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Link to original content: https://pubmed.ncbi.nlm.nih.gov/29285773/
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. 2018 Mar 1;596(5):941-956.
doi: 10.1113/JP275243. Epub 2018 Jan 19.

Functional architecture of the somatosensory homunculus detected by electrostimulation

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Functional architecture of the somatosensory homunculus detected by electrostimulation

Franck-Emmanuel Roux et al. J Physiol. .

Abstract

Key points: We performed a prospective electrostimulation study, based on 50 operated intact patients, to acquire accurate MNI coordinates of the functional areas of the somatosensory homunculus. In the contralateral BA1, the hand representation displayed not only medial-to-lateral, little-finger-to-thumb, but also rostral-to-caudal discrete somatotopy, with the tip of each finger located more caudally than the proximal phalanx. The analysis of the MNI body coordinates showed rare inter-individual variations in the medial-to-lateral somatotopic organization in these patients with rather different intensity thresholds needed to elicit sensations in different body parts. We found some similarities but also substantial differences with the previous, seminal works of Penfield and his colleagues. We propose a new drawing of the human somatosensory homunculus according to MNI space.

Abstract: In this prospective electrostimulation study, based on 50 operated patients with no sensory deficit and no brain lesion in the postcentral gyrus, we acquired coordinates in the standard MNI space of the functional areas of the somatosensory homunculus. The 3D brain volume of each patient was normalized to that space to obtain the MNI coordinates of the stimulation site locations. For 647 sites stimulated on Brodmann Area 1 (and 1025 in gyri nearby), 258 positive points for somatosensory response (40%) were found in the postcentral gyrus. In the contralateral BA1, the hand representation displayed not only medial-to-lateral and little-finger-to-thumb somatotopy, but also rostral-to-caudal discrete somatotopy, with the tip of each finger located more caudally than the proximal phalanx. We detected a medial-to-lateral, tip-to-base tongue organization but no rostral-to-caudal functional organization. The analysis of the MNI body coordinates showed rare inter-individual variations in the medial-to-lateral somatotopic organization in these patients with intact somatosensory cortex. Positive stimulations were detected through the 'on/off' outbreak effect and discriminative touch sensations were the sensations reported almost exclusively by all patients during stimulation. Mean hand (2.39 mA) and tongue (2.60 mA) positive intensity thresholds were lower (P < 0.05) than the intensities required to elicit sensations in the other parts of the body. Unlike the previous, seminal works of Penfield and colleagues, we detected no sensations such as sense of movement or desire to move, no somatosensory responses outside the postcentral gyrus, and no bilateral responses for face/tongue stimulations. We propose a rationalization of the standard drawing of the somatosensory homunculus according to MNI space.

Keywords: electrical stimulation; homunculus; somatosensory systems.

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Figures

Figure 1
Figure 1. Example of electrostimulation mapping for somatosensory BA1 cortex
A, 38‐year‐old patient with a right diffuse astrocytoma IDH mutant (WHO 2016) with no sensorimotor deficit. B, 3D brain localization of the positive stimulations. In the postcentral gyrus (BA1), electrostimulation showed a clear finger somatotopy, in small (3 mm wide), sharply delimited cortical areas from the little (MNI coordinates: X = 39.4, Y = ‐31.2, Z = 64.2), ring (42.9, −29.0, 60.4), middle (44.7, −24.8, 59.5), and index (−44.3, −25.8, 59.0) fingers to the thumb (46.0, −25.7, 50.7). We observed that the displacement of the bipolar electrode on the cortex located adjacent to a positive area often induced another interference. C, accuracy of the technique with 3 mm distance between the stimulating electrodes. [Color figure can be viewed at wileyonlinelibrary.com]
Figure 2
Figure 2. The medial‐to‐lateral and rostral‐to‐caudal sequences of the hand somatotopy
A, distribution over the two hemispheres (left and right templates) of the medial‐to‐lateral somatosensory representation of each finger. B and C, representation of the barycentre of each finger (coloured dots) in right and left hemispheres with amplitude bars representing the standard variations of each localization (coloured lines). Average right and left MNI barycentres (X, Y, Z) of the thumb (46.2, −22.5, 56.7), index (44, −22.8, 59.9), middle finger (40.6, −28.2, 62.1), ring (37.7, −29.2, 64.8) and little finger (35.4, −30, 66.3). Overall, the medial‐to‐lateral space (X MNI coordinates) devoted to the fingers in BA1 was around 1.5 cm. D, right and left hemispheric distribution of the MNI coordinates of the somatosensory base of the fingers (yellow); whole finger sensation (grey); and tips of the fingers (light blue). Individual analysis showed the rostral‐to‐caudal somatosensory cortical representation of the ventral part of the skin of the fingers. This rostral‐to caudal somatotopy was detected at least once in all 5 fingers. E, group analysis confirmed this somatotopic representation with average X, Y, Z MNI coordinates for the group of fingertip points located more posteriorly (X = 41.4; Y = −31.1, Z = 61.1) than the whole finger sensations (39.7, −27.3, 62.9) and base of the finger sensations (43.6, −26.1, 60.1). [Color figure can be viewed at wileyonlinelibrary.com]
Figure 3
Figure 3. The somatotopic sequence of the tongue
The contralateral somatotopic representations displayed the following somatotopy: base of the tongue (red dots) close to the Sylvian fissure, and middle (pink dots) and tip of the tongue (yellow dots) more medial. The representation of the tongue occupied a large portion of the postcentral gyrus (2.5 cm for the mouth). This figure is composed of isolated points found punctually in some patients and of multiple points found in four individual patients (marked 1, 2, 3 and 4 in square boxes). Although a certain degree of variation may exist within this part of the postcentral gyri in the exact location of the tip, middle, and base of the tongue somatosensory cortical localizations, individual somatotopy respects the tip/medial–base/lateral tongue somatotopy. [Color figure can be viewed at wileyonlinelibrary.com]
Figure 4
Figure 4. The somatotopic sequence of the body
A, global somatotopic organization of the body (flesh colour), hand (mauve), and head (green). Dotted boxes: regions of interest for body and face somatotopies. B, top: somatotopic representation of the limbs with their medial‐to‐lateral somatotopic sequence. B, bottom: somatotopic representation of the face (excluding tongue represented in Fig. 3). The medial‐to‐lateral somatotopic sequence of the eyebrows, eyes, cheeks, both lips, teeth, gums, jaws, pharynx, and larynx is shown. [Color figure can be viewed at wileyonlinelibrary.com]
Figure 5
Figure 5. Anatomical relative variations of the human somatosensory cortex
Representation of the relative variations of the human somatosensory cortex on a scale from 0 (medial part) to 1 (lateral part of the postcentral gyrus). [Color figure can be viewed at wileyonlinelibrary.com]

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