Anatomical and functional properties of the foot and leg representation in areas 3b, 1 and 2 of primary somatosensory cortex in humans: A 7T fMRI study

Primary somatosensory cortex (S1) processes somatosensory information and is composed of multiple subregions. In particular, tactile information from the skin is encoded in three subregions, namely Brodmann areas (BAs) 3b, 1 and 2, with each area representing a complete map of the contralateral body. Although, much is known about the somatotopic organization of the hand in human S1, less research has been carried out regarding the somatotopic maps of the foot and leg in S1. Moreover, a latero-medial S1 organization along the superior part of the postcentral gyrus has been reported when moving from hip to toes, yet to date there is no study investigating leg/foot maps within the different subregions of S1. Using ultra-high field MRI (7T), we mapped six cortical representations of the lower limb (hip to toes) at the single subject level and performed this analysis separately for BAs 3b, 1 and 2. Analyzing the BOLD responses associated with tactile stimulations of the mapped foot and leg regions on each side, we quantified the extent and the strength of activation to determine somatotopic organization. In addition, we investigated whether each mapped representation also responded to the stimulation of other body parts (i.e. response selectivity) and conducted dissimilarity analysis relating these anatomical and functional properties of S1 to the physical structure of the lower limbs. Our data reveal somatotopy for the leg, but not for the foot in all investigated BAs, with large inter-subject variability. We found only minor differences between the properties of the three investigated BAs, suggesting that S1 maps for the lower limbs differ from those described for the hand. We also describe greater extent/strength of S1 activation for the big toe representation (compared to the other mapped representations) within all BAs, suggesting a possible homology between the first digit of upper and lower extremity in humans, and report different patterns of selectivity in the foot representations (i.e. lower selectivity) compared to the other leg representations (i.e. greater selectivity). These data provide a detailed description of human S1 subregions for the foot and leg, highlight the importance of high-resolution mapping studies and of single subject analysis, and indicate potential differences between the lower and the upper limb.

Human finger somatotopy in areas 3b, 1, and 2: A 7T fMRI study using a natural stimulus

Olaf Blanke, Juliane Farthouat, Rolf Gruetter, Roberto Martuzzi, Wietske Van der Zwaag

To study the properties of human primary somatosensory (S1) cortex as well as its role in cognitive and social processes, it is necessary to noninvasively localize the cortical representations of the body. Being arguably the most relevant body parts for tactile exploration, cortical representations of fingers are of particular interest. The aim of the present study was to investigate the cortical representation of individual fingers (D1-D5), using human touch as a stimulus. Utilizing the high BOLD sensitivity and spatial resolution at 7T, we found that each finger is represented within three subregions of S1 in the postcentral gyrus. Within each of these three areas, the fingers are sequentially organized (from D1 to D5) in a somatotopic manner. Therefore, these finger representations likely reflect distinct activations of BAs 3b, 1, and 2, similar to those described in electrophysiological work in non-human primates. Quantitative analysis of the local BOLD responses revealed that within BA3b, each finger representation is specific to its own stimulation without any cross-finger responsiveness. This finger response selectivity was less prominent in BA 1 and in BA 2. A test-retest procedure highlighted the reproducibility of the results and the robustness of the method for BA 3b. Finally, the representation of the thumb was enlarged compared to the other fingers within BAs 1 and 2. These findings extend previous human electrophysiological and neuroimaging data but also reveal differences in the functional organization of S1 in human and nonhuman primates. Hum Brain Mapp, 2012. © 2012 Wiley Periodicals, Inc.

Wiley-Blackwell2014

Upper limb cortical maps in amputees with targeted muscle and sensory reinnervation

Michel Akselrod, Olaf Blanke, Maria Laura Blefari, Elisa Canzoneri, Roberto Martuzzi, Giulio Rognini, Roy Salomon, Andrea Serino, Wietske Van der Zwaag

Neuroprosthetics research in amputee patients aims at developing new prostheses that move and feel like real limbs. Targeted muscle and sensory reinnervation (TMSR) is such an approach and consists of rerouting motor and sensory nerves from the residual limb towards intact muscles and skin regions. Movement of the myoelectric prosthesis is enabled via decoded electromyography activity from reinnervated muscles and touch sensation on the missing limb is enabled by stimulation of the reinnervated skin areas. Here we ask whether and how motor control and redirected somatosensory stimulation provided via TMSR affected the maps of the upper limb in primary motor (M1) and primary somatosensory (S1) cortex, as well as their functional connections. To this aim, we tested three TMSR patients and investigated the extent, strength, and topographical organization of the missing limb and several control body regions in M1 and S1 at ultra high-field (7 T) functional magnetic resonance imaging. Additionally, we analysed the functional connectivity between M1 and S1 and of both these regions with fronto-parietal regions, known to be important for multisensory upper limb processing. These data were compared with those of control amputee patients (n = 6) and healthy controls (n = 12). We found that M1 maps of the amputated limb in TMSR patients were similar in terms of extent, strength, and topography to healthy controls and different from non-TMSR patients. S1 maps of TMSR patients were also more similar to normal conditions in terms of topographical organization and extent, as compared to non-targeted muscle and sensory reinnervation patients, but weaker in activation strength compared to healthy controls. Functional connectivity in TMSR patients between upper limb maps in M1 and S1 was comparable with healthy controls, while being reduced in non-TMSR patients. However, connectivity was reduced between S1 and fronto-parietal regions, in both the TMSR and non-TMSR patients with respect to healthy controls. This was associated with the absence of a well-established multisensory effect (visual enhancement of touch) in TMSR patients. Collectively, these results show how M1 and S1 process signals related to movement and touch are enabled by targeted muscle and sensory reinnervation. Moreover, they suggest that TMSR may counteract maladaptive cortical plasticity typically found after limb loss, in M1, partially in S1, and in their mutual connectivity. The lack of multisensory interaction in the present data suggests that further engineering advances are necessary (e.g. the integration of somatosensory feedback into current prostheses) to enable prostheses that move and feel as real limbs.

Oxford University Press2017

Wearable multimodal tactile interfaces for augmenting haptic perception

Simon Gallo

Haptic feedback has been used to faithfully restitute the haptic sense lacking during telemanipulation, but also for providing auxiliary information via the haptic channel to restore functional perception of missing or damaged senses, e.g. sensory substitution for the visually impaired. Yet, despite the growing number of applications that would benefit from haptic feedback, its penetration rate remains low. We have identified three under-researched features of haptic feedback that we believe are necessary to break the bottleneck: multimodality, thermal feedback and wearability. Indeed, while haptic perception results from the integration of multiple somatosensory inputs, the interactions between haptic modalities have rarely been investigated. Thermal feedback is an ideal candidate to explore these interactions as skin temperature is known to modulate the sensitivity of skin receptors. Finally, although haptic perception is distributed over the entire body, most multimodal haptic devices are still bulky and rigid, thus limiting their usage to specific body parts and applications. As the integration of multiple feedback modalities into a flexible display is complex, the benefits of these three features need to be demonstrated. This motivated the developments presented in this thesis. First, we miniaturized and integrated thermal feedback in multisensory platforms to investigate its role in conveying non-sensory information and modulating tactile perception. The first study showed that users are able to distinguish the temperature difference between two adjacent thermal stimuli presented under the fingertip by a high-density thermal display, highlighting the potential of miniaturized displays to deliver thermally-encoded information through small skin areas. A second study showed that modifying the skin temperature yielded changes in the precision of stiffness judgments up to 22.3%, suggesting that thermal feedback can be used to modulate the perception of complex haptic percepts. Moving towards complete wearability, we introduced a wearable multimodal display that matches the skin curvature to deliver thermo-tactile cues optimally, as supported by the high usersâ identification rates of simulated materials. Subsequently, we developed a portable hydraulic actuation that generates multimodal tactile feedback in remote 3D-printed flexible displays, paving the way to truly versatile wearable multimodal displays. Finally, a tactile suit remapping tactile and proprioceptive sensations from the virtual legs of an avatar onto the upper limbs of paraplegic patients is developed. We show that the patients were able to perceive the position of the virtual legs based on tactile feedback alone, that the use of tactile feedback in synchrony with the avatarâs walk changed the perception of the boundaries of their body, and that the modulation of the tactile stimulation induced a robust sensation of walking on different floors. These results demonstrate the potential of wearable tactile displays to create perceptual orthoses. In this work, we have developed the tools to deliver a multimodal tactile stimulation using wearable thermo-tactile displays and have shown how their unique features can impact fields such as surgical and rehabilitation robotics. These findings encourage the future development of wearable multimodal tactile displays taking advantage of the synergies between haptic modalities to improve teleoperation and sensory rehabilitation.