Revealing humans' sensorimotor functions with electrical cortical stimulation

Abstract

Direct electrical stimulation (DES) of the human brain has been used by neurosurgeons for almost a century. Although this procedure serves only clinical purposes, it generates data that have a great scientific interest. Had DES not been employed, our comprehension of the organization of the sensorimotor systems involved in movement execution, language production, the emergence of action intentionality or the subjective feeling of movement awareness would have been greatly undermined. This does not mean, of course, that DES is a gold standard devoid of limitations and that other approaches are not of primary importance, including electrophysiology, modelling, neuroimaging or psychophysics in patients and healthy subjects. Rather, this indicates that the contribution of DES cannot be restricted, in humans, to the ubiquitous concepts of homunculus and somatotopy. DES is a fundamental tool in our attempt to understand the human brain because it represents a unique method for mapping sensorimotor pathways and interfering with the functioning of localized neural populations during the performance of well-defined behavioural tasks.

Keywords: electrical stimulation; homunculus; human; language; sensorimotor maps; somatotopy.

Figure 1.

The nicely ordered homunculus constructed by Penfield is not consistent with the individual data actually collected by this neurosurgeon. (a) (Left part.) Evoked responses identified by Penfield for the different digits; (right part) corresponding homunculus. (b) (Left part.) Evoked responses identified by Penfield were reported on the same graph for the arm (including shoulder, elbow, wrist, hand; red colour) and the digits (blue colour); (right side) corresponding homunculus. (c) (Left part.) Evoked responses identified by Penfield were reported on the same graph for the face (green colour) and the neck (red colour); (right side) corresponding homunculus. (d) (Left part.) Penfield's idea of an inverted homunculus; (right side) corresponding formalization of this idea. Adapted from [6,59], with permission.

Figure 2.

(a) Action zones in the precentral gyrus of the monkey where complex movements are evoked in response to long-train electrical stimulations (adapted from [65], with permission). (b) Sites where complex hand/mouth synergies are evoked by electrical stimulation in the human precentral gyrus. The top panel of the figure displays motor sites (black squares) evoking hand-to-mouth synergies resembling self-feeding, in which DES causes the closing hand to progressively approach the opening mouth. The bottom panel of the figure displays multimodal sites (black squares) that evoke hand/arm actions when stimulated while receiving mouth sensory inputs. Adapted from [69], with permission.

Figure 3.

Language maps indicating, for the (left) dominant hemisphere, the cortical locations where DES induced speech dysfunctions in two large studies involving, respectively, 250 [13] and 165 [20] consecutive patients with gliomas. (a) Brain sites inducing speech arrest per square centimetre of the cortical surface (reconstructed from [13]). (b) Brain sites inducing anomia per square centimetre of the cortical surface (reconstructed from [13]). (c) Brain sites inducing alexia per square centimetre of the cortical surface (reconstructed from [13]). (d) Brain sites inducing speech arrest (red circles) and anomia (blue circles). Each individual circle represents a positive observation. Adapted from [20], with permission.