Adrian ED. The spread of activity in the cerebral cortex. J Physiol
1936;88:127-61.
Alarcón G, Martinez J, Kerai SV, Lacruz ME, Quiroga RQ, Selway RP, et al.
In vivo neuronal firing patterns during human epileptiform discharges
replicated by electrical stimulation. Clin Neurophysiol 2012;123:1736-44.
10
Bernier GP, Richer F, Giard N, Bouvier G, Mercier M, Turmel A, et al.
11
Electrical stimulation of the human brain in epilepsy. Epilepsia 1990;31:513-
12
20.
13
14
Blume WT, Jones DC, Pathak P. Properties of after-discharges from cortical
15
electrical stimulation in focal epilepsies. Clin Neurophysiol 2004;115:982-9.
16
17
Buser P, Bancaud J, Talairach J, Szikla G. Amygdalo-hippocampal
18
interconnections in man. Physiological study during stereotaxic explorations.
19
Electroencephalogr Clin Neurophysiol. 1969;26:637.
20
27
Kobayashi et al 28
Buser P, Bancaud J. Unilateral connections between amygdala and
hippocampus in man. A study of epileptic patients with depth electrodes.
Electroencephalogr Clin Neurophysiol. 1983;55:1-12.
Cherlow DG, Dymond AM, Crandall PH, Walter RD, Serafetinides EA.
Evoked response and after-discharge thresholds to electrical stimulation in
temporal lobe epileptics. Arch Neurol 1977;34:527-31.
Conner CR, Ellmore TM, DiSano MA, Pieters TA, Potter AW, Tandon N.
10
Anatomic and electro-physiologic connectivity of the language system: a
11
combined DTI-CCEP study. Comput Biol Med 2011;41:1100-9.
12
13
Enatsu R, Jin K, Elwan S, Kubota Y, Piao Z, O'Connor T, et al. Correlations
14
between ictal propagation and response to electrical cortical stimulation: a
15
cortico-cortical evoked potential study. Epilepsy Res 2012;101:76-87.
16
17
Entz L, Tóth E, Keller CJ, Bickel S, Groppe DM, Fabó D, et al. Evoked
18
effective connectivity of the human neocortex. Hum Brain Mapp
19
2014;35:5736-53.
20
28
Kobayashi et al 29
Greenlee JD, Oya H, Kawasaki H, Volkov IO, Severson MA 3rd, Howard MA
3rd, et al. Functional connections within the human inferior frontal gyrus. J
Comp Neurol 2007;503:550-9.
Iwasaki M, Enatsu R, Matsumoto R, Novak E, Thankappen B, Piao Z, et al.
Accentuated cortico-cortical evoked potentials in neocortical epilepsy in
areas of ictal onset. Epileptic Disord 2010;12:292-302.
Kalamangalam GP, Tandon N, Slater JD. Dynamic mechanisms underlying
10
afterdischarge: a human subdural recording study. Clin Neurophysiol
11
2014;125:1324-38.
12
13
Kobayashi K, Matsumoto R, Matsuhashi M, Usami K, Shimotake A, Kunieda
14
T, et al. High frequency activity overriding cortico-cortical evoked potentials
15
reflects altered excitability in the human epileptic focus. Clin Neurophysiol
16
2017;128:1673-1681.
17
18
Lesser RP, Lüders H, Klem G, Dinner DS, Morris HH, Hahn J. Cortical
19
afterdischarge and functional response thresholds: results of extraoperative
20
testing. Epilepsia 1984;25:615-21.
21
29
Kobayashi et al 30
Matsumoto R, Ikeda A, Ohara S, Matsuhashi M, Baba K, Yamane F, et al.
Motor-related functional subdivisions of human lateral premotor cortex:
epicortical recording in conditional visuomotor task. Clin Neurophysiol
2003;114:1102-15.
Matsumoto R, Nair DR, LaPresto E, Najm I, Bingaman W, Shibasaki H, et al.
Functional connectivity in the human language system: a cortico-cortical
evoked potential study. Brain 2004;127:2316-30.
10
Matsumoto R, Kinoshita M, Taki J, Hitomi T, Mikuni N, Shibasaki H, et al. In
11
vivo epileptogenicity of focal cortical dysplasia: a direct cortical paired
12
stimulation study. Epilepsia 2005;46:1744-9.
13
14
Matsumoto R, Nair DR, LaPresto E, Bingaman W, Shibasaki H, Lüders HO.
15
Functional connectivity in human cortical motor system: a cortico-cortical
16
evoked potential study. Brain 2007;130:181-97.
17
18
Matsumoto R, Nair DR, Ikeda A, Fumuro T, Lapresto E, Mikuni N, et al.
19
Parieto-frontal network in humans studied by cortico-cortical evoked
20
potential. Hum Brain Mapp 2012;33:2856-72.
21
30
Kobayashi et al 31
Matsumoto R, Kunieda T, Nair D. Single pulse electrical stimulation to probe
functional and pathological connectivity in epilepsy. Seizure 2017;44:27-36.
Matsumoto R, Kunieda T. Cortico-cortical evoked potential mapping. In:
Lhatoo S, Kahane P, Lüders H, editors. Invasive Studies of the Human
Epileptic Brain: Principles and Practice. Oxford: Oxford University Press;
2018. p. 431-53. ISBN-13: 978-0198714668.
Matsuzaki N, Juhász C, Asano E. Cortico-cortical evoked potentials and
10
stimulation-elicited gamma activity preferentially propagate from lower- to
11
higher-order visual areas. Clin Neurophysiol. 2013;124:1290-6.
12
13
Suzuki H, Enatsu R, Kanno A, Suzuki Y, Yokoyama R, Ookawa S, et al.
14
Threshold and distribution of afterdischarges with electrical cortical
15
stimulation. J Clin Neurosci 2018;55:71-75.
16
17
Terada K, Umeoka S, Usui N, Baba K, Usui K, Fujitani S, et al. Uneven
18
interhemispheric connections between left and right primary sensori-motor
19
areas. Hum Brain Mapp 2012;33:14-26.
20
21
Usami K, Matsumoto R, Kobayashi K, Hitomi T, Shimotake A, Kikuchi T, et
22
al. Sleep modulates cortical connectivity and excitability in humans: Direct
31
Kobayashi et al 32
evidence from neural activity induced by single-pulse electrical stimulation.
Hum Brain Mapp 2015;36:4714-29.
Valentín A, Anderson M, Alarcón G, Seoane JJ, Selway R, Binnie CD, et al.
Responses to single pulse electrical stimulation identify epileptogenesis in
the human brain in vivo. Brain 2002;125:1709-18.
Valentín A, Alarcón G, Honavar M, García Seoane JJ, Selway RP, Polkey
CE, et al. Single pulse electrical stimulation for identification of structural
10
abnormalities and prediction of seizure outcome after epilepsy surgery: a
11
prospective study. Lancet Neurol 2005;4:718-26.
12
13
Yamamoto J, Ikeda A, Satow T, Takeshita K, Takayama M, Matsuhashi M, et
14
al. Low-frequency electric cortical stimulation has an inhibitory effect on
15
epileptic focus in mesial temporal lobe epilepsy. Epilepsia 2002;43:491-5.
16
17
Yamamoto J, Ikeda A, Kinoshita M, Matsumoto R, Satow T, Takeshita K, et
18
al. Low-frequency electric cortical stimulation decreases interictal and ictal
19
activity in human epilepsy. Seizure 2006;15:520-7.
20
32
Kobayashi et al 33
Figure Legends
Figure 1: A representative ECoG of stimulus-induced clinical seizure
(Patient 3)
A: Ictal ECoG induced by SPES on the pair of electrodes on the precentral
gyrus (C19-C20). Repetitive spikes appeared on the B plate, followed by
paroxysmal fast occurring on the C plate (shown in the magenta frames).
The patient showed a habitual seizure characterized by right foot twitches.
The recording band-pass filter was 0.08-600 Hz and the filter for display is
10
1.6-50 Hz.
11
B: Configuration of implanted SDG electrodes. SOZs defined by the initial
12
ictal ECoG changes in the spontaneous seizure are shown as red circles.
13
Abbreviations: ECoG = electrocorticogram; SPES = single-pulse electrical
14
stimulation; SDG = subdural grid; SOZ = seizure-onset zone.
15
16
Figure 2: A representative ECoG of stimulus-induced clinical seizure
17
(Patient 25)
18
A: In this patient (Patient 25), SOZ was not conventionally identified because
19
spontaneous seizure did not occur despite AED reduction. One electrode
20
pair of SPESs (A12-A17) induced a habitual seizure that included
21
hyperventilation and right face twitches. This finally evolved to focal to
22
bilateral tonic-clonic seizure. Clear ictal ECoG changes are highlighted by the
33
Kobayashi et al 34
frames in magenta. The surgical removal of the areas including the pair that
induced the seizure and showed the earliest ECoG changes during the
induced seizure led to seizure freedom for more than 2 years. The recording
band-pass filter was 0.08-300 Hz and the filter for display is 1.6-50 Hz.
B: Configuration of implanted SDG electrodes. Probable SOZs, defined by
this stimulus-induced clinical seizure, are shown as orange circles.
Abbreviations: SOZ = seizure-onset zone; SPES = single-pulse electrical
stimulation; AC-PC line = anterior commissure – posterior commissure line;
VAC line = line vertical to the AC-PC line through the AC; Rt = right; AED =
10
antiepileptic drug; ECoG = electrocorticogram; SDG = subdural grid.
34
Kobayashi et al. 35
Table 1: Patient profile
Patient
1 (1st SDG)
1 (2nd SDG)
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
Total
Total except
for Patient 17
Age and
gender
23F
23F
23M
40M
22M
44M
24M
17F
29M
34M
38F
28F
55M
41F
52M
Epilepsy
Etiology
Rt FLE
Rt FLE
Rt OLE
Lt F-PLE
Lt F-TLE
Rt FLE
Lt FLE
Lt TLE
Lt TLE
Rt P-TLE
Lt TLE
Rt PLE
Lt TLE
Lt TLE
Lt TLE
27F
27F
39M
45M
61M
30F
28F
39M
29M
21M
16F
41M
16M
39F
23F
Rt TLE
Rt PLE
Lt FLE
Lt FLE
Lt PLE
Rt TLE
Lt TLE
Rt TLE
Rt FLE
Lt TLE
Lt FLE
Lt TLE
Rt F-T-PLE
Lt FLE
Lt PLE
FCD IA
FCD IA
FCD IIA
Mixed oligoastrocytoma
Gliosis (F), FCD IA (T)
Mixed oligoastrocytoma, FCD IA
FCD IB
FCD IB
HS, FCD IA
Posttraumatic change (P), HS (T), Scar (T)
FCD IIA
Low grade neuroepithelial tumor
Diffuse astrocytoma
FCD IA
Arteriovenous malformation, Gliosis,
Inflammatory infiltration
FCD IA
FCD IIB
FCD IIB
FCD IA
Oligoastrocytoma
FCD IIA, Mild gliosis
Non-neoplastic brain tissue
HS, FCD IA
FCD IA
HS, FCD IA
Dysmorphic neuroepithelial tumor
HS, FCD IA
FCD IC
FCD IIB
FCD IIB
Implanted SDG
electrodes
52
44
52
56
66
48
100
60
102
82
88
48
56
102
110
Total SPES
pairs
27
24
18
22
36
26
50
34
51
55
44
28
27
49
38
SPES pairs for SOZ stim
(ADs and clinical seizures)
5 (3 clinical seizures)
10
4 (2 ADs)
4 (1 AD)
10
SPES pairs for non-SOZ stim
(ADs and clinical seizures)
24
21
16
17 (1 AD)
29 (1 clinical seizure)
24
40
28
47 (1 AD)
46
41
25
23 (3 ADs)
45
28 (1 AD)
76
72
108
104
106
102
106
90
100
82
92
92
162
68
84
40
36
54
50
58
40
55
48
58
53
55
47
82
36
42
1283
1229
n.a.
5 (1 AD)
12
6 (1 clinical seizure)
12
38
29
n.a.
47
50 (1 AD)
38
50
45
50
41
49
35 (1 AD)
78
27
36
162
(4 ADs and 4 clinical seizures)
1067
(8 ADs and 1 clinical seizure)
SPES, single-pulse electrical stimulation; SOZ, seizure onset zone; stim, stimulation; AD, afterdischarge; SDG, subdural grid; FLE, frontal lobe
epilepsy; OLE, occipital lobe epilepsy; PLE, parietal lobe epilepsy; TLE, temporal lobe epilepsy; FCD, focal cortical dysplasia; HS, hippocampal
sclerosis; n.a., not available
35
Kobayashi et al. 36
Table 2: EEG characteristics of stimulus-induced clinical seizures and ADs
Patient
Event
Clinical seizure
Clinical seizure
Clinical seizure
25
Clinical seizure
Clinical seizure
AD
AD
12
AD
21
AD
AD
AD
12
AD
12
AD
12
AD
14
AD
19
AD
26
AD
Stimulus site
(anatomical
location)
SOZ
(PCL)
SOZ
(PrCG)
SOZ
(PrCG)
SOZ
(PrCG)
non-SOZ
(Ento)
SOZ
(Ento)
SOZ
(Ento)
SOZ
(Ento)
SOZ
(Ento)
non-SOZ
(PrCG)
non-SOZ
(IFG)
non-SOZ
(IFG)
non-SOZ
(FuG)
non-SOZ
(ITG)
non-SOZ
(Ento)
non-SOZ
(FuG)
non-SOZ
(ITG)
Involvement of
adjacent electrode
(<2 cm)
Involvement of
remote electrode
(>5 cm or other lobes)
Involvement
of SOZ
180
Involvement of
near electrode
(2-5 cm)
Consistency of
propagation pattern with
spontaneous seizure
Consistent
51
Consistent
15
241
Consistent
10
142
(no spontaneous seizure)
12
104
Consistent
10
50
44
14
10
28
61
10
34
10
94
10
45
Inconsistent: narrower
distribution
Inconsistent: narrower
distribution
Inconsistent: narrower
distribution
Inconsistent: narrower
distribution
Inconsistent: narrower
distribution
Inconsistent: narrower
distribution
Inconsistent: different
locations
Consistent
10
10
80
10
34
10
519
Stimulus
intensity (mA)
Duration of EEG
changes (sec)
12
Inconsistent: different
locations
Inconsistent: partial
overlap
Inconsistent: different
locations
Inconsistent: partial
overlap
AD, afterdischarge; SOZ, seizure onset zone; PCL, paracentral lobule; PrCG, precentral gyrus; Ento, entorhinal cortex; IFG, inferior frontal gyrus;
FuG, fusiform gyrus; ITG, inferior temporal gyrus
36
...