The “frontal syndrome” revisited: Lessons from electrostimulation mapping studies

For a long time, in a localizationist view of brain functioning, a combination of symptoms called “frontal syndrome” has been interpreted as the direct result of damages involving the frontal lobe(s). The goal of this review is to challenge this view, that is, to move to a hodotopical approach to lesion mapping, on the basis of new insights provided by intraoperative electrostimulation mapping investigations in patients who underwent awake surgery for cerebral tumors. These original data reported in the last decade break with the traditional dogma of a modular and fixed organization of the central nervous system, by switching to the concepts of cerebral connectivity and plasticity – i.e., a brain organization based on dynamic interrelationships between parallel distributed networks. According to this revisited model, “frontal symptoms” can be generated by tumor or electrostimulation not only of the frontal lobes, but also of cortical and subcortical (white matter pathways/deep gray nuclei) structures outside the frontal lobes: especially, stimulation of the superior longitudinal fascicle may elicit speech production disorders, syntactic disturbances, involuntary language switching or phonemic paraphasia (arcuate fascicle), stimulation of the inferior fronto-occipital fascicle can generate semantic paraphasia or deficit of cross-modal judgment, stimulation of the subcallosal fasciculus may elicit transcortical motor aphasia, while stimulation of the striatum induces preservations. On the other hand, it is also possible to perform extensive right or left frontal lobectomy in patients who continue to have a normal familial, social and professional life, without “frontal syndrome”. Therefore, this provocative approach may open the door to a renewal in the modeling of brain processing as well as in its clinical applications, especially in the fields of cerebral surgery and functional rehabilitation. These findings illustrate well the need to reinforce links between cognitive neuroscience and clinical neurology/neurosurgery.