Transhemispheric depolarizations persist in the intracerebral hemorrhage swine brain following corpus callosal transection

Spontaneous episodes of spreading depression (SD) originating in multiple sources adjacent to a focal intracerebral hemorrhage (ICH) propagate into brain regions away from the lesion site soon after injury onset. Although these transient depolarizations have not been established in the opposite hemisphere of the swine ICH model, we have reported a diminishing of sensory responsiveness in this homotopic brain region following induction of a unilateral hemorrhage lesion. This study examined whether transient depolarizations exist in this distant brain region contralateral to the ICH site. Electrocorticographic (ECoG) recordings of brain activity were collected bilaterally from the primary somatosensory (SI) cortices of the swine brain prior to and immediately after an intracerebral injection of collagenase or saline or the insertion of the infusion pipette into the SI cortex of the right hemisphere. Transient depolarizations were present in both hemispheres of all the experimental groups. The earliest negative DC potential shifts were observed in the injured SI cortex within the first hour after collagenase injection, as compared to T = 3 h in the saline-injected group and T = 4 h in the infusion pipette only group. In contrast, transient depolarizations were first detected in the left SI cortex contralateral to the lesioned hemisphere within 2 h after collagenase infusion, by T = 4h after saline infusion and by T = 3 h in the pipette only group. Propagating waves of negative DC potential shifts continued in both brain hemispheres, particularly in the ICH group, throughout the 11-h recording period. This novel finding of recurrent depolarizing waves in the hemisphere contralateral to the injury site prompted us to examine whether corpus callosal connections may play a role in this transhemispheric phenomenon. In a separate group of animals, the corpus callosum was transected prior to acquiring DC potential recordings and collagenase injection. The onset pattern of negative DC shifts in the callosotomized + collagenase-injected group was similar to the collagenase group with an intact corpus callosum. Initial generation of SD in the callosotomized + collagenase-injected group occurred by T = 1 h in the ICH injured right hemisphere and T = 2 h in the contralateral hemisphere. These transient depolarizations also persisted throughout 11-h recording period indicating that the corpus callosal transection did not hinder these remote propagating waves of depolarization. The presence of SD in the SI cortices of both hemispheres in all experimental groups of this study suggests that a focal mechanical or hemorrhagic injury increases the susceptibility of distant ipsilateral and contralateral brain regions to depolarizing perturbations. The mechanism for these transient depolarizations in the contralateral hemisphere apparently does not involve transhemispheric propagation along corpus callosal fibers.