Cardiovascular responses to static exercise in patients with Brown-Séquard syndrome

The purpose of this study was to determine the contributions of central command and the exercise pressor reflex in regulating the cardiovascular response to static exercise in patients with Brown-Sequard syndrome. In this rare condition, a hemisection of the spinal cord typically leaves one side of the body with diminished sensation and normal motor function and the other side with diminished motor function and normal sensation. Four, otherwise healthy, patients with Brown-Sequard syndrome and varying degrees of motor and sensory dysfunction were studied during four isometric knee extension protocols involving both voluntary contraction and electrically stimulated contractions of each leg. Heart rate, blood pressure, force production and ratings of perceived exertion were measured during all conditions. Measurements were also made during post-contraction thigh cuff occlusion and during a cold pressor test. With the exception of electrical stimulation of the leg with a sensory deficit, protocols yielded increases in heart rate and blood pressure. Cuff occlusion sustained blood pressure above resting levels only when the leg had intact sensation. While voluntary contraction (or attempted contraction) of the leg with a motor deficit produced the lowest force, it produced the highest ratings of perceived exertion coupled with the greatest elevations in heart rate and blood pressure. These data show that the magnitude of the heart rate and blood pressure responses in these patients was greatly affected by an increased central command; however, there were marked cardiovascular responses due to activation of the exercise pressor reflex in the absence of central command. Despite numerous studies investigating the neural control mechanisms underlying cardiovascular adjustments to static exercise, our understanding of this topic remains incomplete. The two most widely accepted mechanisms, first forwarded by Johansson (1893), are that the stimulus for the cardiovascular response to exercise originates from (i) the exercising muscle (muscle afferent input), and/or (ii) the brain (central command). Both central command (Krogh & Lindhard, 1912; Goodwin et al. 1972) and reflex input from the contracting muscles (Alam & Smirk, 1937; Coote et al. 1971; McCloskey & Mitchell, 1972) are known to elicit increases in cardiovascular function. Furthermore, both central command and the exercise pressor reflex can act as redundant control mechanisms (Mitchell & Schmidt, 1983; Mitchell, 1990). As a means of identifying their individual contributions, investigators have employed numerous strategies to alter either central command or muscle afferent input during exercise; however, few of these studies have explored this interaction utilizing a patient model. There have been limited studies of patients with sensory and motor disorders and of those studies, the results have been somewhat inconsistent. Alam & Smirk (1938) studied a patient lacking all sensory input from one leg and found that cardiovascular responses during one-legged volitional exercise were similar for both legs, but that blood pressure fell during post-exercise circulatory occlusion in the limb lacking sensation. The authors concluded that the cardiovascular activation must have resulted from a central neural mechanism during exercise. Similarly, Duncan et al. (1981) reported increases in heart rate and arterial pressure during static exercise in two subjects with sensory neuropathies. One subject had a partial Brown-Sequard lesion and the other a congenital sensory neuropathy. Both subjects could perform isometric forearm exercise in the absence of sensory afferent input. They concluded that cardiovascular responses could be elicited without input from the contracting muscle. In contrast to these studies, Lind et al. (1968) exercised a patient with syringomelia that effected the forearm sensory nerves in one arm, and observed no elevation in arterial pressure when the affected arm was used. The investigators concluded that cardiovascular responses to static exercise were indeed dependent upon afferent input from the contracting limb. Taken together these findings do not present a consistent picture of the relationship between central command and the exercise pressor reflex during exercise in these patients. In order to further our understanding in this area, patients with Brown-Sequard syndrome were studied. The Brown-Sequard syndrome is classically defined as a spinal hemiplegia resulting from the effect of a disease of, or an injury to, the lateral half of the spinal cord (Brown-Sequard, 1868; Fig. 1). The neurological signs caudal to the hemisected region of the spinal cord are utilized by physicians to clinically diagnose the Brown-Sequard syndrome in spinal cord-injured patients. This syndrome, which occurs in less than 1 % of all spinal cord injuries, results in absent or diminished sensation for pain and temperature in one leg because of interruption of the spinothalamic tract and paresis or paralysis of the contralateral leg due to interruption of the corticospinal tract. Of specific relevance to this investigation, signals from group III and IV muscle afferents travelling through the dorsal horn (Light & Perl, 1985) are also disrupted unilaterally. Thus Brown-Sequard patients provide an excellent model for investigating the individual roles of central command and the exercise pressor reflex in determining the cardiovascular response during static exercise. The purpose of this study was to assess the cardiovascular responses during voluntary and electrically stimulated exercise in a group of spinal cord-injured subjects with Brown-Sequard syndrome and to determine the individual contributions of central command and the exercise pressor reflex. Figure 1 Schematic diagram representing a spinal cord section with selected tracts METHODS Subjects Four spinal cord-injured patients, previously diagnosed with Brown-Sequard syndrome by their neurologists, were recruited for participation in the study. These patients had all undergone physical therapy for their injury and had no other medical complications at the time of the study. All patients signed an informed consent form as approved by The University of Texas Southwestern Medical Center Institutional Review Board and conforming to guidelines set forth in the Declaration of Helsinki. Subjects' descriptive characteristics are presented in Table 1. Table 1 Subject descriptive characteristics Patient 01 was a 28-year-old female who sustained an injury to cervical level 5 secondary to a gunshot wound 10 years ago. She presented with motor function (grade 3+/5 or greater) in her right extremities and non-functional motor strength in her left lower extremity. Although she was an independent ambulator in the household setting, she was limited in the community setting secondary to the weakness in her left leg. Sensation to pain and temperature was intact in her left extremities and absent in her right extremities. This profound absence was evident by the numerous numbers of inflammatory insect bites observed on her right upper extremity secondary to reported fire ant bites from a recent picnic outing. Patient 02 was a 30-year-old female who had recently (6 months) sustained a cervical level 5 injury in a fall from a trampoline. She demonstrated the greatest neurological recovery of the four patients studied. She had normal strength in her left extremities. Although her strength was functional in her right extremities, it tested in the 3+ to 4 range on a 5-point scale. She was an independent ambulator and was able to negotiate all obstacles in the community setting, but was limited in endurance. Sensation both to pinprick and temperature was normal in her right extremities but impaired in her left extremities. Patient 03 was a 30-year-old male who had injured thoracic level 4 in a motor vehicle accident 19 years ago. He presented with normal strength in the right lower extremity and weakness in his left lower extremity. He could ambulate with the assistance of a left orthosis, but relied on his wheelchair for mobility. Sensation to pinprick and temperature was intact in his left lower extremity and absent in the contralateral right lower extremity. Patient 04 was a 28-year-old male who had sustained an injury to thoracic level 8 in a motor vehicle accident 8 years previously. Of the four subjects, he presented with the least neurological recovery. He demonstrated absent volitional control in his left leg with only involuntary muscle spasms present. Although voluntary muscle contractions were present in the right lower extremities, these were non-functional. The patient depended on his wheelchair for all mobility. The left lower extremity demonstrated intact sensation to pinprick and temperature with absent sensation to pinprick and temperature in the right lower extremity.