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Thalamic arousal network disturbances in temporal lobe epilepsy and improvement after surgery.
González HFJ, Chakravorti S, Goodale SE, Gupta K, Claassen DO, Dawant B, Morgan VL, Englot DJ
(2019) J Neurol Neurosurg Psychiatry 90: 1109-1116
MeSH Terms: Adult, Arousal, Brain Stem, Case-Control Studies, Epilepsy, Temporal Lobe, Female, Functional Neuroimaging, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Neocortex, Neural Pathways, Neurosurgical Procedures, Thalamic Nuclei, Thalamus
Show Abstract · Added June 22, 2019
OBJECTIVE - The effects of temporal lobe epilepsy (TLE) on subcortical arousal structures remain incompletely understood. Here, we evaluate thalamic arousal network functional connectivity in TLE and examine changes after epilepsy surgery.
METHODS - We examined 26 adult patients with TLE and 26 matched control participants and used resting-state functional MRI (fMRI) to measure functional connectivity between the thalamus (entire thalamus and 19 bilateral thalamic nuclei) and both neocortex and brainstem ascending reticular activating system (ARAS) nuclei. Postoperative imaging was completed for 19 patients >1 year after surgery and compared with preoperative baseline.
RESULTS - Before surgery, patients with TLE demonstrated abnormal thalamo-occipital functional connectivity, losing the normal negative fMRI correlation between the intralaminar central lateral (CL) nucleus and medial occipital lobe seen in controls (p < 0.001, paired t-test). Patients also had abnormal connectivity between ARAS and CL, lower ipsilateral intrathalamic connectivity, and smaller ipsilateral thalamic volume compared with controls (p < 0.05 for each, paired t-tests). Abnormal brainstem-thalamic connectivity was associated with impaired visuospatial attention (ρ = -0.50, p = 0.02, Spearman's rho) while lower intrathalamic connectivity and volume were related to higher frequency of consciousness-sparing seizures (p < 0.02, Spearman's rho). After epilepsy surgery, patients with improved seizures showed partial recovery of thalamo-occipital and brainstem-thalamic connectivity, with values more closely resembling controls (p < 0.01 for each, analysis of variance).
CONCLUSIONS - Overall, patients with TLE demonstrate impaired connectivity in thalamic arousal networks that may be involved in visuospatial attention, but these disturbances may partially recover after successful epilepsy surgery. Thalamic arousal network dysfunction may contribute to morbidity in TLE.
© Author(s) (or their employer(s)) 2019. No commercial re-use. See rights and permissions. Published by BMJ.
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16 MeSH Terms
Brainstem Functional Connectivity Disturbances in Epilepsy may Recover After Successful Surgery.
González HFJ, Goodale SE, Jacobs ML, Haas KF, Landman BA, Morgan VL, Englot DJ
(2020) Neurosurgery 86: 417-428
MeSH Terms: Adult, Brain Stem, Epilepsy, Temporal Lobe, Female, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Nerve Net, Postoperative Period, Recovery of Function
Show Abstract · Added June 22, 2019
BACKGROUND - Focal seizures in temporal lobe epilepsy (TLE) are associated with widespread brain network perturbations and neurocognitive problems.
OBJECTIVE - To determine whether brainstem connectivity disturbances improve with successful epilepsy surgery, as recent work has demonstrated decreased brainstem connectivity in TLE that is related to disease severity and neurocognitive profile.
METHODS - We evaluated 15 adult TLE patients before and after (>1 yr; mean, 3.4 yr) surgery, and 15 matched control subjects using magnetic resonance imaging to measure functional and structural connectivity of ascending reticular activating system (ARAS) structures, including cuneiform/subcuneiform nuclei (CSC), pedunculopontine nucleus (PPN), and ventral tegmental area (VTA).
RESULTS - TLE patients who achieved long-term postoperative seizure freedom (10 of 15) demonstrated increases in functional connectivity between ARAS structures and fronto-parietal-insular neocortex compared to preoperative baseline (P = .01, Kruskal-Wallis), with postoperative connectivity patterns resembling controls' connectivity. No functional connectivity changes were detected in 5 patients with persistent seizures after surgery (P = .9, Kruskal-Wallis). Among seizure-free postoperative patients, larger increases in CSC, PPN, and VTA functional connectivity were observed in individuals with more frequent seizures before surgery (P < .05 for each, Spearman's rho). Larger postoperative increases in PPN functional connectivity were seen in patients with lower baseline verbal IQ (P = .03, Spearman's rho) or verbal memory (P = .04, Mann-Whitney U). No changes in ARAS structural connectivity were detected after successful surgery.
CONCLUSION - ARAS functional connectivity disturbances are present in TLE but may recover after successful epilepsy surgery. Larger increases in postoperative connectivity may be seen in individuals with more severe disease at baseline.
Copyright © 2019 by the Congress of Neurological Surgeons.
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11 MeSH Terms
Relating structural and functional brainstem connectivity to disease measures in epilepsy.
Englot DJ, Gonzalez HFJ, Reynolds BB, Konrad PE, Jacobs ML, Gore JC, Landman BA, Morgan VL
(2018) Neurology 91: e67-e77
MeSH Terms: Adult, Brain Stem, Case-Control Studies, Cognition Disorders, Epilepsy, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Nerve Net, Neuropsychological Tests, Oxygen, Retrospective Studies
Show Abstract · Added September 25, 2018
OBJECTIVE - While epilepsy studies rarely examine brainstem, we sought to examine the hypothesis that temporal lobe epilepsy (TLE) leads to subcortical arousal center dysfunction, contributing to neocortical connectivity and neurocognitive disturbances.
METHODS - In this case-control study of 26 adult patients with TLE and 26 controls, we used MRI to measure structural and functional connectivity of the cuneiform/subcuneiform nuclei (CSC), pedunculopontine nucleus, and ventral tegmental area. Ascending reticular activating system connectivity patterns were related to neuropsychological and disease measures.
RESULTS - Compared to controls, patients with TLE demonstrated reductions in ascending reticular activating system structural and functional connectivity, most prominently to neocortical regions ( < 0.05, unpaired tests, corrected). While reduced CSC structural connectivity was related to impaired performance IQ and visuospatial memory, diminished CSC functional connectivity was associated with impaired verbal IQ and language abilities ( < 0.05, Spearman ρ, tests). Finally, CSC structural connectivity decreases were quantitatively associated with consciousness-impairing seizure frequency ( < 0.05, Spearman ρ) and the presence of generalized seizures ( < 0.05, unpaired test), suggesting a relationship to disease severity.
CONCLUSIONS - Connectivity perturbations in brainstem arousal centers are present in TLE and may contribute to neurocognitive problems. These studies demonstrate the underappreciated role of brainstem networks in epilepsy and may lead to novel neuromodulation targets to treat or prevent deleterious brain network effects of seizures in TLE.
© 2018 American Academy of Neurology.
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15 MeSH Terms
Noise-induced cochlear synaptopathy in rhesus monkeys (Macaca mulatta).
Valero MD, Burton JA, Hauser SN, Hackett TA, Ramachandran R, Liberman MC
(2017) Hear Res 353: 213-223
MeSH Terms: Animals, Auditory Fatigue, Auditory Threshold, Cochlea, Cochlear Diseases, Disease Models, Animal, Evoked Potentials, Auditory, Brain Stem, Hair Cells, Auditory, Hearing, Hearing Loss, Noise-Induced, Macaca mulatta, Noise, Otoacoustic Emissions, Spontaneous, Synapses, Synaptic Transmission, Time Factors
Show Abstract · Added April 3, 2018
Cochlear synaptopathy can result from various insults, including acoustic trauma, aging, ototoxicity, or chronic conductive hearing loss. For example, moderate noise exposure in mice can destroy up to ∼50% of synapses between auditory nerve fibers (ANFs) and inner hair cells (IHCs) without affecting outer hair cells (OHCs) or thresholds, because the synaptopathy occurs first in high-threshold ANFs. However, the fiber loss likely impairs temporal processing and hearing-in-noise, a classic complaint of those with sensorineural hearing loss. Non-human primates appear to be less vulnerable to noise-induced hair-cell loss than rodents, but their susceptibility to synaptopathy has not been studied. Because establishing a non-human primate model may be important in the development of diagnostics and therapeutics, we examined cochlear innervation and the damaging effects of acoustic overexposure in young adult rhesus macaques. Anesthetized animals were exposed bilaterally to narrow-band noise centered at 2 kHz at various sound-pressure levels for 4 h. Cochlear function was assayed for up to 8 weeks following exposure via auditory brainstem responses (ABRs) and otoacoustic emissions (OAEs). A moderate loss of synaptic connections (mean of 12-27% in the basal half of the cochlea) followed temporary threshold shifts (TTS), despite minimal hair-cell loss. A dramatic loss of synapses (mean of 50-75% in the basal half of the cochlea) was seen on IHCs surviving noise exposures that produced permanent threshold shifts (PTS) and widespread hair-cell loss. Higher noise levels were required to produce PTS in macaques compared to rodents, suggesting that primates are less vulnerable to hair-cell loss. However, the phenomenon of noise-induced cochlear synaptopathy in primates is similar to that seen in rodents.
Copyright © 2017 Elsevier B.V. All rights reserved.
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16 MeSH Terms
Functional connectivity disturbances of the ascending reticular activating system in temporal lobe epilepsy.
Englot DJ, D'Haese PF, Konrad PE, Jacobs ML, Gore JC, Abou-Khalil BW, Morgan VL
(2017) J Neurol Neurosurg Psychiatry 88: 925-932
MeSH Terms: Adult, Brain, Brain Mapping, Brain Stem, Case-Control Studies, Cerebral Cortex, Epilepsy, Temporal Lobe, Female, Humans, Limbic System, Magnetic Resonance Imaging, Male, Middle Aged, Neocortex, Neural Inhibition, Neural Pathways, Neurocognitive Disorders, Synaptic Transmission
Show Abstract · Added June 23, 2017
OBJECTIVE - Seizures in temporal lobe epilepsy (TLE) disturb brain networks and lead to connectivity disturbances. We previously hypothesised that recurrent seizures in TLE may lead to abnormal connections involving subcortical activating structures including the ascending reticular activating system (ARAS), contributing to neocortical dysfunction and neurocognitive impairments. However, no studies of ARAS connectivity have been previously reported in patients with epilepsy.
METHODS - We used resting-state functional MRI recordings in 27 patients with TLE (67% right sided) and 27 matched controls to examine functional connectivity (partial correlation) between eight brainstem ARAS structures and 105 cortical/subcortical regions. ARAS nuclei included: cuneiform/subcuneiform, dorsal raphe, locus coeruleus, median raphe, parabrachial complex, pontine oralis, pedunculopontine and ventral tegmental area. Connectivity patterns were related to disease and neuropsychological parameters.
RESULTS - In control subjects, regions showing highest connectivity to ARAS structures included limbic structures, thalamus and certain neocortical areas, which is consistent with prior studies of ARAS projections. Overall, ARAS connectivity was significantly lower in patients with TLE than controls (p<0.05, paired t-test), particularly to neocortical regions including insular, lateral frontal, posterior temporal and opercular cortex. Diminished ARAS connectivity to these regions was related to increased frequency of consciousness-impairing seizures (p<0.01, Pearson's correlation) and was associated with impairments in verbal IQ, attention, executive function, language and visuospatial memory on neuropsychological evaluation (p<0.05, Spearman's rho or Kendell's tau-b).
CONCLUSIONS - Recurrent seizures in TLE are associated with disturbances in ARAS connectivity, which are part of the widespread network dysfunction that may be related to neurocognitive problems in this devastating disorder.
© Article author(s) (or their employer(s) unless otherwise stated in the text of the article) 2017. All rights reserved. No commercial use is permitted unless otherwise expressly granted.
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18 MeSH Terms
Decreased subcortical cholinergic arousal in focal seizures.
Motelow JE, Li W, Zhan Q, Mishra AM, Sachdev RN, Liu G, Gummadavelli A, Zayyad Z, Lee HS, Chu V, Andrews JP, Englot DJ, Herman P, Sanganahalli BG, Hyder F, Blumenfeld H
(2015) Neuron 85: 561-72
MeSH Terms: Animals, Arousal, Brain Stem, Cholinergic Neurons, Female, Magnetic Resonance Imaging, Organ Culture Techniques, Rats, Rats, Sprague-Dawley, Seizures
Show Abstract · Added August 12, 2016
Impaired consciousness in temporal lobe seizures has a major negative impact on quality of life. The prevailing view holds that this disorder impairs consciousness by seizure spread to the bilateral temporal lobes. We propose instead that seizures invade subcortical regions and depress arousal, causing impairment through decreases rather than through increases in activity. Using functional magnetic resonance imaging in a rodent model, we found increased activity in regions known to depress cortical function, including lateral septum and anterior hypothalamus. Importantly, we found suppression of intralaminar thalamic and brainstem arousal systems and suppression of the cortex. At a cellular level, we found reduced firing of identified cholinergic neurons in the brainstem pedunculopontine tegmental nucleus and basal forebrain. Finally, we used enzyme-based amperometry to demonstrate reduced cholinergic neurotransmission in both cortex and thalamus. Decreased subcortical arousal is a critical mechanism for loss of consciousness in focal temporal lobe seizures.
Copyright © 2015 Elsevier Inc. All rights reserved.
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10 MeSH Terms
Neonatal carotid repair at ECMO decannulation: patency rates and early neurologic outcomes.
Duggan EM, Maitre N, Zhai A, Krishnamoorthi H, Voskresensky I, Hardison D, Tice J, Pietsch JB, Lovvorn HN
(2015) J Pediatr Surg 50: 64-8
MeSH Terms: Brain, Carotid Arteries, Evoked Potentials, Auditory, Brain Stem, Extracorporeal Membrane Oxygenation, Female, Heart Defects, Congenital, Humans, Infant, Newborn, Ligation, Male, Postoperative Period, Retrospective Studies, Vascular Patency
Show Abstract · Added October 1, 2015
PURPOSE - Neonates placed on veno-arterial extracorporeal membrane oxygenation (VA-ECMO) undergo either carotid repair or ligation at decannulation. Study aims were to evaluate carotid patency rates after repair and to compare early neurologic outcomes between repaired and ligated patients.
METHODS - A retrospective study of all neonates without congenital heart disease (CHD) who had VA-ECMO between 1989 and 2012 was completed using our institutional ECMO Registry. Carotid patency after repair, neuroimaging studies, and auditory brainstem response (ABR) testing at time of discharge were examined.
RESULTS - 140 neonates were placed on VA-ECMO during the study period. Among survivors, 84% of carotids repaired and imaged remained patent at last study. No significant differences were observed between infants in the repaired and ligated groups regarding diagnosis, ECMO duration, or length of stay. A large proportion (43%) developed a severe brain lesion after VA-ECMO, but few failed their ABR testing. Differences in early neurologic outcomes between the two groups of survivors were not significant.
CONCLUSIONS - At this single institution, carotid patency is excellent following repair at ECMO decannulation. No increased incidence of severe brain lesions or greater neurosensory impairment in the repair group was observed. Further studies are needed to investigate the effects of ligation on longer-term neurocognitive outcomes.
Copyright © 2015 Elsevier Inc. All rights reserved.
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13 MeSH Terms
Brainstem arteriovenous malformations: anatomical subtypes, assessment of "occlusion in situ" technique, and microsurgical results.
Han SJ, Englot DJ, Kim H, Lawton MT
(2015) J Neurosurg 122: 107-17
MeSH Terms: Adolescent, Adult, Aged, Aged, 80 and over, Brain Stem, Cerebral Angiography, Cerebral Revascularization, Child, Child, Preschool, Female, Follow-Up Studies, Humans, Infant, Intracranial Arteriovenous Malformations, Male, Medulla Oblongata, Middle Aged, Pons, Treatment Outcome, Young Adult
Show Abstract · Added August 12, 2016
OBJECT - The surgical management of brainstem arteriovenous malformations (AVMs) might benefit from the definition of anatomical subtypes and refinements of resection techniques. Many brainstem AVMs sit extrinsically on pia mater rather than intrinsically in the parenchyma, allowing treatment by occluding feeding arteries circumferentially, interrupting draining veins after arteriovenous shunting is eliminated, and leaving the obliterated nidus behind. The authors report here the largest series of brainstem AVMs to define 6 subtypes, assess this "occlusion in situ" technique, and analyze the microsurgical results.
METHODS - Brainstem AVMs were categorized as 1 of 6 types: anterior midbrain, posterior midbrain, anterior pontine, lateral pontine, anterior medullary, and lateral medullary AVMs. Data from a prospectively maintained AVM registry were reviewed to evaluate multidisciplinary treatment results.
RESULTS - During a 15-year period, the authors treated 29 patients with brainstem AVMs located in the midbrain (1 anterior and 6 posterior), pons (6 anterior and 7 lateral), and medulla (1 anterior and 8 lateral). The nidus was pial in 26 cases and parenchymal in 3 cases. Twenty-three patients (79%) presented with hemorrhage. Brainstem AVMs were either resected (18 patients, 62%) or occluded in situ (11 patients, 38%). All lateral pontine AVMs were resected, and the occlusion in situ rate was highest with anterior pontine AVMs (83%). Angiography confirmed complete obliteration in 26 patients (89.6%). The surgical mortality rate was 6.9%, and the rate of permanent neurological deterioration was 13.8%. At follow-up (mean 1.3 years), good outcomes (modified Rankin Scale [mRS] score ≤ 2) were observed in 18 patients (66.7%) and poor outcomes (mRS score of 3-5) were observed in 9 patients (33.3%). The mRS scores in 21 patients (77.8%) were unchanged or improved. The best outcomes were observed with lateral pontine (100%) and lateral medullary (75%) AVMs, and the rate of worsening/death was greatest with posterior midbrain and anterior pontine AVMs (50% each).
CONCLUSIONS - Brainstem AVMs can be differentiated by their location in the brainstem (midbrain, pons, or medulla) and the surface on which they are based (anterior, posterior, or lateral). Anatomical subtypes can help the neurosurgeon determine how to advise patients, with lateral subtypes being a favorable surgical indication along with extrinsic pial location and hemorrhagic presentation. Most AVMs are dissected with the intention to resect them, and occlusion in situ is reserved for those AVMs that do not separate cleanly from the brainstem, that penetrate into the parenchyma, or are more anterior in location, where it is difficult to visualize and preserve perforating arteries (anterior pontine and lateral medullary AVMs). Although surgical morbidity is considerable, surgery results in a better obliteration rate than nonoperative management and is indicated in highly selected patients with high rerupture risks.
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20 MeSH Terms
Long-term change in ventricular size following endoscopic third ventriculostomy for hydrocephalus due to tectal plate gliomas.
Romeo A, Naftel RP, Griessenauer CJ, Reed GT, Martin R, Shannon CN, Grabb PA, Tubbs RS, Wellons JC
(2013) J Neurosurg Pediatr 11: 20-5
MeSH Terms: Adolescent, Anesthesia, General, Brain Stem Neoplasms, Cerebral Ventricles, Child, Child, Preschool, Endoscopy, Female, Follow-Up Studies, Glioma, Humans, Hydrocephalus, Intracranial Hypertension, Male, Postoperative Complications, Radiography, Reoperation, Retrospective Studies, Treatment Failure, Treatment Outcome, Ventriculostomy
Show Abstract · Added March 20, 2014
OBJECT - Endoscopic third ventriculostomy (ETV) is an alternative to shunt placement in children with hydrocephalus due to tectal plate gliomas (TPGs). However, controversy remains regarding the amount of ventricular size reduction that should be expected after ETV. This study investigates ventricular size change after ETV for TPGs.
METHODS - Twenty-two children were identified from a 15-year retrospective database of neuroendoscopic procedures performed at the authors' institution, Children's Hospital of Alabama, in patients with a minimum of 1 year of follow-up. Clinical outcomes, including the need for further CSF diversion and symptom resolution, were recorded. The frontal and occipital horn ratio (FOR) was measured on pre- and postoperative, 1-year, and last follow-up imaging studies.
RESULTS - In 17 (77%) of 22 children no additional procedure for CSF diversion was required. Of those in whom CSF diversion failed, 4 underwent successful repeat ETV and 1 required shunt replacement. Therefore, in 21 (96%) of 22 patients, CSF diversion was accomplished with ETV. Preoperative and postoperative imaging was available for 18 (82%) of 22 patients. The FOR decreased in 89% of children who underwent ETV. The FOR progressively decreased 1.7%, 11.2%, and 12.7% on the initial postoperative, 1-year, and last follow-up images, respectively. The mean radiological follow-up duration for 18 patients was 5.4 years. When ETV failed, the FOR increased at the time of failure in all patients. Failure occurred 1.6 years after initial ETV on average. The mean clinical follow-up period for all 22 patients was 5.3 years. In all cases clinical improvement was demonstrated at the last follow-up.
CONCLUSIONS - Endoscopic third ventriculostomy successfully treated hydrocephalus in the extended follow-up period of patients with TPGs. The most significant reduction in ventricular size was observed at the the 1-year followup, with only modest reduction thereafter.
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21 MeSH Terms
Recurring episodes of Bell's mania after cerebrovascular accident.
Bobo WV, Murphy MJ, Heckers SH
(2009) Psychosomatics 50: 285-8
MeSH Terms: Anti-Anxiety Agents, Bipolar Disorder, Brain Stem Infarctions, Catatonia, Cerebellum, Delirium, Diagnosis, Differential, Dose-Response Relationship, Drug, Female, Humans, Lorazepam, Middle Aged, Pons, Recurrence
Show Abstract · Added February 12, 2015
BACKGROUND - Bell's mania (mania with delirium) is an acute neurobehavioral syndrome of unknown etiology that is characterized by the rapid onset of grandiosity, psychomotor excitement, emotional lability, psychosis, and sleep disruption consistent with mania, coupled with alterations in sensorium, and disorientation characteristic of delirium. Catatonia is a common feature of the syndrome.
METHOD - The authors describe a case of recurrent delirium/mania with prominent catatonic features after a cerebellar and pontine stroke, and subsequent successful treatment with lorazepam.
RESULTS - Symptoms quickly resolved after antipsychotics were discontinued, with continuation of valproate and lorazepam treatment.
DISCUSSION - Failure to recognize this patient's syndrome as a form of catatonia could have had severe, even life-threatening, consequences. The use of neuroleptic medications in cases of delirium/mania with catatonic signs may result in marked clinical deterioration, whereas high-dose lorazepam can ameliorate catatonic signs.
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14 MeSH Terms