Skip to main content
Top
Published in: Current Neurology and Neuroscience Reports 6/2016

Open Access 01-06-2016 | Neuroimaging (DJ Brooks, Section Editor)

Advances of Molecular Imaging in Epilepsy

Authors: Marian Galovic, Matthias Koepp

Published in: Current Neurology and Neuroscience Reports | Issue 6/2016

Login to get access

Abstract

Positron emission tomography (PET) is a neuroimaging method that offers insights into the molecular functioning of a human brain. It has been widely used to study metabolic and neurotransmitter abnormalities in people with epilepsy. This article reviews the development of several PET radioligands and their application in studying the molecular mechanisms of epilepsy. Over the last decade, tracers binding to serotonin and γ-aminobutyric acid (GABA) receptors have been used to delineate the location of the epileptic focus. PET studies have examined the role of opioids, cannabinoids, acetylcholine, and dopamine in modulating neuronal hyperexcitability and seizure termination. In vivo analyses of drug transporters, e.g., P-glycoprotein, have increased our understanding of pharmacoresistance that could inform new therapeutic strategies. Finally, PET experiments targeting neuroinflammation and glutamate receptors might guide the development of novel biomarkers of epileptogenesis.
Literature
1.
go back to reference Phelps ME, Huang SC, Hoffman EJ, Selin C, Sokoloff L, Kuhl DE. Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: validation of method. Ann Neurol. 1979;6:371–88.CrossRefPubMed Phelps ME, Huang SC, Hoffman EJ, Selin C, Sokoloff L, Kuhl DE. Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: validation of method. Ann Neurol. 1979;6:371–88.CrossRefPubMed
2.
go back to reference Kuhl DE, Engel J, Phelps ME, Selin C. Epileptic patterns of local cerebral metabolism and perfusion in humans determined by emission computed tomography of 18FDG and 13NH3. Ann Neurol. 1980;8:348–60.CrossRefPubMed Kuhl DE, Engel J, Phelps ME, Selin C. Epileptic patterns of local cerebral metabolism and perfusion in humans determined by emission computed tomography of 18FDG and 13NH3. Ann Neurol. 1980;8:348–60.CrossRefPubMed
3.
go back to reference la Fougère C, Rominger A, Förster S, Geisler J, Bartenstein P. PET and SPECT in epilepsy: a critical review. Epilepsy Behav. 2009;15:50–5.CrossRefPubMed la Fougère C, Rominger A, Förster S, Geisler J, Bartenstein P. PET and SPECT in epilepsy: a critical review. Epilepsy Behav. 2009;15:50–5.CrossRefPubMed
4.
go back to reference Laufs H, Richardson MP, Salek-Haddadi A, Vollmar C, Duncan JS, Gale K, et al. Converging PET and fMRI evidence for a common area involved in human focal epilepsies. Neurology. 2011;77:904–10.CrossRefPubMedPubMedCentral Laufs H, Richardson MP, Salek-Haddadi A, Vollmar C, Duncan JS, Gale K, et al. Converging PET and fMRI evidence for a common area involved in human focal epilepsies. Neurology. 2011;77:904–10.CrossRefPubMedPubMedCentral
5.
go back to reference Centeno M, Vollmar C, Stretton J, Symms MR, Thompson PJ, Richardson MP, et al. Structural changes in the temporal lobe and piriform cortex in frontal lobe epilepsy. Epilepsy Res. 2014;108:978–81.CrossRefPubMedPubMedCentral Centeno M, Vollmar C, Stretton J, Symms MR, Thompson PJ, Richardson MP, et al. Structural changes in the temporal lobe and piriform cortex in frontal lobe epilepsy. Epilepsy Res. 2014;108:978–81.CrossRefPubMedPubMedCentral
6.
go back to reference Piredda S, Gale K. A crucial epileptogenic site in the deep prepiriform cortex. Nature. 1985;317:623–5.CrossRefPubMed Piredda S, Gale K. A crucial epileptogenic site in the deep prepiriform cortex. Nature. 1985;317:623–5.CrossRefPubMed
7.
go back to reference Vivash L, Gregoire M-C, Lau EW, Ware RE, Binns D, Roselt P, et al. 18F-flumazenil: a γ-aminobutyric acid A-specific PET radiotracer for the localization of drug-resistant temporal lobe epilepsy. J Nucl Med. 2013;54:1270–7.CrossRefPubMed Vivash L, Gregoire M-C, Lau EW, Ware RE, Binns D, Roselt P, et al. 18F-flumazenil: a γ-aminobutyric acid A-specific PET radiotracer for the localization of drug-resistant temporal lobe epilepsy. J Nucl Med. 2013;54:1270–7.CrossRefPubMed
8.
go back to reference During MJ, Spencer DD. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet. 1993;341:1607–10.CrossRefPubMed During MJ, Spencer DD. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet. 1993;341:1607–10.CrossRefPubMed
9.
go back to reference Yeh GC, Bonhaus DW, Nadler JV, McNamara JO. N-methyl-D-aspartate receptor plasticity in kindling: quantitative and qualitative alterations in the N-methyl-D-aspartate receptor-channel complex. Proc Natl Acad Sci U S A. 1989;86:8157–60.CrossRefPubMedPubMedCentral Yeh GC, Bonhaus DW, Nadler JV, McNamara JO. N-methyl-D-aspartate receptor plasticity in kindling: quantitative and qualitative alterations in the N-methyl-D-aspartate receptor-channel complex. Proc Natl Acad Sci U S A. 1989;86:8157–60.CrossRefPubMedPubMedCentral
10.
go back to reference Stasheff SF, Anderson WW, Clark S, Wilson WA. NMDA antagonists differentiate epileptogenesis from seizure expression in an in vitro model. Science. 1989;245:648–51.CrossRefPubMed Stasheff SF, Anderson WW, Clark S, Wilson WA. NMDA antagonists differentiate epileptogenesis from seizure expression in an in vitro model. Science. 1989;245:648–51.CrossRefPubMed
11.
go back to reference Kumlien E, Hartvig P, Valind S, Oye I, Tedroff J, Långström B. NMDA-receptor activity visualized with (S)-[N-methyl-11C]ketamine and positron emission tomography in patients with medial temporal lobe epilepsy. Epilepsia. 1999;40:30–7.CrossRefPubMed Kumlien E, Hartvig P, Valind S, Oye I, Tedroff J, Långström B. NMDA-receptor activity visualized with (S)-[N-methyl-11C]ketamine and positron emission tomography in patients with medial temporal lobe epilepsy. Epilepsia. 1999;40:30–7.CrossRefPubMed
12.
go back to reference McGinnity CJ, Hammers A, Riaño Barros DA, Luthra SK, Jones PA, Trigg W, et al. Initial evaluation of 18F-GE-179, a putative PET Tracer for activated N-methyl D-aspartate receptors. J Nucl Med. 2014;55:423–30.CrossRefPubMed McGinnity CJ, Hammers A, Riaño Barros DA, Luthra SK, Jones PA, Trigg W, et al. Initial evaluation of 18F-GE-179, a putative PET Tracer for activated N-methyl D-aspartate receptors. J Nucl Med. 2014;55:423–30.CrossRefPubMed
13.••
go back to reference McGinnity CJ, Koepp MJ, Hammers A, Riaño Barros DA, Pressler RM, Luthra S, et al. NMDA receptor binding in focal epilepsies. J Neurol Neurosurg Psychiatr. 2015;86:1150–7. This is the first study to demonstrate a global increase of NMDA receptor activation in epilepsy patients. Interestingly, those on antidepressants had a markedly lower NMDA receptor binding.CrossRefPubMedPubMedCentral McGinnity CJ, Koepp MJ, Hammers A, Riaño Barros DA, Pressler RM, Luthra S, et al. NMDA receptor binding in focal epilepsies. J Neurol Neurosurg Psychiatr. 2015;86:1150–7. This is the first study to demonstrate a global increase of NMDA receptor activation in epilepsy patients. Interestingly, those on antidepressants had a markedly lower NMDA receptor binding.CrossRefPubMedPubMedCentral
14.
go back to reference Feldmann M, Koepp M. P-glycoprotein imaging in temporal lobe epilepsy: in vivo PET experiments with the Pgp substrate [11C]-verapamil. Epilepsia. 2012;53 Suppl 6:60–3.CrossRefPubMed Feldmann M, Koepp M. P-glycoprotein imaging in temporal lobe epilepsy: in vivo PET experiments with the Pgp substrate [11C]-verapamil. Epilepsia. 2012;53 Suppl 6:60–3.CrossRefPubMed
15.
go back to reference Siddiqui A, Kerb R, Weale ME, Brinkmann U, Smith A, Goldstein DB, et al. Association of multidrug resistance in epilepsy with a polymorphism in the drug-transporter gene ABCB1. N Engl J Med. 2003;348:1442–8.CrossRefPubMed Siddiqui A, Kerb R, Weale ME, Brinkmann U, Smith A, Goldstein DB, et al. Association of multidrug resistance in epilepsy with a polymorphism in the drug-transporter gene ABCB1. N Engl J Med. 2003;348:1442–8.CrossRefPubMed
16.
go back to reference Volk HA, Burkhardt K, Potschka H, Chen J, Becker A, Loscher W. Neuronal expression of the drug efflux transporter P-glycoprotein in the rat hippocampus after limbic seizures. Neuroscience. 2004;123:751–9.CrossRefPubMed Volk HA, Burkhardt K, Potschka H, Chen J, Becker A, Loscher W. Neuronal expression of the drug efflux transporter P-glycoprotein in the rat hippocampus after limbic seizures. Neuroscience. 2004;123:751–9.CrossRefPubMed
17.
go back to reference Sisodiya SM, Lin W-R, Harding BN, Squier MV, Thom M. Drug resistance in epilepsy: expression of drug resistance proteins in common causes of refractory epilepsy. Brain. 2002;125:22–31.CrossRefPubMed Sisodiya SM, Lin W-R, Harding BN, Squier MV, Thom M. Drug resistance in epilepsy: expression of drug resistance proteins in common causes of refractory epilepsy. Brain. 2002;125:22–31.CrossRefPubMed
18.
go back to reference Eyal S, Ke B, Muzi M, Link JM, Mankoff DA, Collier AC, et al. Regional P-glycoprotein activity and inhibition at the human blood–brain barrier as imaged by positron emission tomography. Clin Pharmacol Ther. 2010;87:579–85.CrossRefPubMedPubMedCentral Eyal S, Ke B, Muzi M, Link JM, Mankoff DA, Collier AC, et al. Regional P-glycoprotein activity and inhibition at the human blood–brain barrier as imaged by positron emission tomography. Clin Pharmacol Ther. 2010;87:579–85.CrossRefPubMedPubMedCentral
19.
go back to reference Wagner CC, Bauer M, Karch R, Feurstein T, Kopp S, Chiba P, et al. A pilot study to assess the efficacy of tariquidar to inhibit P-glycoprotein at the human blood–brain barrier with (R)-11C-verapamil and PET. J Nucl Med. 2009;50:1954–61.CrossRefPubMedPubMedCentral Wagner CC, Bauer M, Karch R, Feurstein T, Kopp S, Chiba P, et al. A pilot study to assess the efficacy of tariquidar to inhibit P-glycoprotein at the human blood–brain barrier with (R)-11C-verapamil and PET. J Nucl Med. 2009;50:1954–61.CrossRefPubMedPubMedCentral
20.
go back to reference Langer O, Bauer M, Hammers A, Karch R, Pataraia E, Koepp MJ, et al. Pharmacoresistance in epilepsy: a pilot PET study with the P-glycoprotein substrate R-[(11)C]verapamil. Epilepsia. 2007;48:1774–84.CrossRefPubMed Langer O, Bauer M, Hammers A, Karch R, Pataraia E, Koepp MJ, et al. Pharmacoresistance in epilepsy: a pilot PET study with the P-glycoprotein substrate R-[(11)C]verapamil. Epilepsia. 2007;48:1774–84.CrossRefPubMed
21.••
go back to reference Feldmann M, Asselin M-C, Liu J, Wang S, McMahon A, Anton-Rodriguez J, et al. P-glycoprotein expression and function in patients with temporal lobe epilepsy: a case–control study. Lancet Neurol. 2013;12:777–85. Feldman et al. demonstrated increased activity of the drug transporter P-glycoprotein in pharmacoresistant epilepsy patients. This could contribute to multidrug resistance by reducing the intracellular concentration of antiepileptic drugs.CrossRefPubMed Feldmann M, Asselin M-C, Liu J, Wang S, McMahon A, Anton-Rodriguez J, et al. P-glycoprotein expression and function in patients with temporal lobe epilepsy: a case–control study. Lancet Neurol. 2013;12:777–85. Feldman et al. demonstrated increased activity of the drug transporter P-glycoprotein in pharmacoresistant epilepsy patients. This could contribute to multidrug resistance by reducing the intracellular concentration of antiepileptic drugs.CrossRefPubMed
22.
go back to reference Shin JW, Chu K, Shin SA, Jung KH, Lee ST, Lee YS, et al. Clinical applications of simultaneous PET/MR imaging using (R)-[11C]-verapamil with cyclosporine A: preliminary results on a surrogate marker of drug-resistant epilepsy. AJNR Am J Neuroradiol. 2015. Shin JW, Chu K, Shin SA, Jung KH, Lee ST, Lee YS, et al. Clinical applications of simultaneous PET/MR imaging using (R)-[11C]-verapamil with cyclosporine A: preliminary results on a surrogate marker of drug-resistant epilepsy. AJNR Am J Neuroradiol. 2015.
23.
go back to reference Bauer M, Karch R, Zeitlinger M, Liu J, Koepp MJ, Asselin M-C, et al. In vivo P-glycoprotein function before and after epilepsy surgery. Neurology. 2014;83:1326–31.CrossRefPubMedPubMedCentral Bauer M, Karch R, Zeitlinger M, Liu J, Koepp MJ, Asselin M-C, et al. In vivo P-glycoprotein function before and after epilepsy surgery. Neurology. 2014;83:1326–31.CrossRefPubMedPubMedCentral
25.
go back to reference Seneca N, Zoghbi SS, Liow J-S, Kreisl W, Herscovitch P, Jenko K, et al. Human brain imaging and radiation dosimetry of 11C-N-desmethyl-loperamide, a PET radiotracer to measure the function of P-glycoprotein. J Nucl Med. 2009;50:807–13. Seneca N, Zoghbi SS, Liow J-S, Kreisl W, Herscovitch P, Jenko K, et al. Human brain imaging and radiation dosimetry of 11C-N-desmethyl-loperamide, a PET radiotracer to measure the function of P-glycoprotein. J Nucl Med. 2009;50:807–13.
26.
go back to reference Amhaoul H, Hamaide J, Bertoglio D, Reichel SN, Verhaeghe J, Geerts E, et al. Brain inflammation in a chronic epilepsy model: evolving pattern of the translocator protein during epileptogenesis. Neurobiol Dis. 2015;82:526–39.CrossRefPubMed Amhaoul H, Hamaide J, Bertoglio D, Reichel SN, Verhaeghe J, Geerts E, et al. Brain inflammation in a chronic epilepsy model: evolving pattern of the translocator protein during epileptogenesis. Neurobiol Dis. 2015;82:526–39.CrossRefPubMed
27.
go back to reference Das A, Wallace GC, Holmes C, McDowell ML, Smith JA, Marshall JD, et al. Hippocampal tissue of patients with refractory temporal lobe epilepsy is associated with astrocyte activation, inflammation, and altered expression of channels and receptors. Neuroscience. 2012;220:237–46.CrossRefPubMedPubMedCentral Das A, Wallace GC, Holmes C, McDowell ML, Smith JA, Marshall JD, et al. Hippocampal tissue of patients with refractory temporal lobe epilepsy is associated with astrocyte activation, inflammation, and altered expression of channels and receptors. Neuroscience. 2012;220:237–46.CrossRefPubMedPubMedCentral
28.
go back to reference Dedeurwaerdere S, Callaghan PD, Pham T, Rahardjo GL, Amhaoul H, Berghofer P, et al. PET imaging of brain inflammation during early epileptogenesis in a rat model of temporal lobe epilepsy. EJNMMI Res. 2012;2:60.CrossRefPubMedPubMedCentral Dedeurwaerdere S, Callaghan PD, Pham T, Rahardjo GL, Amhaoul H, Berghofer P, et al. PET imaging of brain inflammation during early epileptogenesis in a rat model of temporal lobe epilepsy. EJNMMI Res. 2012;2:60.CrossRefPubMedPubMedCentral
29.
go back to reference Kim J-E, Choi H-C, Song H-K, Jo S-M, Kim D-S, Choi S-Y, et al. Levetiracetam inhibits interleukin-1 beta inflammatory responses in the hippocampus and piriform cortex of epileptic rats. Neurosci Lett. 2010;471:94–9.CrossRefPubMed Kim J-E, Choi H-C, Song H-K, Jo S-M, Kim D-S, Choi S-Y, et al. Levetiracetam inhibits interleukin-1 beta inflammatory responses in the hippocampus and piriform cortex of epileptic rats. Neurosci Lett. 2010;471:94–9.CrossRefPubMed
30.
go back to reference Amhaoul H, Staelens S, Dedeurwaerdere S. Imaging brain inflammation in epilepsy. Neuroscience. 2014;279:238–52.CrossRefPubMed Amhaoul H, Staelens S, Dedeurwaerdere S. Imaging brain inflammation in epilepsy. Neuroscience. 2014;279:238–52.CrossRefPubMed
31.
go back to reference Ory D, Planas A, Dresselaers T, Gsell W, Postnov A, Celen S, et al. PET imaging of TSPO in a rat model of local neuroinflammation induced by intracerebral injection of lipopolysaccharide. Nucl Med Biol. 2015;42:753–61.CrossRefPubMed Ory D, Planas A, Dresselaers T, Gsell W, Postnov A, Celen S, et al. PET imaging of TSPO in a rat model of local neuroinflammation induced by intracerebral injection of lipopolysaccharide. Nucl Med Biol. 2015;42:753–61.CrossRefPubMed
32.
go back to reference Sandiego CM, Gallezot J-D, Pittman B, Nabulsi N, Lim K, Lin S-F, et al. Imaging robust microglial activation after lipopolysaccharide administration in humans with PET. Proc Natl Acad Sci U S A. 2015;112:12468–73.CrossRefPubMedPubMedCentral Sandiego CM, Gallezot J-D, Pittman B, Nabulsi N, Lim K, Lin S-F, et al. Imaging robust microglial activation after lipopolysaccharide administration in humans with PET. Proc Natl Acad Sci U S A. 2015;112:12468–73.CrossRefPubMedPubMedCentral
33.
go back to reference Banati RB, Goerres GW, Myers R, Gunn RN, Turkheimer FE, Kreutzberg GW, et al. [11C](R)-PK11195 positron emission tomography imaging of activated microglia in vivo in Rasmussen's encephalitis. Neurology. 1999;53:2199–203.CrossRefPubMed Banati RB, Goerres GW, Myers R, Gunn RN, Turkheimer FE, Kreutzberg GW, et al. [11C](R)-PK11195 positron emission tomography imaging of activated microglia in vivo in Rasmussen's encephalitis. Neurology. 1999;53:2199–203.CrossRefPubMed
34.
go back to reference Kumar A, Chugani HT, Luat A, Asano E, Sood S. Epilepsy surgery in a case of encephalitis: use of 11C-PK11195 positron emission tomography. Pediatr Neurol. 2008;38:439–42.CrossRefPubMed Kumar A, Chugani HT, Luat A, Asano E, Sood S. Epilepsy surgery in a case of encephalitis: use of 11C-PK11195 positron emission tomography. Pediatr Neurol. 2008;38:439–42.CrossRefPubMed
35.
go back to reference Goerres GW, Revesz T, Duncan J, Banati RB. Imaging cerebral vasculitis in refractory epilepsy using [(11)C](R)-PK11195 positron emission tomography. AJR Am J Roentgenol. 2001;176:1016–8.CrossRefPubMed Goerres GW, Revesz T, Duncan J, Banati RB. Imaging cerebral vasculitis in refractory epilepsy using [(11)C](R)-PK11195 positron emission tomography. AJR Am J Roentgenol. 2001;176:1016–8.CrossRefPubMed
36.••
go back to reference Gershen LD, Zanotti-Fregonara P, Dustin IH, Liow JS, Hirvonen J, Kreisl WC, et al. Neuroinflammation in temporal lobe epilepsy measured using positron emission tomographic imaging of translocator protein. JAMA Neurol. 2015;72:882–8. Gershen et al. showed increased TSPO activity in the temporal lobes of epilepsy patients. This supports the role of neuroinflammation in epilepsy and epileptogenesis.CrossRefPubMed Gershen LD, Zanotti-Fregonara P, Dustin IH, Liow JS, Hirvonen J, Kreisl WC, et al. Neuroinflammation in temporal lobe epilepsy measured using positron emission tomographic imaging of translocator protein. JAMA Neurol. 2015;72:882–8. Gershen et al. showed increased TSPO activity in the temporal lobes of epilepsy patients. This supports the role of neuroinflammation in epilepsy and epileptogenesis.CrossRefPubMed
37.
go back to reference Hirvonen J, Kreisl WC, Fujita M, Dustin I, Khan O, Appel S, et al. Increased in vivo expression of an inflammatory marker in temporal lobe epilepsy. J Nucl Med. 2012;53:234–40.CrossRefPubMed Hirvonen J, Kreisl WC, Fujita M, Dustin I, Khan O, Appel S, et al. Increased in vivo expression of an inflammatory marker in temporal lobe epilepsy. J Nucl Med. 2012;53:234–40.CrossRefPubMed
38.
39.
go back to reference Louw D, Sutherland GR, Glavin GB, Girvin J. A study of monoamine metabolism in human epilepsy. Can J Neurol Sci. 1989;16:394–7.PubMed Louw D, Sutherland GR, Glavin GB, Girvin J. A study of monoamine metabolism in human epilepsy. Can J Neurol Sci. 1989;16:394–7.PubMed
40.
go back to reference Chugani DC. α-methyl-L-tryptophan: mechanisms for tracer localization of epileptogenic brain regions. Biomarkers Med. 2011;5:567–75.CrossRef Chugani DC. α-methyl-L-tryptophan: mechanisms for tracer localization of epileptogenic brain regions. Biomarkers Med. 2011;5:567–75.CrossRef
41.
go back to reference Chugani DC, Chugani HT, Muzik O, Shah JR, Shah AK, Canady A, et al. Imaging epileptogenic tubers in children with tuberous sclerosis complex using alpha-[11C]methyl-L-tryptophan positron emission tomography. Ann Neurol. 1998;44:858–66.CrossRefPubMed Chugani DC, Chugani HT, Muzik O, Shah JR, Shah AK, Canady A, et al. Imaging epileptogenic tubers in children with tuberous sclerosis complex using alpha-[11C]methyl-L-tryptophan positron emission tomography. Ann Neurol. 1998;44:858–66.CrossRefPubMed
42.
go back to reference Asano E, Chugani DC, Muzik O, Shen C, Juhász C, Janisse J, et al. Multimodality imaging for improved detection of epileptogenic foci in tuberous sclerosis complex. Neurology. 2000;54:1976–84.CrossRefPubMed Asano E, Chugani DC, Muzik O, Shen C, Juhász C, Janisse J, et al. Multimodality imaging for improved detection of epileptogenic foci in tuberous sclerosis complex. Neurology. 2000;54:1976–84.CrossRefPubMed
43.
go back to reference Kagawa K, Chugani DC, Asano E, Juhász C, Muzik O, Shah A, et al. Epilepsy surgery outcome in children with tuberous sclerosis complex evaluated with alpha-[11C]methyl-L-tryptophan positron emission tomography (PET). J Child Neurol. 2005;20:429–38.CrossRefPubMed Kagawa K, Chugani DC, Asano E, Juhász C, Muzik O, Shah A, et al. Epilepsy surgery outcome in children with tuberous sclerosis complex evaluated with alpha-[11C]methyl-L-tryptophan positron emission tomography (PET). J Child Neurol. 2005;20:429–38.CrossRefPubMed
44.••
go back to reference Chugani HT, Luat AF, Kumar A, Govindan R, Pawlik K, Asano E. α-[11C]-methyl-L-tryptophan—PET in 191 patients with tuberous sclerosis complex. Neurology. 2013;81:674–80. Chugani et al. reported findings of [11C]AMT-PET in a large cohort of patients with tuberous sclerosis complex. There was excellent agreement between lateralization on ictal EEG and PET, whereas PET provided additional localizing information in certain cases.CrossRefPubMedPubMedCentral Chugani HT, Luat AF, Kumar A, Govindan R, Pawlik K, Asano E. α-[11C]-methyl-L-tryptophan—PET in 191 patients with tuberous sclerosis complex. Neurology. 2013;81:674–80. Chugani et al. reported findings of [11C]AMT-PET in a large cohort of patients with tuberous sclerosis complex. There was excellent agreement between lateralization on ictal EEG and PET, whereas PET provided additional localizing information in certain cases.CrossRefPubMedPubMedCentral
45.•
go back to reference Rubí S, Costes N, Heckemann RA, Bouvard S, Hammers A, Martí Fuster B, et al. Positron emission tomography with α-[11C]methyl-L-tryptophan in tuberous sclerosis complex-related epilepsy. Epilepsia. 2013;54:2143–50. Rubí et al. demonstrated the use of [11C]AMT-PET in one of few studies performed outside of Detroit. The found low sensitivity but excellent specificity for focus localization in a small external validation cohort of tuberous sclerosis patients.CrossRefPubMed Rubí S, Costes N, Heckemann RA, Bouvard S, Hammers A, Martí Fuster B, et al. Positron emission tomography with α-[11C]methyl-L-tryptophan in tuberous sclerosis complex-related epilepsy. Epilepsia. 2013;54:2143–50. Rubí et al. demonstrated the use of [11C]AMT-PET in one of few studies performed outside of Detroit. The found low sensitivity but excellent specificity for focus localization in a small external validation cohort of tuberous sclerosis patients.CrossRefPubMed
46.
go back to reference Juhász C, Chugani DC, Padhye UN, Muzik O, Shah A, Asano E, et al. Evaluation with alpha-[11C]methyl-L-tryptophan positron emission tomography for reoperation after failed epilepsy surgery. Epilepsia. 2004;45:124–30.CrossRefPubMed Juhász C, Chugani DC, Padhye UN, Muzik O, Shah A, Asano E, et al. Evaluation with alpha-[11C]methyl-L-tryptophan positron emission tomography for reoperation after failed epilepsy surgery. Epilepsia. 2004;45:124–30.CrossRefPubMed
47.
go back to reference Juhász C, Chugani DC, Muzik O, Shah A, Asano E, Mangner TJ, et al. Alpha-methyl-L-tryptophan PET detects epileptogenic cortex in children with intractable epilepsy. Neurology. 2003;60:960–8.CrossRefPubMed Juhász C, Chugani DC, Muzik O, Shah A, Asano E, Mangner TJ, et al. Alpha-methyl-L-tryptophan PET detects epileptogenic cortex in children with intractable epilepsy. Neurology. 2003;60:960–8.CrossRefPubMed
48.
go back to reference Garibotto V, Picard F. Nuclear medicine imaging in epilepsy. Epileptologie. 2013;30:109–21. Garibotto V, Picard F. Nuclear medicine imaging in epilepsy. Epileptologie. 2013;30:109–21.
49.•
go back to reference Martinez A, Finegersh A, Cannon DM, Dustin I, Nugent A, Herscovitch P, et al. The 5-HT1A receptor and 5-HT transporter in temporal lobe epilepsy. Neurology. 2013;80:1465–71. Martinez et al. found a reduced activity of the serotonin transporter in epilepsy patients with comorbid depression. This might represent an attempt of the brain to compensate for reduced serotonin levels in concomitant depression.CrossRefPubMedPubMedCentral Martinez A, Finegersh A, Cannon DM, Dustin I, Nugent A, Herscovitch P, et al. The 5-HT1A receptor and 5-HT transporter in temporal lobe epilepsy. Neurology. 2013;80:1465–71. Martinez et al. found a reduced activity of the serotonin transporter in epilepsy patients with comorbid depression. This might represent an attempt of the brain to compensate for reduced serotonin levels in concomitant depression.CrossRefPubMedPubMedCentral
50.
go back to reference Toczek MT, Carson RE, Lang L, Ma Y, Spanaki MV, Der MG, et al. PET imaging of 5-HT1A receptor binding in patients with temporal lobe epilepsy. Neurology. 2003;60:749–56.CrossRefPubMed Toczek MT, Carson RE, Lang L, Ma Y, Spanaki MV, Der MG, et al. PET imaging of 5-HT1A receptor binding in patients with temporal lobe epilepsy. Neurology. 2003;60:749–56.CrossRefPubMed
51.
go back to reference Savic I, Lindstrom P, Gulyás B, Halldin C, Andrée B, Farde L. Limbic reductions of 5-HT1A receptor binding in human temporal lobe epilepsy. Neurology. 2004;62:1343–51.CrossRefPubMed Savic I, Lindstrom P, Gulyás B, Halldin C, Andrée B, Farde L. Limbic reductions of 5-HT1A receptor binding in human temporal lobe epilepsy. Neurology. 2004;62:1343–51.CrossRefPubMed
52.
go back to reference Giovacchini G, Toczek MT, Bonwetsch R, Bagic A, Lang L, Fraser C, et al. 5-HT 1A receptors are reduced in temporal lobe epilepsy after partial-volume correction. J Nucl Med. 2005;46:1128–35.PubMedPubMedCentral Giovacchini G, Toczek MT, Bonwetsch R, Bagic A, Lang L, Fraser C, et al. 5-HT 1A receptors are reduced in temporal lobe epilepsy after partial-volume correction. J Nucl Med. 2005;46:1128–35.PubMedPubMedCentral
53.
go back to reference Hasler G, Bonwetsch R, Giovacchini G, Toczek MT, Bagic A, Luckenbaugh DA, et al. 5-HT1A receptor binding in temporal lobe epilepsy patients with and without major depression. BPS. 2007;62:1258–64. Hasler G, Bonwetsch R, Giovacchini G, Toczek MT, Bagic A, Luckenbaugh DA, et al. 5-HT1A receptor binding in temporal lobe epilepsy patients with and without major depression. BPS. 2007;62:1258–64.
54.
go back to reference Liew CJ, Lim Y-M, Bonwetsch R, Shamim S, Sato S, Reeves-Tyer P, et al. 18F-FCWAY and 18F-FDG PET in MRI-negative temporal lobe epilepsy. Epilepsia. 2009;50:234–9.CrossRefPubMedPubMedCentral Liew CJ, Lim Y-M, Bonwetsch R, Shamim S, Sato S, Reeves-Tyer P, et al. 18F-FCWAY and 18F-FDG PET in MRI-negative temporal lobe epilepsy. Epilepsia. 2009;50:234–9.CrossRefPubMedPubMedCentral
55.
go back to reference Merlet I, Ostrowsky K, Costes N, Ryvlin P, Isnard J, Faillenot I, et al. 5-HT1A receptor binding and intracerebral activity in temporal lobe epilepsy: an [18F]MPPF-PET study. Brain. 2004;127:900–13.CrossRefPubMed Merlet I, Ostrowsky K, Costes N, Ryvlin P, Isnard J, Faillenot I, et al. 5-HT1A receptor binding and intracerebral activity in temporal lobe epilepsy: an [18F]MPPF-PET study. Brain. 2004;127:900–13.CrossRefPubMed
56.
go back to reference Merlet I, Ryvlin P, Costes N, Dufournel D, Isnard J, Faillenot I, et al. Statistical parametric mapping of 5-HT1A receptor binding in temporal lobe epilepsy with hippocampal ictal onset on intracranial EEG. Neuroimage. 2004;22:886–96.CrossRefPubMed Merlet I, Ryvlin P, Costes N, Dufournel D, Isnard J, Faillenot I, et al. Statistical parametric mapping of 5-HT1A receptor binding in temporal lobe epilepsy with hippocampal ictal onset on intracranial EEG. Neuroimage. 2004;22:886–96.CrossRefPubMed
57.
go back to reference Didelot A, Ryvlin P, Lothe A, Merlet I, Hammers A, Mauguière F. PET imaging of brain 5-HT1A receptors in the preoperative evaluation of temporal lobe epilepsy. Brain. 2008;131:2751–64.CrossRefPubMed Didelot A, Ryvlin P, Lothe A, Merlet I, Hammers A, Mauguière F. PET imaging of brain 5-HT1A receptors in the preoperative evaluation of temporal lobe epilepsy. Brain. 2008;131:2751–64.CrossRefPubMed
58.
go back to reference Didelot A, Mauguière F, Redouté J, Bouvard S, Lothe A, Reilhac A, et al. Voxel-based analysis of asymmetry index maps increases the specificity of 18F-MPPF PET abnormalities for localizing the epileptogenic zone in temporal lobe epilepsies. J Nucl Med. 2010;51:1732–9.CrossRefPubMed Didelot A, Mauguière F, Redouté J, Bouvard S, Lothe A, Reilhac A, et al. Voxel-based analysis of asymmetry index maps increases the specificity of 18F-MPPF PET abnormalities for localizing the epileptogenic zone in temporal lobe epilepsies. J Nucl Med. 2010;51:1732–9.CrossRefPubMed
59.
go back to reference Theodore WH, Hasler G, Giovacchini G, Kelley K, Reeves-Tyer P, Herscovitch P, et al. Reduced hippocampal 5HT1A PET receptor binding and depression in temporal lobe epilepsy. Epilepsia. 2007;48:1526–30.CrossRefPubMed Theodore WH, Hasler G, Giovacchini G, Kelley K, Reeves-Tyer P, Herscovitch P, et al. Reduced hippocampal 5HT1A PET receptor binding and depression in temporal lobe epilepsy. Epilepsia. 2007;48:1526–30.CrossRefPubMed
60.
go back to reference Lothe A, Didelot A, Hammers A, Costes N, Saoud M, Gilliam F, et al. Comorbidity between temporal lobe epilepsy and depression: a [18F]MPPF PET study. Brain. 2008;131:2765–82.CrossRefPubMed Lothe A, Didelot A, Hammers A, Costes N, Saoud M, Gilliam F, et al. Comorbidity between temporal lobe epilepsy and depression: a [18F]MPPF PET study. Brain. 2008;131:2765–82.CrossRefPubMed
61.
go back to reference Cannon DM, Ichise M, Rollis D, Klaver JM, Gandhi SK, Charney DS, et al. Elevated serotonin transporter binding in major depressive disorder assessed using positron emission tomography and [11C]DASB; comparison with bipolar disorder. BPS. 2007;62:870–7. Cannon DM, Ichise M, Rollis D, Klaver JM, Gandhi SK, Charney DS, et al. Elevated serotonin transporter binding in major depressive disorder assessed using positron emission tomography and [11C]DASB; comparison with bipolar disorder. BPS. 2007;62:870–7.
62.
go back to reference Haut SR, Albin RL. Dopamine and epilepsy: hints of complex subcortical roles. Neurology. 2008;71:784–5.CrossRefPubMed Haut SR, Albin RL. Dopamine and epilepsy: hints of complex subcortical roles. Neurology. 2008;71:784–5.CrossRefPubMed
63.
64.
go back to reference Deransart C, Riban V, Lê B, Marescaux C, Depaulis A. Dopamine in the striatum modulates seizures in a genetic model of absence epilepsy in the rat. Neuroscience. 2000;100:335–44.CrossRefPubMed Deransart C, Riban V, Lê B, Marescaux C, Depaulis A. Dopamine in the striatum modulates seizures in a genetic model of absence epilepsy in the rat. Neuroscience. 2000;100:335–44.CrossRefPubMed
65.
go back to reference Biraben A, Semah F, Ribeiro M-J, Douaud G, Remy P, Depaulis A. PET evidence for a role of the basal ganglia in patients with ring chromosome 20 epilepsy. Neurology. 2004;63:73–7.CrossRefPubMed Biraben A, Semah F, Ribeiro M-J, Douaud G, Remy P, Depaulis A. PET evidence for a role of the basal ganglia in patients with ring chromosome 20 epilepsy. Neurology. 2004;63:73–7.CrossRefPubMed
66.
go back to reference Bouilleret V, Semah F, Biraben A, Taussig D, Chassoux F, Syrota A, et al. Involvement of the basal ganglia in refractory epilepsy: an 18F-fluoro-L-DOPA PET study using 2 methods of analysis. J Nucl Med. 2005;46:540–7.PubMed Bouilleret V, Semah F, Biraben A, Taussig D, Chassoux F, Syrota A, et al. Involvement of the basal ganglia in refractory epilepsy: an 18F-fluoro-L-DOPA PET study using 2 methods of analysis. J Nucl Med. 2005;46:540–7.PubMed
67.
go back to reference Bouilleret V, Semah F, Chassoux F, Mantzaridez M, Biraben A, Trebossen R, et al. Basal ganglia involvement in temporal lobe epilepsy: a functional and morphologic study. Neurology. 2008;70:177–84.CrossRefPubMed Bouilleret V, Semah F, Chassoux F, Mantzaridez M, Biraben A, Trebossen R, et al. Basal ganglia involvement in temporal lobe epilepsy: a functional and morphologic study. Neurology. 2008;70:177–84.CrossRefPubMed
68.
go back to reference Werhahn KJ, Landvogt C, Klimpe S, Buchholz H-G, Yakushev I, Siessmeier T, et al. Decreased dopamine D2/D3-receptor binding in temporal lobe epilepsy: an [18F]fallypride PET study. Epilepsia. 2006;47:1392–6.CrossRefPubMed Werhahn KJ, Landvogt C, Klimpe S, Buchholz H-G, Yakushev I, Siessmeier T, et al. Decreased dopamine D2/D3-receptor binding in temporal lobe epilepsy: an [18F]fallypride PET study. Epilepsia. 2006;47:1392–6.CrossRefPubMed
69.
go back to reference Yakushev IY, Dupont E, Buchholz H-G, Tillmanns J, Debus F, Cumming P, et al. In vivo imaging of dopamine receptors in a model of temporal lobe epilepsy. Epilepsia. 2010;51:415–22.CrossRefPubMed Yakushev IY, Dupont E, Buchholz H-G, Tillmanns J, Debus F, Cumming P, et al. In vivo imaging of dopamine receptors in a model of temporal lobe epilepsy. Epilepsia. 2010;51:415–22.CrossRefPubMed
70.
go back to reference Landvogt C, Buchholz H-G, Bernedo V, Schreckenberger M, Werhahn KJ. Alteration of dopamine D2/D3 receptor binding in patients with juvenile myoclonic epilepsy. Epilepsia. 2010;51:1699–706.CrossRefPubMed Landvogt C, Buchholz H-G, Bernedo V, Schreckenberger M, Werhahn KJ. Alteration of dopamine D2/D3 receptor binding in patients with juvenile myoclonic epilepsy. Epilepsia. 2010;51:1699–706.CrossRefPubMed
71.
go back to reference Bernedo Paredes VE, Buchholz H-G, Gartenschläger M, Breimhorst M, Schreckenberger M, Werhahn KJ. Reduced D2/D3 receptor binding of extrastriatal and striatal regions in temporal lobe epilepsy. PLoS ONE. 2015;10, e0141098.CrossRefPubMedPubMedCentral Bernedo Paredes VE, Buchholz H-G, Gartenschläger M, Breimhorst M, Schreckenberger M, Werhahn KJ. Reduced D2/D3 receptor binding of extrastriatal and striatal regions in temporal lobe epilepsy. PLoS ONE. 2015;10, e0141098.CrossRefPubMedPubMedCentral
72.
go back to reference Fedi M, Berkovic SF, Scheffer IE, O'Keefe G, Marini C, Mulligan R, et al. Reduced striatal D1 receptor binding in autosomal dominant nocturnal frontal lobe epilepsy. Neurology. 2008;71:795–8.CrossRefPubMed Fedi M, Berkovic SF, Scheffer IE, O'Keefe G, Marini C, Mulligan R, et al. Reduced striatal D1 receptor binding in autosomal dominant nocturnal frontal lobe epilepsy. Neurology. 2008;71:795–8.CrossRefPubMed
73.
go back to reference Ciumas C, Wahlin T-BR, Jucaite A, Lindstrom P, Halldin C, Savic I. Reduced dopamine transporter binding in patients with juvenile myoclonic epilepsy. Neurology. 2008;71:788–94.CrossRefPubMed Ciumas C, Wahlin T-BR, Jucaite A, Lindstrom P, Halldin C, Savic I. Reduced dopamine transporter binding in patients with juvenile myoclonic epilepsy. Neurology. 2008;71:788–94.CrossRefPubMed
74.
go back to reference Ciumas C, Wahlin T-BR, Espino C, Savic I. The dopamine system in idiopathic generalized epilepsies: identification of syndrome-related changes. Neuroimage. 2010;51:606–15.CrossRefPubMed Ciumas C, Wahlin T-BR, Espino C, Savic I. The dopamine system in idiopathic generalized epilepsies: identification of syndrome-related changes. Neuroimage. 2010;51:606–15.CrossRefPubMed
75.
go back to reference Odano I, Varrone A, Savic I, Ciumas C, Karlsson P, Jucaite A, et al. Quantitative PET analyses of regional [11C]PE2I binding to the dopamine transporter—application to juvenile myoclonic epilepsy. Neuroimage. 2012;59:3582–93.CrossRefPubMed Odano I, Varrone A, Savic I, Ciumas C, Karlsson P, Jucaite A, et al. Quantitative PET analyses of regional [11C]PE2I binding to the dopamine transporter—application to juvenile myoclonic epilepsy. Neuroimage. 2012;59:3582–93.CrossRefPubMed
76.
go back to reference Rocha L, Alonso-Vanegas M, Villeda-Hernández J, Mújica M, Cisneros-Franco JM, López-Gómez M, et al. Dopamine abnormalities in the neocortex of patients with temporal lobe epilepsy. Neurobiol Dis. 2012;45:499–507.CrossRefPubMed Rocha L, Alonso-Vanegas M, Villeda-Hernández J, Mújica M, Cisneros-Franco JM, López-Gómez M, et al. Dopamine abnormalities in the neocortex of patients with temporal lobe epilepsy. Neurobiol Dis. 2012;45:499–507.CrossRefPubMed
77.
go back to reference Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, et al. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science. 2003;302:84–8.CrossRefPubMed Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, et al. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science. 2003;302:84–8.CrossRefPubMed
78.
go back to reference Wallace MJ, Blair RE, Falenski KW, Martin BR, DeLorenzo RJ. The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J Pharmacol Exp Ther. 2003;307:129–37.CrossRefPubMed Wallace MJ, Blair RE, Falenski KW, Martin BR, DeLorenzo RJ. The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J Pharmacol Exp Ther. 2003;307:129–37.CrossRefPubMed
79.
go back to reference Falenski KW, Blair RE, Sim-Selley LJ, Martin BR, DeLorenzo RJ. Status epilepticus causes a long-lasting redistribution of hippocampal cannabinoid type 1 receptor expression and function in the rat pilocarpine model of acquired epilepsy. Neuroscience. 2007;146:1232–44.CrossRefPubMedPubMedCentral Falenski KW, Blair RE, Sim-Selley LJ, Martin BR, DeLorenzo RJ. Status epilepticus causes a long-lasting redistribution of hippocampal cannabinoid type 1 receptor expression and function in the rat pilocarpine model of acquired epilepsy. Neuroscience. 2007;146:1232–44.CrossRefPubMedPubMedCentral
80.
go back to reference Karlócai MR, Tóth K, Watanabe M, Ledent C, Juhász G, Freund TF, et al. Redistribution of CB1 cannabinoid receptors in the acute and chronic phases of pilocarpine-induced epilepsy. PLoS ONE. 2011;6, e27196.CrossRefPubMedPubMedCentral Karlócai MR, Tóth K, Watanabe M, Ledent C, Juhász G, Freund TF, et al. Redistribution of CB1 cannabinoid receptors in the acute and chronic phases of pilocarpine-induced epilepsy. PLoS ONE. 2011;6, e27196.CrossRefPubMedPubMedCentral
81.
go back to reference Chen K, Neu A, Howard AL, Földy C, Echegoyen J, Hilgenberg L, et al. Prevention of plasticity of endocannabinoid signaling inhibits persistent limbic hyperexcitability caused by developmental seizures. J Neurosci. 2007;27:46–58.CrossRefPubMed Chen K, Neu A, Howard AL, Földy C, Echegoyen J, Hilgenberg L, et al. Prevention of plasticity of endocannabinoid signaling inhibits persistent limbic hyperexcitability caused by developmental seizures. J Neurosci. 2007;27:46–58.CrossRefPubMed
82.
go back to reference Goffin K, Van Paesschen W, Van Laere K. In vivo activation of endocannabinoid system in temporal lobe epilepsy with hippocampal sclerosis. Brain. 2011;134:1033–40.CrossRefPubMed Goffin K, Van Paesschen W, Van Laere K. In vivo activation of endocannabinoid system in temporal lobe epilepsy with hippocampal sclerosis. Brain. 2011;134:1033–40.CrossRefPubMed
83.
go back to reference Riaño Barros DA, McGinnity CJ, Rosso L, Heckemann RA, Howes OD, Brooks DJ, et al. Test-retest reproducibility of cannabinoid-receptor type 1 availability quantified with the PET ligand [11C]MePPEP. Neuroimage. 2014;97:151–62.CrossRefPubMedPubMedCentral Riaño Barros DA, McGinnity CJ, Rosso L, Heckemann RA, Howes OD, Brooks DJ, et al. Test-retest reproducibility of cannabinoid-receptor type 1 availability quantified with the PET ligand [11C]MePPEP. Neuroimage. 2014;97:151–62.CrossRefPubMedPubMedCentral
84.
go back to reference Koepp MJ, Richardson MP, Brooks DJ, Duncan JS. Focal cortical release of endogenous opioids during reading-induced seizures. Lancet. 1998;352:952–5.CrossRefPubMed Koepp MJ, Richardson MP, Brooks DJ, Duncan JS. Focal cortical release of endogenous opioids during reading-induced seizures. Lancet. 1998;352:952–5.CrossRefPubMed
85.
go back to reference Bartenstein PA, Duncan JS, Prevett MC, Cunningham VJ, Fish DR, Jones AK, et al. Investigation of the opioid system in absence seizures with positron emission tomography. J Neurol Neurosurg Psychiatr. 1993;56:1295–302.CrossRefPubMedPubMedCentral Bartenstein PA, Duncan JS, Prevett MC, Cunningham VJ, Fish DR, Jones AK, et al. Investigation of the opioid system in absence seizures with positron emission tomography. J Neurol Neurosurg Psychiatr. 1993;56:1295–302.CrossRefPubMedPubMedCentral
86.
go back to reference Hammers A, Asselin M-C, Hinz R, Kitchen I, Brooks DJ, Duncan JS, et al. Upregulation of opioid receptor binding following spontaneous epileptic seizures. Brain. 2007;130:1009–16.CrossRefPubMed Hammers A, Asselin M-C, Hinz R, Kitchen I, Brooks DJ, Duncan JS, et al. Upregulation of opioid receptor binding following spontaneous epileptic seizures. Brain. 2007;130:1009–16.CrossRefPubMed
87.
go back to reference McGinnity CJ, Shidahara M, Feldmann M, Keihaninejad S, Riaño Barros DA, Gousias IS, et al. Quantification of opioid receptor availability following spontaneous epileptic seizures: correction of [11C]diprenorphine PET data for the partial-volume effect. Neuroimage. 2013;79:72–80.CrossRefPubMed McGinnity CJ, Shidahara M, Feldmann M, Keihaninejad S, Riaño Barros DA, Gousias IS, et al. Quantification of opioid receptor availability following spontaneous epileptic seizures: correction of [11C]diprenorphine PET data for the partial-volume effect. Neuroimage. 2013;79:72–80.CrossRefPubMed
88.
go back to reference De Fusco M, Becchetti A, Patrignani A, Annesi G, Gambardella A, Quattrone A, et al. The nicotinic receptor beta 2 subunit is mutant in nocturnal frontal lobe epilepsy. Nat Genet. 2000;26:275–6.CrossRefPubMed De Fusco M, Becchetti A, Patrignani A, Annesi G, Gambardella A, Quattrone A, et al. The nicotinic receptor beta 2 subunit is mutant in nocturnal frontal lobe epilepsy. Nat Genet. 2000;26:275–6.CrossRefPubMed
89.
go back to reference Steinlein OK, Mulley JC, Propping P, Wallace RH, Phillips HA, Sutherland GR, et al. A missense mutation in the neuronal nicotinic acetylcholine receptor alpha 4 subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy. Nat Genet. 1995;11:201–3.CrossRefPubMed Steinlein OK, Mulley JC, Propping P, Wallace RH, Phillips HA, Sutherland GR, et al. A missense mutation in the neuronal nicotinic acetylcholine receptor alpha 4 subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy. Nat Genet. 1995;11:201–3.CrossRefPubMed
90.
go back to reference Picard F, Bruel D, Servent D, Saba W, Fruchart-Gaillard C, Schöllhorn-Peyronneau M-A, et al. Alteration of the in vivo nicotinic receptor density in ADNFLE patients: a PET study. Brain. 2006;129:2047–60.CrossRefPubMed Picard F, Bruel D, Servent D, Saba W, Fruchart-Gaillard C, Schöllhorn-Peyronneau M-A, et al. Alteration of the in vivo nicotinic receptor density in ADNFLE patients: a PET study. Brain. 2006;129:2047–60.CrossRefPubMed
91.
go back to reference Löscher W, Hirsch LJ, Schmidt D. The enigma of the latent period in the development of symptomatic acquired epilepsy—traditional view versus new concepts. Epilepsy Behav. 2015;52:78–92.CrossRefPubMed Löscher W, Hirsch LJ, Schmidt D. The enigma of the latent period in the development of symptomatic acquired epilepsy—traditional view versus new concepts. Epilepsy Behav. 2015;52:78–92.CrossRefPubMed
Metadata
Title
Advances of Molecular Imaging in Epilepsy
Authors
Marian Galovic
Matthias Koepp
Publication date
01-06-2016
Publisher
Springer US
Published in
Current Neurology and Neuroscience Reports / Issue 6/2016
Print ISSN: 1528-4042
Electronic ISSN: 1534-6293
DOI
https://doi.org/10.1007/s11910-016-0660-7

Other articles of this Issue 6/2016

Current Neurology and Neuroscience Reports 6/2016 Go to the issue

Neuroimaging (DJ Brooks, Section Editor)

Imaging Systemic Dysfunction in Parkinson’s Disease

Critical Care (SA Mayer, Section Editor)

Brain Multimodality Monitoring: Updated Perspectives

Genetics (V Bonifati, Section Editor)

ALS: Recent Developments from Genetics Studies

Behavior (H Kirshner, Section Editor)

Kleine-Levin Syndrome

Neurology of Systemic Diseases (J Biller, Section Editor)

Neurologic Complications in the Intensive Care Unit