Bell′s Cruciate Paralysis

Cruciate paralysis was first described clinically by Bell as a syndrome characterized by “paralysis in both arms without weakness in the legs.”11–15 Causative mechanisms are typically due to cervical fractures in the region of the CVJ.15 The basis for the clinical presentation was thought to be due to midline damage to the rostral portion of the pyramidal decussation that would selectively injure the fibers of the corticospinal tract subserving hand and arm function.7 In 1901, Wallenberg reported on the complex anatomy present at the CVJ, including the illustration that fibers serving function to the arms decussate more rostrally than those subserving the legs.16 He described a patient in his report with “hemiplegia cruciata” or ipsilateral arm weakness and contralateral leg weakness. Wallenberg′s presumption was that this injury could be explained by rostral unilateral damage to the recently crossed corticospinal fibers of the arm and uncrossed fibers of the legs ( Fig. 5.1 ). This observation suggested a somatotopical organization of these fibers at the CVJ.17 Although this theory has prevailed in neuro-anatomical texts, no evidence to date has supported the presence of a somatotopically organized corticospinal tract at the CVJ.18,19

Central Cord Syndrome

Schneider and colleagues initially described central cord syndrome as a neurological ailment of the CVJ that caused disproportionate arm versus leg weakness similar in clinical presentation to Bell′s cruciate paralysis.20 The syndrome is reported more frequently among older persons with cervical spondylosis and spinal stenosis and accounts for 9% of the total incidence of spinal cord injuries.21 The proposed pathophysiological mechanism was thought to be due to selective injury to the medial based arm fibers of a somatotopically organized corticospinal tract within the posterolateral funiculus of the spinal cord.22

The Evidence Against Somatotopical Organization of the Corticospinal Tract

Neuroanatomical studies in primates have never supported the theory that there is a somatotopic organization of the corticospinal tract (CST). Pre- and post-decussation fibers are diffusely located within the pyramids and corticospinal tract, respectively, in the posterolateral funiculus as demonstrated by Marchi degeneration studies and modern tracer techniques.23–26 Similar evidence can be extracted from human reports where lesions of the central nervous system cause retrograde degeneration of the CST in the brainstem and spinal cord.27,28 Although there appears to be laminar organization spanning the motor cortex, internal capsule, and pons, it is lost at the levels of the medulla and spinal cord. Therefore, the manner in which both Bell′s cruciate paralysis and central cord syndrome (CCS) were once thought to have occurred via injury to a somatotopically organized CST must be rethought.

One potential theory to explain the differential findings between upper and lower extremity function in these syndromes, which does not require somatotopic organization of the CST, may be that the CST is more important for the function of the hands and arms than the lower extremities. This difference could explain the observation that an injury at the CVJ could present as a disproportionate weakness of the upper extremities versus the lower. As one ascends the phylogenetic scale, the CST assumes a more important role in movements associated with hand function.29–32 In higher order mammals with upright postures and complex hand functions, the CST becomes larger in diameter due to an increased number of axons that synapse on motor neurons in the ventral horn of the spinal cord at these associated upper levels.29–31,33 Sherrington was so impressed with this increase in size of the CST that he remarked, “There is no other system which shows such increase in relative size as traced from lower to higher mammalian types.”34 Following an injection of an anterograde tracer into the primate motor cortex, Pappas and colleagues confirmed that the CST lacks a somatotopical organization at the level of the medullary decussation.26

Two alternative mechanisms have been proposed to explain the clinical findings in cruciate paralysis. The first includes selective injury to the ventral CST, which can serve as a significant outflow for the CST that is absent below the cervical enlargment.28,35 Focal damage to this tract from an anterior spinal fracture could explain the findings in cruciate paralysis. The other mechanism consists of an injury to the collateral fibers of the CST to the brainstem, central gray matter, and dorsal column nuclei. Although the importance of these collateral fiber tracts has yet to be determined, they appear to be segregated from fiber terminations supplying the hind limb.

Selective Primate Corticospinal Tract Lesioning and the Importance of Hand Function

Several studies have focused on the effects following transection of one or both CSTs at the level of the medullary pyramids or cerebral peduncles in the primate.36–39 In primates, the CST is isolated from other tracts in the brainstem and spinal cord and can therefore be selectively injured. In general, incomplete lesions of the CST do not produce catastrophic motor deficits and recover over time. The predominate deficit following selective lesions of the CST in primates is greater hand and arm weakness when compared with the distal extremities (e.g., elimination of discrete finger movements, diminished general usage, loss of initiative, defective contact placing and grasping, and difficulty in the release of a grasp once initiated).36,40 Bucy and colleagues described the return of function in these primate studies in a similar manner as that observed with Bell′s cruciate paralysis and CCS in observed in humans (“recovery began in the proximal musculature and progressed to the distal musculature as the lower extremities usually recovered before the upper extremities”).41

Recent data published by Jimenez and colleagues investigated whether there was a reduction in the large a motor neurons at C7, C8, and T1 following traumatic central cord syndrome in postmortem human cervical spinal cord specimens. The spinal cords were divided into acute/subacute (less than 5 weeks, n = 2) and chronic (greater than 5 weeks, n = 3) depending on the time of death after the initial injury. The chronic group was further subdivided into a high-level cervical group (injury at C2, n = 1) and low-level cervical group (injury at C5-C6, n = 2). They found a significant reduction in a motor neurons at C7-T1, with respect to the chronic low-level cervical injury group, and attributed this finding to the proximity of the initial injury to these structures. Jimenez and colleagues also noted that CCS can occur following a more rostral injury to the CST without affecting these lower a motor axons controlling hand function ( Fig. 5.2 ).42

Cortical and Spinal Plasticity Following Experimental Selective Lesioning

Nishimura and colleagues explored the mechanism for recovery in hand function following distinct lesions in the CST of macaque monkeys at the C4/5 levels. They theorized that alternate indirect corticomotoneuronal pathways (e.g., sub-cortical or spinal interneuronal systems) were responsible for this recovery. Positron emission tomography (PET) postinjury revealed that activity increased in a similar pattern to preinjury early in the postinjury period. Yet later, new areas of brain activity were documented. To confirm whether these increased regions of activity observed in PET contributed to hand-directed activity, Nishimura and colleagues selectively inhibited these areas with a gamma-aminobutyric acid type A receptor agonist. Their work suggests that alternate pathways are activated late in the recovery phase with the end result of the restoration of hand function.43

Maier and colleagues have examined spinal cord plasticity following transection of the CST at the level of the brainstem in rats.44 They restricted movement of the unaffected limb, forcing the animals to use the impaired one. This forced rehabilitation of the affected limb was followed by a fuller behavioral recovery on physical tasks in the experimental group. Histologically the group demonstrated lesion-induced growth in the CST from the unlesioned side across the midline via CST collaterals.

Evidence Against Somatotopical Organization of the Corticospinal Tract in Humans

Findings from lesion studies at the CVJ in primates can be extrapolated and applied to clinical and anatomical data available in humans to help explain alternative mechanisms for the neurological findings observed in Bell′s cruciate paralysis and CCS. There is a size difference when comparing the CST in humans versus primates. Napier has attributed this increase in size and number of fibers in humans to further refinements of hand dexterity and function.46 Thus, it is plausible that an injury to this tract may result in greater hand and arm dysfunction in humans when compared with a similar injury in primates.

Furthermore, injuries would also have to be localized to a region of small area located at the medullary decussation or cervical spinal cord to produce differences in the closely packaged hand, arm, and leg fibers. Neuropathological studies of patients following spinal cord injury reveal that focal injuries of the cervical and medullary region are quite uncommon and that wide variations exist between lesion volumes. Thus, in humans, Bell′s cruciate paralysis and CCS may be explained by an injury to the entire corticospinal tract. A case report of a 72-year-old patient with cruciate paralysis (0/5 strength in the upper extremities versus 3/5 in the lower) following a fracture of the C2 vertebrae revealed anterograde degeneration of the spinal cord as far down inferiorly as the lumbar cord on pathological examination.13 This finding suggests that fibers supplying the lower extremities were not spared as previously assumed by Bell.

Composition of the corticospinal tract includes 60% of fibers arising from the primary motor cortex (Brodmann area 4).47 The diameter of the largest axons ranges from 10 mm to 25 mm. They arise from the pyramidal cells of Betz, which account for only 4% of the total fibers in the corticospinal tract.48 Large-diameter fibers synapse directly on a motor neurons that tend to supply distal musculature of the upper extremities.33,48,49 However, most of the fibers in the CST are of small diameter, conduct signals at slow rates, and synapse with interneurons.49 Because traumatic injuries are more likely to injure large fibers than injure small ones, a diffuse injury could selectively affect them and cause a disparate injury to hand function.50,51