Electrical Stimulation Mapping of the Brain: Basic Principles and Emerging Alternatives

Abstract

The application of electrical stimulation mapping (ESM) of the brain for clinical use is approximating a century. Despite this long-standing history, the value of ESM for guiding surgical resections and sparing eloquent cortex is documented largely by small retrospective studies, and ESM protocols are largely inherited and lack standardization. Although models are imperfect and mechanisms are complex, the probabilistic causality of ESM has guaranteed its perpetuation into the 21st century. At present, electrical stimulation of cortical tissue is being revisited for network connectivity. In addition, noninvasive and passive mapping techniques are rapidly evolving to complement and potentially replace ESM in specific clinical situations. Lesional and epilepsy neurosurgery cases now offer different opportunities for multimodal functional assessments.

Fig. 1

Subdural ESM across three centuries. A, Sir David Ferrier (1843–1928). His book, The Functions of the Brain, published in 1876, is seminal in the history of neuroscience. The extensive electrical stimulation mapping across multiple species contained therein was the principal inspiration for human ESM, including the first isolated attempts at human functional stimulation to shortly follow across three continents. B and C, Sagittal and axial drawings of ESM in monkey brain from Ferrier’s book. D, Ezio Sciamanna (1850–1905). Sciamanna was one the founders of what is now the School of Medicine at Sapienza University in Rome. Sciamanna (Italy 1882), along with Bartholow (United States 1874) and Alberti (Argentina 1883), followed Ferrier’s work with the first isolated cases of human ESM. E, Lateral view of exposed cortex of Sciamanna’s patient, Ferdinando Rinalducci. Electrical stimulation sites are numbered. Motor responses comprising contraction of facial, forearm, finger, and neck muscles were obtained after stimulation of gray matter (“galvanizzazione sulla dura madre”) at points B, C, E, and G of his original illustration. F, Lateral X-ray of a novel high-density, 250-channel subdural ECoG grid (Albany Medical Center, Albany, NY, 2016).

FIG. 2

Stimulation intensity (mA) plotted against charge density (μC/cm²) of commonly used SEEG, grid/strip, and intraoperative probe electrodes (top). Charge density is segregated into “safe,” “risky,” and “dangerous” categories based on criteria used by the FDA for the approval of the predicate stimulator device (bottom).^, These safety criteria do not take into account other important factors in safety, including interelectrode distance, and presence (ECoG) or absence (SEEG) of current shunting through cerebrospinal fluid, for example.

FIG. 3

Geometry (to scale) of exposed “effective” surfaces available for stimulation of commonly used surface (grid/strip), depth (SEEG), and probe (intraoperative handheld) electrodes. Note relatively equivalent effective surfaces of grid and depth electrodes as compared to significant difference in their respective interelectrode distances. Commonly used stimulation paradigms for each are exemplified, although no current consensus exists.

FIG. 4

Persistent postoperative language deficits reported in an international survey of 56 international epilepsy centers. Percentages listed at right are reported attributions to decline by respondents, including insufficient (22%) and incomplete (17%) testing of resected site. (Reprinted from Hamberger et al.)

FIG. 5

Illustration of common stimulation parameters across 1/3 second for grid (A), depth (B), and alternative high-frequency monopolar stimulation (“train of five” method, C).

FIG. 6

CCEP resulting from intraoperative stimulation under general anesthesia. A, Stimulation of inferior frontal gyrus yields CCEP responses over middle and posterior parts of superior, middle, and inferior temporal gyri. Maximal CCEP amplitude is observed over the location marked with star. B, Corresponding CCEP waveform. (Adapted with permission from Yamao et al.)

FIG. 7

Example ECoG-based mapping results of receptive language function. Red circles give those locations whose ECoG broadband activity changes when the patient listens to the Boston Aphasia Battery (unpublished results).

FIG. 8

Principle of TMS. Current in the coil generates a magnetic field B that induces an electric field E. The drawing on the right illustrates a lateral view of the precentral gyrus in the right hemisphere. Two pyramidal axons are shown with a typical orientation of the magnetic field. The electric field is parallel to the scalp and may induce action potentials in the axons. (Adapted with permission from Ruohonen and Ilmoniemi.)