Functional Magnetic Resonance Imaging Networks Induced by Intracranial Stimulation May Help Defining the Epileptogenic Zone

Jones, Stephen E.; Zhang, Myron; Avitsian, Rafi; Bhattacharyya, Pallab K.; Bulacio, Juan; Cendes, Fernando; Enatsu, Rei; Lowe, Mark J.; Najm, Imad; Nair, Dileep; Phillips, Michael; González-Martínez, Jorge

doi:10.1089/brain.2014.0225

Cited by 24 publications

(22 citation statements)

References 36 publications

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“…This work falls in line with multiple other recent publications elaborating on either neuroimaging or electrophysiological representations of focal epilepsy as a network disease resulting from dysfunctional electrical connections across distinct brain regions, sometimes with a clear imaging correlate (atrophy of various hypothetically "connected" brain regions (1-3) or abnormal functional connectivity measures [4]) and sometimes supported by abnormal electrical connectivity patterns (5). The strengths of such a thought process are many.…”

Section: Commentarysupporting

confidence: 86%

Outcomes of Epilepsy Surgery for Epileptic Networks

Jehi¹

2017

Epilepsy Curr

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CommentaryResective brain surgery to treat drug-resistant focal epilepsy is a major endeavor. Patients, family members, neurologists, neuroradiologists, neuropsychologists, neurosurgeons, and psychiatrists invest significant time and resources to localize the epilepsy and develop a safe and rational surgical strategy. The typical presurgical workup is usually extremely thorough with multiple electroencephalographic recordings, several sophisticated neuroimaging studies, and sometimes risky intracranial evaluations. Yet, the final critical step of determining the "epileptogenic zone" (EZ), that is, the "area of cortex that is necessary and sufficient for initiating seizures and whose removal (or disconnection) is necessary for complete abolition of seizures, " remains essentially a subjective assessment, relying heavily on the healthcare provider's interpretation of fairly complex presurgical data points. Efforts attempting to infuse more objectivity into the definition of the EZ, such as the article highlighted in this commentary, are highly welcome.In this study, Sinha et al. report on dynamical computational models, informed with patient EEG data, that can "estimate" the extent of epileptogenicity in distinct brain regions and thus predict seizure outcome after epilepsy surgery should these regions be removed. This work falls in line with multiple other recent publications elaborating on either neuroimaging or electrophysiological representations of focal epilepsy as a network disease resulting from dysfunctional electrical connections across distinct brain regions, sometimes with a clear imaging correlate (atrophy of various hypothetically "connected" brain regions (1-3) or abnormal functional connectivity measures [4]) and sometimes supported by abnormal electrical connectivity patterns (5). The strengths of such a thought process are many. First, epilepsy surgery is conceptualized as a treatment aiming to remove a critical node in an epileptic network rather than an extraction of a limited epileptic focus. The mere appreciation of epilepsy as resulting from multiple connected brain regions, all with a potential for triggering seizures, albeit to varying degrees, facilitates the understanding of surgical failure as sometimes resulting from an incomplete disruption of this epileptic network rather than from mislocalization of the epileptic focus. Second, work attempting to let the data speak for itself through computational modeling Surgery can be a last resort for patients with intractable, medically refractory epilepsy. For many of these patients, however, there is substantial risk that the surgery will be ineffective. The prediction of who is likely to benefit from a surgical approach is crucial for being able to inform patients better, conduct principled prospective clinical trials, and ultimately tailor therapeutic approaches to these patients more effectively. Dynamical computational models, informed with patient data, can be used to make predictions and give mechanistic insight. In this study, we devel...

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Section: Commentarysupporting

confidence: 86%

Outcomes of Epilepsy Surgery for Epileptic Networks

Jehi¹

2017

Epilepsy Curr

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“…Our method has obvious clinical value within patients with epilepsy (as indeed confirmed in the studies by Jones et al, 2014a and b), but the very nature of the epilepsy raises the concern that findings about brain connectivity in this population may not generalize to healthy individuals. We suggest two approaches to this issue.…”

Section: Discussionmentioning

confidence: 56%

“…Nonetheless, it is possible to pass current through the electrodes, and to combine such stimulation with fMRI, first demonstrated at the Cleveland Clinic (Jones et al, 2014a; Jones et al, 2014b). In that study, the clinical purpose of es-fMRI was to stimulate the putative epileptogenic zone and use fMRI as a measure of increased excitability of pathological tissue.…”

Section: Discussionmentioning

confidence: 99%

Mapping effective connectivity in the human brain with concurrent intracranial electrical stimulation and BOLD-fMRI

Oya

Howard

Magnotta

et al. 2017

Journal of Neuroscience Methods

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Background Understanding brain function requires knowledge of how one brain region causally influences another. This information is difficult to obtain directly in the human brain, and is instead typically inferred from resting-state fMRI. New method Here, we demonstrate the safety and scientific promise of a novel and complementary approach: concurrent electrical stimulation and fMRI (es-fMRI) at 3 Tesla in awake neurosurgical patients with implanted depth electrodes. Results We document the results of safety testing, actual experimental setup, and stimulation parameters, that safely and reliably evoke activation in distal structures through stimulation of amygdala, cingulate, or prefrontal cortex. We compare connectivity inferred from the evoked patterns of activation with that estimated from standard resting-state fMRI in the same patients: while connectivity patterns obtained with each approach are correlated, each method produces unique results. Response patterns were stable over the course of 11 minutes of es-fMRI runs. Comparison with existing method es-fMRI in awake humans yields unique information about effective connectivity, complementing resting-state fMRI. Although our stimulations were below the level of inducing any apparent behavioral or perceptual effects, a next step would be to use es-fMRI to modulate task performances. This would reveal the acute network-level changes induced by the stimulation that mediate the behavioral and cognitive effects seen with brain stimulation. Conclusions es-fMRI provides a novel and safe approach for mapping effective connectivity in the human brain in a clinical setting, and will inform treatments for psychiatric and neurodegenerative disorders that use deep brain stimulation.

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“…We harnessed a new approach for similarly assessing effective connectivity in humans and monkeys, using combined electrical stimulation and functional MRI (esfMRI) 26,35 . We found comparable fronto-temporal effective connectivity in both species from stimulating auditory cortex in several vlPFC and MTL subregions.…”

Section: Discussionmentioning

confidence: 99%

Common Fronto-temporal Effective Connectivity in Humans and Monkeys

Rocchi

Oya

Balezeau

et al. 2020

Preprint

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Highlights 22 • Privileged human auditory to inferior frontal connectivity, linked to monkeys 23 • Common auditory to parahippocampal effective connectivity in both species 24 • Greater lateralization in human effective connectivity, more symmetrical in monkeys 25 • Human fronto-temporal network function rooted in evolutionarily conserved signature 26 27 eTOC short summary 28 Functional connectivity between regions crucial for language and declarative memory is thought to 29 have substantially differentiated in humans. Using a new technique to similarly visualize directional 30 effective connectivity in humans and monkeys, we found remarkably comparable connectivity patterns 31 in both species between fronto-temporal regions crucial for cognition. 32 33 ABSTRACT 36 Cognitive pathways supporting human language and declarative memory are thought to have uniquely 37 evolutionarily differentiated in our species. However, cross-species comparisons are missing on site-38 specific effective connectivity between regions important for cognition. We harnessed a new approach 39 using functional imaging to visualize the impact of direct electrical brain stimulation in human 40 neurosurgery patients. Applying the same approach with macaque monkeys, we found remarkably 41 comparable patterns of effective connectivity between auditory cortex and ventro-lateral prefrontal 42 cortex (vlPFC) and parahippocampal cortex in both species. Moreover, in humans electrical 43 tractography revealed rapid evoked potentials in vlPFC from stimulating auditory cortex and speech 44 sounds drove vlPFC, consistent with prior evidence in monkeys of direct projections from auditory 45 cortex to vocalization responsive regions in vlPFC. The results identify a common effective 46 connectivity signature that from auditory cortex is equally direct to vlPFC and indirect to the homology, convergence or divergence, can be of substantial theoretical significance: Within the motor 52 domain, human and nonhuman primates have direct cortico-spinal projections subserving fine 53 movement control that are indirect in rodents 1 . Also, human laryngeal motor cortex projects directly to 54 a brain stem nucleus (ambiguus) controlling laryngeal muscles 2 . Such projections for vocal production 55 are more indirect in nonhuman primates 3 and rodents 4 , shedding light on human speech evolution 5 . 56 Language defines us as a species and because of its prominent role in declarative memory 57 substantial evolutionary differentiation of human cognitive pathways is expected. Comparative studies 58 often see considerable levels of evolutionary conservation alongside insights on species-specific 59 differences 6-12 . Yet, certain cross-species comparisons are missing, such as on the impact of directed 60 effective connectivity with the required precision of site-specific perturbation that can be applied to 61 both human and nonhuman primates. Thereby, the question on the extent of differentiation versus 62 conservation in primate fronto-temporal systems-although crucial fo...

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Functional Magnetic Resonance Imaging Networks Induced by Intracranial Stimulation May Help Defining the Epileptogenic Zone

Cited by 24 publications

References 36 publications

Outcomes of Epilepsy Surgery for Epileptic Networks

Outcomes of Epilepsy Surgery for Epileptic Networks

Mapping effective connectivity in the human brain with concurrent intracranial electrical stimulation and BOLD-fMRI

Common Fronto-temporal Effective Connectivity in Humans and Monkeys

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