Brain injury forces of moderate magnitude elicit the fencing response

Abstract

Introduction: Traumatic brain injury is heterogeneous, both in its induction and ensuing neurological sequelae. In this way, medical care depends on accurately identifying the severity of injury-related forces. Clinically, injury severity is determined by a combination of the Glasgow Coma Scale, length of unconsciousness, posttraumatic amnesia, and persistence of neurological sequelae. In the laboratory, injury severity is gauged by the biomechanical forces and the acute suppression of neurological reflexes. The present communication describes and validates the "fencing response" as an overt indicator of injury force magnitude and midbrain localization to aid in injury identification and classification.

Methods: Using YouTube, the Internet video database, videos were screened for head injury resulting in unconsciousness and documented for the fencing response. Adult male rats were subjected to midline fluid percussion brain injury at two severities, observed for acute neurological reflexes and the midbrain evaluated histopathologically.

Results: Tonic posturing (fencing response) has been observed to precede convulsions in sports injuries at the moment of impact, where extension and flexion of opposite arms occurs despite body position or gravity. Of the 35 videos identified by an impact to the head and period of unconsciousness, 66% showed a fencing response at the moment of impact, regardless of the side of impact, without ensuing convulsion. Similarly, diffuse brain-injured rats demonstrate a fencing response upon injury at moderate (1.9 atm, 39/44 animals) but not mild severity (1.1 atm, 0/19 animals). The proximity of the lateral vestibular nucleus to the cerebellar peduncles makes it vulnerable to mechanical forces that initiate a neurochemical storm to elicit the neuromotor response, disrupt the blood-brain barrier, and alter the nuclear volume.

Conclusions: Therefore, the fencing response likely indicates neurological disturbance unique from convulsion associated with mechanical forces of moderate magnitude imparted on the midbrain and can assist in guiding medical care after injury.

FIGURE 1—

Incidence of the fencing response versus nonfencing responses in the compilation of YouTube^™ knockout videos.

FIGURE 2—

Schematic illustrations of the fencing response during a knockout. A, The individual receives a punch to the head. B, After the traumatic blow to the head, the unconscious individual immediately exhibits extension in one arm and contralateral flexion while falling to the ground. C, During prostration, the rigidity of the extended and flexed arms is retained for several seconds as flaccidity gradually returns.

FIGURE 3—

In the rodent, the incidence of the fencing response is injury severity dependent. A, FPI is scalable between mild and moderate severity on the basis of injury atmospheres (atm). B, The duration of righting reflex suppression increases with injury severity. Uninjured sham animals have ~10-s righting reflex times. C, Mild brain-injured animals do not demonstrate a fencing response. In moderate brain-injured animals, the fencing response predominates.

FIGURE 4—

Time-lapse images of the fencing response in the rat after fluid percussion brain injury. Anesthetized animals are hand-held in a right lateral recumbent position and attached to the injury device, at right (not shown). A, Before the injury, the animal’s forearms are flaccid and fall toward the ground. B, At 0.0 s, the brain injury is induced. C–K, The extension of the left limb and flexion of the right limb, coupled with the formation of “fists” in both paws, can be seen over the 0.2-s intervals. L, The rigidity of the response is sustained as flaccidity gradually returns.

FIGURE 5—

Brainstem histopathology after midline fluid percussion brain injury in the rat. A, E, and I, The proximity of the LVN to the inferior cerebellar peduncles (icp) and vestibulocochlear nerve (8vn) predicts axonal pathology from injury-related forces. In moderate brain-injured rats 15 min after injury, lateral vestibular neurons appear shrunken (B) and proximal to blood–brain barrier (BBB) disruption as indicated by IgG extravasation (C, D). In mild brain-injured rats, neurons display altered morphology (F) and BBB disruption (G, H). The lateral vestibular nuclei in sham animals have large motor neurons (J) and patent BBB (K, L). Scale bars, 50 μm.

FIGURE 6—

Using the rotator, the volume of a three-dimensional object can be estimated in two-dimensional tissue sections. For each neuron identified within the sampling frame, the neuronal nuclear volume was estimated. Measurements were pooled within a group and binned into 20 size ranges. The percentage of nuclear volume measurements within each bin size is plotted for each group at 10–15 min after sham or brain injury. After mild and moderate brain injury, the nuclear size distribution shows a shift toward smaller volumes compared with the sham group. To provide a reference point, the mean nuclear volume for the sham group is indicated by the black vertical line in each graph.