Somatotopic Mapping of the Developing Sensorimotor Cortex in the Preterm Human Brain

Abstract

In the mature mammalian brain, the primary somatosensory and motor cortices are known to be spatially organized such that neural activity relating to specific body parts can be somatopically mapped onto an anatomical “homunculus”. This organization creates an internal body representation which is fundamental for precise motor control, spatial awareness and social interaction. Although it is unknown when this organization develops in humans, animal studies suggest that it may emerge even before the time of normal birth. We therefore characterized the somatotopic organization of the primary sensorimotor cortices using functional MRI and a set of custom-made robotic tools in 35 healthy preterm infants aged from 31 + 6 to 36 + 3 weeks postmenstrual age. Functional responses induced by somatosensory stimulation of the wrists, ankles, and mouth had a distinct spatial organization as seen in the characteristic mature homunculus map. In comparison to the ankle, activation related to wrist stimulation was significantly larger and more commonly involved additional areas including the supplementary motor area and ipsilateral sensorimotor cortex. These results are in keeping with early intrinsic determination of a somatotopic map within the primary sensorimotor cortices. This may explain why acquired brain injury in this region during the preterm period cannot be compensated for by cortical reorganization and therefore can lead to long-lasting motor and sensory impairment.

Body-map proto-organization in newborn macaques

“…Interestingly, the magnitude of fMRI evoked responses to stimulation of the face, hand and foot was weaker in our younger monkeys (up to 146 days) than in older monkeys ( Supplementary Figure 1), suggesting that while the somatotopic organization is adult-like, response properties remain immature for the first several months. Our data are consistent with a recent paper that showed spatially distinct representations of the face, hand, and ankle within primary somato-motor cortex in preterm humans 40 . Our data demonstrate that the large-scale topographic organization of primary somato-motor cortex is adult like at birth and indicates that postnatal experience is not needed for their formation.…”

Resting-state connectivity reveals a role for sensorimotor systems in vocal emotional processing in children

“…The medial and lateral peaks that we found are additionally suggestive of a close link between perceptual and production mechanisms in the motor system. We know from the motor literature that there are somatotopically organized maps in SMA and in motor and lateral premotor cortices (e.g., Fontaine et al, 2002;Muakkassa and Strick, 1979;Zeharia et al, 2012), maps that can be seen already in the human preterm period (Dall'Orso et al, 2018). In SMA, the peak that we found corresponds to the site established to control the production of orofacial movements and vocalizations/speech (e.g., Fontaine et al, 2002;Fried et al, 1991;Kirzinger and Jürgens, 1982).…”

Neurocognitive consequences of hand augmentation

“…Hand representation in the primary sensorimotor cortex of the brain has a well-established functional structure that develops very early on (6,7). It is highly consistent within (8) and across (9) participants and is preserved even after severe loss of motor functions due to e.g.…”