Lack of somatotopy among corticospinal tract fibers passing through the primate craniovertebral junction and cervical spinal cord: pathoanatomical substrate of central cord syndrome and cruciate paralysis

OBJECTIVE In some cases of incomplete cervical spinal cord injury (iSCI) there is marked paresis and dysfunction of upper-extremity movement but not lower-extremity movement. A continued explanation of such symptoms is a somatotopic organization of corticospinal tract (CST) fibers passing through the decussation at the craniovertebral junction (CVJ) and lateral CST (LCST). In central cord syndrome, it has been suggested that injury to the core of the cervical cord may include selective damage to medially located arm/hand LCST fibers, without compromising laterally located leg fibers. Because such somatotopic organization in the primate CST might contribute to the disproportionate motor deficits after some forms of iSCI, the authors made a systematic investigation of CST organization in the CVJ and LCST using modern neuroanatomical techniques. METHODS High-resolution anterograde tracers were used in 11 rhesus macaque monkeys to define the course of the corticospinal projection (CSP) through the CVJ and LCST from the arm/hand, shoulder, and leg areas of the primary motor cortex (M1). This approach labels CST fibers of all sizes, large and small, arising in these areas. The CSP from the dorsolateral and ventrolateral premotor cortex and supplementary motor area were also studied. A stereological approach was adapted to quantify labeled fiber distribution in 8 cases. RESULTS There was no evidence for somatotopic organization of CST fibers passing through the CVJ or contralateral LCST. Fiber labeling from each cortical representation was widespread throughout the CST at the CVJ and LCST and overlapped extensively with fibers from other representations. This study demonstrated no significant difference between medial versus lateral subsectors of the LCST in terms of number of fibers labeled from the M1 arm/hand area. CONCLUSIONS This investigation firmly rejects the concept of somatotopy among CST fibers passing through the CVJ and LCST, in contrast with the somatotopy in the cortex, corona radiata, and internal capsule. All CST fibers in the CVJ and LCST would thus appear to be equally susceptible to focal or diffuse injury, regardless of their cortical origin. The disproportionate impairment of arm/hand movement after iSCI must therefore be due to other factors, including greater dependence of hand/arm movements on the CST compared with the lower limb. The dispersed and intermingled nature of frontomotor fibers may be important in motor recovery after cervical iSCI.

Case Study: Mapping Evoked Fields in Primary Motor and Sensory Areas via Magnetoencephalography in Tetraplegia

Devices interfacing with the brain through implantation in cortical or subcortical structures have great potential for restoration and rehabilitation in patients with sensory or motor dysfunction. Typical implantation surgeries are planned based on maps of brain activity generated from intact function. However, mapping brain activity for planning implantation surgeries is challenging in the target population due to abnormal residual function and, increasingly often, existing MRI-incompatible implanted hardware. Here, we present methods and results for mapping impaired somatosensory and motor function in an individual with paralysis and an existing brain–computer interface (BCI) device. Magnetoencephalography (MEG) was used to directly map the neural activity evoked during transcutaneous electrical stimulation and attempted movement of the impaired hand. Evoked fields were found to align with the expected anatomy and somatotopic organization. This approach may be valuable for guiding implants in other applications, such as cortical stimulation for pain and to improve implant targeting to help reduce the craniotomy size.

Gamma Oscillations and Coherence Are Weaker in the Dorsomedial Subregion of STN in Parkinson's Disease

Background: Deep-brain stimulation (DBS) of the subthalamic nucleus (STN) is an effective treatment for motor symptoms of advanced Parkinson's disease (PD). Due to a lack of detailed somatotopic organization in STN, the clinically most effective part of the STN for stimulation has already become one of the hot research focuses. At present, there are some reports about topographic distribution for different depths within the STN, but few about a mediolateral topography in this area.Objective: The objective was to investigate the local field potential (LFP) distribution patterns in dorsomedial and dorsolateral subparts of STN.Methods: In total, 18 PD patients eventually enrolled in this study. The DBS electrodes were initially located on the lateral portion of dorsolateral STN. Because of internal capsule side effects presented at low threshold (below 1.5 mA), the electrode was reimplanted more medially to the dorsomedial STN. In this process, intraoperative LFPs from dorsomedial and dorsolateral STN were recorded from the inserted electrode. Both beta power and gamma power of the LFPs were calculated using the power spectral density (PSD) for each DBS contact pair. Furthermore, coherence between any two pairs of contacts was computed in the dorsomedial and dorsolateral parts of STN, respectively. Meanwhile, the Unified Parkinson's Disease Rating Scale part III (UPDRS-III) was monitored prior to surgery and at the 6-month follow-up.Results: Compared to the dorsolateral part of STN, gamma oscillations (p < 0.01) and coherence (p < 0.05) were all weaker in the dorsomedial part. However, no obvious differences in beta oscillations and coherence were observed between the two groups (p > 0.05). Moreover, it should be noted that DBS of the dorsomedial STN resulted in significant improvement in the UPDRS-III in PD patients. There was a 61.50 ± 21.30% improvement in UPDRS-III scores in Med-off/Stim-on state relative to the Med-off state at baseline (from 15.44 ± 6.84 to 43.94 ± 15.79, p < 0.01).Conclusions: The specific features of gamma activity may be used to differentiate STN subregions. Moreover, the dorsomedial part of STN might be a potential target for DBS in PD.

Human Somatosensory Processing and Artificial Somatosensation

In the past few years, we have gained a better understanding of the information processing mechanism in the human brain, which has led to advances in artificial intelligence and humanoid robots. However, among the various sensory systems, studying the somatosensory system presents the greatest challenge. Here, we provide a comprehensive review of the human somatosensory system and its corresponding applications in artificial systems. Due to the uniqueness of the human hand in integrating receptor and actuator functions, we focused on the role of the somatosensory system in object recognition and action guidance. First, the low-threshold mechanoreceptors in the human skin and somatotopic organization principles along the ascending pathway, which are fundamental to artificial skin, were summarized. Second, we discuss high-level brain areas, which interacted with each other in the haptic object recognition. Based on this close-loop route, we used prosthetic upper limbs as an example to highlight the importance of somatosensory information. Finally, we present prospective research directions for human haptic perception, which could guide the development of artificial somatosensory systems.

Representational similarity scores of digits in the sensorimotor cortex are associated with behavioral performance

Previous studies aimed to unravel a digit-specific somatotopic organization in the primary sensorimotor (SM1) cortex. It is, however, yet to be determined whether such digit somatotopy is associated with motor performance (i.e., effector selection) and digit enslaving (unintentional co-contraction of fingers) during different types of motor tasks. Here, we adopted multivariate representational similarity analysis, applied to high-field (7T) MRI data, to explore digit activation patterns in response to online finger tapping. Sixteen young adults (7 males, mean age: 24.4 years) underwent MRI, and additionally performed an offline choice reaction time task (CRTT) to assess effector selection. During both the finger tapping task (FTT) and the CRTT, force sensor data of all digits were acquired. This allowed us to assess digit enslaving (obtained from CRTT & FTT), as well as digit interference (i.e., erroneous effector selection; obtained from CRTT) and correlate these variables with digit representational similarity scores of SM1. Digit enslaving during finger tapping was associated with contralateral SM1 representational similarity scores of both hands. During the reacton time task, digit enslaving of the right hand only was associated with representational similarity scores of left SM1. Additionally, right hand digit interference was associated with representational similarity scores of left S1. In conclusion, we demonstrate a cortical origin of digit enslaving, and uniquely reveal that effector selection performance is predicted by digit representations in the somatosensory cortex.

Rescue Subthalamic Deep Brain Stimulation for Refractory Meige Syndrome

Meige syndrome is a segmental form of dystonia. It is a disabling disease, especially when refractory to treatment with botulinum toxin. A well-established therapeutic option is deep brain stimulation (DBS), and the target in bilateral globus pallidus internus (GPi DBS) demonstrated satisfactory short- and long-term efficacy. However, some patients present minor or suboptimal responses after GPi DBS, and in those cases, rescue DBS may be appropriate. The present case illustrates a good outcome after subthalamic nucleus (STN) and not after GPi DBS (considering that both were well positioned and had adequate programming). The larger dimension of the GPi and its somatotopic organization, with the stimulation outside the “face region,” could explain our outcomes.

Charcot's motor brain map and 19th-century neurosurgery

Neurosurgery is predicated on the knowledge of the structure-function relationship of the brain. When the topic is broached in its historiography, it begins with Fritch and Hitzig's report on the localization of motor function in the cortex of the dog and skips rapidly to Wilder Penfield's homunculus. In that gap are found the origins of modern neurosurgery in 3 papers published by Jean-Martin Charcot and Albert Pitres between 1877 and 1879 in which they describe the somatotopic organization of the human motor cortex and draw the first human brain map. Their findings, obtained through the clinicopathological method, gave relevance to David Ferrier's observations in animals. Their work was extensively cited, and their illustrations reproduced by Ferrier in his landmark lecture to the Royal College of Physicians in 1878. It was known to William Macewen, who used localization to guide him in resecting intracranial mass lesions, and to William Osler and John Hughlings Jackson, who were early advocates of intracranial surgery. This paper describes Charcot and Pitres' discovery of the cortical origin of human voluntary movement and its somatotopic organization, and their influence on 19th-century intracranial surgery. It fills a gap in the historiography of cerebral localization and neurosurgery.