The anterior nucleus of the thalamus plays a role in the epileptic network

Abstract

Objectives: We investigated both the metabolic differences and interictal/ictal discharges of the anterior nucleus of the thalamus (ANT) in patients with epilepsy to clarify the relationship between the ANT and the epileptic network.

Methods: Nineteen patients with drug-resistant epilepsy who underwent stereoelectroencephalography were studied. Metabolic differences in ANT were analyzed using [18F] fluorodeoxyglucose-positron emission tomography with three-dimensional (3D) visual and quantitative analyses. Interictal and ictal discharges in the ANT were analyzed using visual and time-frequency analyses. The relationship between interictal discharge and metabolic differences was analyzed.

Results: We found that patients with temporal lobe epilepsy (TLE) showed significant metabolic differences in bilateral ANT compared with extratemporal lobe epilepsy in 3D visual and quantitative analyses. Four types of interictal activities were recorded from the ANT: spike, high-frequency oscillation (HFO), slow-wave, and α-rhythmic activity. Spike and HFO waveforms were recorded mainly in patients with TLE. Two spike patterns were recorded: synchronous and independent. In 83.3% of patients, ANT was involved during seizures. Three seizure onset types of ANT were recorded: low-voltage fast activity, rhythmic spikes, and theta band discharge. The time interval of seizure onset between the seizure onset zone and ANT showed two patterns: immediate and delayed.

Interpretation: ANT can receive either interictal discharges or ictal discharges which propagate from the epileptogenic zones. Independent epileptic discharges can also be recorded from the ANT in some patients. Metabolic anomalies and epileptic discharges in the ANT indicate that the ANT plays a role in the epileptic network in most patients with epilepsy, especially TLE.

Figure 1

PET‐MRI, 3D‐view of the ANT and postoperative MRI in a patient with TLE (patient 5, A) and in a patient with ETLE (patient 8, B). The ANT is delineated in the coronal PET‐MRI images in the left portion of (A) and (B); the middle and upper portions of (A) and (B) represent a magnified image of the ANT region; the middle and lower portions of (A) and (B) show the 3D view of the ventral side of the ANT; the right portion of (A) and (B) is the post‐operative MRI. The images in (A) show hypometabolism in the temporal lobe (red arrows) and the ipsilateral ANT (black arrows). The images in (B) show that the metabolic difference in the bilateral ANT was not significant. L = left

Figure 2

Differences of AAI across different categories (A) and surgical outcomes in different groups (B). (C) Distribution of the different interictal activity types in the ANT across different categories. In the group (Ipsi‐) TLE, the patient with both spike and HFO is represented by HFO only, and the patient with both S spike and I spike is represented by I spike only; in the group (Ipsi‐) ETLE, the patients with both α‐rhythmic activities and slow‐wave are represented by α‐rhythmic only. (D) Distribution of the different seizure onset types in the ANT across different categories. Ipsi‐, ANT hypometabolism side was ipsilateral to the EZ; con‐, the ANT hypometabolism side was contralateral to the EZ; P, all patients; S + H, patients with spike and HFO; S − w + α, patients with slow‐wave and α‐rhythmic activity.

Figure 3

Reconstruction of the depth electrodes and recording of interictal activities in the ANT and SOZ in a patient with TLE (patient 13). (A, C, E) Reconstruction in 2D and 3D views of the depth electrodes in the ANT (yellow) and SOZ (green); the red points are the contacts in the ANT. (B, D, F) PET‐MRI and 3D view of the ANT; the red contacts are located in the ANT region. (G) Interictal activities of the SOZ and ANT; HFO (black triangle) and synchronous spikes (black circle) were recorded in the ANT. The time interval of the beginning of the synchronous spike between the SOZ (red vertical line) and ANT (green vertical line) was 21 and 28 msec, respectively (zoomed red boxes). The bottom of this image is the time–frequency analysis of the interictal activities in the SOZ and ANT corresponding to the blue and red boxes. L, left.

Figure 4

Reconstruction of the depth electrodes and recording of interictal activities in the ANT and SOZ in a patient with ETLE (patient 18). (A, C, E) Reconstruction (in 2D and 3D views) of the depth electrodes in the ANT (yellow) and SOZ (green); the red points are the contacts in the ANT. (B, D, F) PET‐MRI and 3D view of the ANT; the red contacts are located in the ANT. (G) Interictal activities of the SOZ and ANT; slow‐wave (black triangle) and α‐rhythmic activities (black circle) were recorded in the ANT. The bottom of this image is the time–frequency analysis of the interictal activities in the ANT corresponding to the blue and red boxes. L, left.

Figure 5

Two patterns of the spike in the ANT. Interictal activities of the SOZ and ANT of patient 17; synchronous (black circle) and independent (black square) spikes were recorded. The time interval of the beginning of the S‐spike between the SOZ (red vertical line) and ANT (green vertical line) was 20 msec; an independent spike (purple vertical line) in the ANT was recorded (zoomed red box). Image reconstruction revealed that the second contact in the ANT was close to the thalamostriate veins, and the discharge rhythm was synchronous with the heart rate.

Figure 6

Two patterns of the ictal interval between SOZ and ANT, and examples of the seizure onset types of the ANT. (A) Immediate pattern: the seizure onset between the SOZ (red boxes) and ANT (blue boxes) almost simultaneously. (B) Delayed patterns: the seizure onset between the SOZ (red boxes) and ANT (blue boxes) shows a longer interval, about 8 sec. Examples of seizure onset types of the ANT and their time–frequency analysis: LVFA (C), RS (D) and theta (E). (F) There was no obvious evolution of activities in the ANT during ictal evolution in the SOZ.