Changes in glutamate concentration, glucose metabolism, and cerebral blood flow during focal brain cooling of the epileptogenic cortex in humans

Nomura, Sadahiro; Fujii, Masami; Inoue, Takao; He, Yeting; Maruta, Yuichi; Koizumi, Hiroyasu; Suehiro, Eiichi; Imoto, Hirochika; Ishihara, Hideyuki; Oka, Fumiaki; Matsumoto, Mishiya; Owada, Yuji; Yamakawa, Takeshi; Suzuki, Michiyasu

doi:10.1111/epi.12600

Cited by 34 publications

(40 citation statements)

References 32 publications

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“…It has long before suggested that neurotransmitter release has temperature dependence which causes changes in PSP generation [ 61 ]. This was confirmed by experimental observations of reduced efficacy of neurotransmitter vesicle release and reduced extracellular glutamate concentration during cooling [ 38 , 40 ] that imply lower neurotransmitter concentration at the synapses to bind at the post-synaptic receptor and generate PSP. In light of this, it was straightforward to assume a temperature dependence on the post-synaptic impulse response function in a neural mass model.…”

Section: Discussionsupporting

confidence: 66%

“…We explore prospective mechanisms of cooling on epileptic discharges by introducing temperature dependence in the neural mass model of Wendling et al in light of findings observed in in vitro and in vivo experiments published in literature. In particular, changes in synaptic dynamics were reported from in vitro cooling experiments such as reduction in the efficacy of neurotransmitter vesicle release [ 38 ], loss of dendritic spines [ 39 ] and reduced glutamate concentrations [ 40 , 41 ], suggesting a possible synaptic mechanism. A recent study with patients with intractable epilepsy also reports reduced extracellular glutamate and GABA concentrations during focal brain cooling [ 42 ].…”

Section: Introductionmentioning

confidence: 99%

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Differential temperature sensitivity of synaptic and firing processes in a neural mass model of epileptic discharges explains heterogeneous response of experimental epilepsy to focal brain cooling

et al. 2017

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Experiments with drug-induced epilepsy in rat brains and epileptic human brain region reveal that focal cooling can suppress epileptic discharges without affecting the brain’s normal neurological function. Findings suggest a viable treatment for intractable epilepsy cases via an implantable cooling device. However, precise mechanisms by which cooling suppresses epileptic discharges are still not clearly understood. Cooling experiments in vitro presented evidence of reduction in neurotransmitter release from presynaptic terminals and loss of dendritic spines at post-synaptic terminals offering a possible synaptic mechanism. We show that termination of epileptic discharges is possible by introducing a homogeneous temperature factor in a neural mass model which attenuates the post-synaptic impulse responses of the neuronal populations. This result however may be expected since such attenuation leads to reduced post-synaptic potential and when the effect on inhibitory interneurons is less than on excitatory interneurons, frequency of firing of pyramidal cells is consequently reduced. While this is observed in cooling experiments in vitro, experiments in vivo exhibit persistent discharges during cooling but suppressed in magnitude. This leads us to conjecture that reduction in the frequency of discharges may be compensated through intrinsic excitability mechanisms. Such compensatory mechanism is modelled using a reciprocal temperature factor in the firing response function in the neural mass model. We demonstrate that the complete model can reproduce attenuation of both magnitude and frequency of epileptic discharges during cooling. The compensatory mechanism suggests that cooling lowers the average and the variance of the distribution of threshold potential of firing across the population. Bifurcation study with respect to the temperature parameters of the model reveals how heterogeneous response of epileptic discharges to cooling (termination or suppression only) is exhibited. Possibility of differential temperature effects on post-synaptic potential generation of different populations is also explored.

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Section: Discussionsupporting

confidence: 66%

Section: Introductionmentioning

confidence: 99%

Differential temperature sensitivity of synaptic and firing processes in a neural mass model of epileptic discharges explains heterogeneous response of experimental epilepsy to focal brain cooling

et al. 2017

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“…Thus, the use of Peltier device may be more feasible in anesthetized patients during the acute phase of cerebral ischemia in anesthetized patients. The Peltier cooling system has been extensively studied for the treatment of epilepsy and has demonstrated clinical efficacy with an intraoperative application in epilepsy patients (Nomura et al, 2014). Efforts to develop clinically feasible implantable device are continuing (Dinis et al, 2017;Hata et al, 2017), and Peltier's elementbased cooling has been successfully tested in nonhuman primate (Inoue et al, 2017), as a potential clinically therapeutic strategy.…”

Section: Discussionmentioning

confidence: 99%

Targeted Temperature Management: Peltier's Element-Based Focal Brain Cooling Protects Penumbra Neurons from Progressive Damage in Experimental Cerebral Ischemia

Tauchi

Rink

Fujioka

et al. 2018

Therapeutic Hypothermia and Temperature Management

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Targeted temperature management (TTM), or therapeutic hypothermia, is one of the most potent neuroprotective approaches after ischemic and traumatic brain injuries. TTM has been applied clinically with various methods, but effective achievement and maintenance of the target temperature remain challenging. Furthermore, timing of cooling and target body and brain temperature to optimize effectiveness for neuroprotection and to minimize side effects are yet to be standardized. Focal brain cooling is a potential strategy to minimize adverse effects of systemic TTM. In this study, we report on a focal brain cooling device for animals and its effectiveness of focal cooling in several animal models of ischemic cerebral stroke. A focal brain cooling device was constructed using a Peltier's element, a thermoelectric heat pump. The device was validated for its cooling ability, and optimal settings to induce an effective intracranial temperature were determined using male Sprague-Dawley rats. Transient and permanent middle cerebral artery occlusions were experimentally induced, and focal brain cooling was applied using the device varying the timing and duration of cooling. The stroke-induced infarct and edema volumes were evaluated from Nissl-stained cryosections. The focal brain cooling device was able to decrease and subsequently maintained cerebral hypothermia in free-moving rats without altering the core temperature. The device with validated intracranial temperatures produced neuroprotective effects in the acute phase of ischemic neural death, reperfusion injury, progressing damage to the penumbra, and edema formation. In conclusion, our validated focal cooling device enabled rapid and accurate cerebral TTM in rats. Using this device, we were able to test the neuroprotective effect of focal TTM in several pathological stages of cerebral ischemia, which warrants further studies to develop clinically feasible TTM procedures for patients with cerebral stroke.

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“…Its utility and safety to control cortical excitation has been reported both from experimental animal 11,14,15 and human research 10,16 . A common form of CC clinical utilization is topical application of cooled saline during events of epileptiform discharges and seizures during neurosurgeries [17][18][19][20] .…”

Section: Introductionmentioning

confidence: 99%

Focal cortical surface cooling is a novel and safe method for intraoperative functional brain mapping

Ibayashi

Ramirez-Cardenas

Oya

et al. 2020

Preprint

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Objective: Electrical cortical stimulation (ECS) has been the gold standard for intraoperative functional mapping in neurosurgery, yet it carries the risk of induced seizures. Here we assess the safety of focal cortical cooling (CC) as a potential alternative to ECS for functional brain mapping. Methods: We retrospectively reviewed 40 consecutive subjects (n=13 tumor, 27 mesial temporal lobe epilepsy (MTLE) resection) who underwent intraoperative CC during craniotomy at the University of Iowa Hospital and Clinics from 2007 through 2019 (CC group). Thirty-eight of the 40 subjects had ECS performed along with CC during the same procedure. To assess the safety of CC, intra-and post-operative seizure incidence and post-operative neurological deficits were collected together with new post-operative radiographic findings not related to the surgical procedure itself (i.e. non-mapping portions). As a control cohort, we collected 55 consecutive subjects (n=21 MTLE, 34 tumor/vascular pathology) who underwent awake ECS mapping without CC between 2006 and 2019 (ECS-alone group). To evaluate potential long term effects of mapping techniques (CC and/or ECS), we separately collected another 25 consecutive subjects who underwent anterior temporal lobectomy(ATL) without CC nor ECS between 2007 and 2019 (No ECS/No CC-ATL group).Results: A total of 79 brain sites were cooled in the 40 CC subjects, including inferior frontal gyrus (44%), precentral gyrus (39%), postcentral gyrus (6%), subcentral gyrus (4%) and superior temporal gyrus (6%). No intraoperative seizures were reported in the CC group, whereas 3.6% of ECS-alone group had intraoperative seizures. The incidence of seizure(s) within the first postoperative week did not significantly differ amongst CC (7.9%), ECS-alone (9.0%) and No ECS/No CC-ATL groups (12%). There was no significante difference in the incidence of postoperative radiographic change between CC (7.5%) and ECS-alone groups (5.5 %). The long term seizure outcome for MTLE subjects did not statistically differ regarding 'good' outcomes (Engel Ⅰ+Ⅱ):CC group (80%), ECS-alone (83.3%) and No ECS/No CC-ATL group (83.3%). Conclusions:Cortical cooling when used as an intraoperative mapping technique is safe, and may complement traditional electrical cortical stimulation.

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Changes in glutamate concentration, glucose metabolism, and cerebral blood flow during focal brain cooling of the epileptogenic cortex in humans

Cited by 34 publications

References 32 publications

Differential temperature sensitivity of synaptic and firing processes in a neural mass model of epileptic discharges explains heterogeneous response of experimental epilepsy to focal brain cooling

Differential temperature sensitivity of synaptic and firing processes in a neural mass model of epileptic discharges explains heterogeneous response of experimental epilepsy to focal brain cooling

Targeted Temperature Management: Peltier's Element-Based Focal Brain Cooling Protects Penumbra Neurons from Progressive Damage in Experimental Cerebral Ischemia

Focal cortical surface cooling is a novel and safe method for intraoperative functional brain mapping

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