchers employed a connectivity-fingerprint matching approach in eighteen rhesus macaques, examined using resting-state functional magnetic resonance imaging under anesthesia. The results reveal similarities with the posterior part of the PFO, but no homolog of the anterior part could be identified in the macaque brain.
Taken together, these observations point to the emergence of the aPFO as an evolutionary advantage specific to hominids, potentially underpinning modern speech capabilities. By distinguishing a language-anchored region from a region oriented toward cognitive control, and by showing that only the latter has a counterpart in the macaque, this study provides part of the answer to the specifically human nature of speech mastery.