Auditory Target and Novelty Processing in Patients with Unilateral Hippocampal Sclerosis: A Current-Source Density Study

Abstract

The capacity to respond to novel events is crucial for adapting to the constantly changing environment. Here, we recorded 29-channel Event Related Brain Potentials (ERPs) during an active auditory novelty oddball paradigm and used for the first time Current Source Density-transformed Event Related Brain Potentials and associated time-frequency spectra to study target and novelty processing in a group of epileptic patients with unilateral damage of the hippocampus (N = 18) and in healthy matched control participants (N = 18). Importantly, we used Voxel-Based Morphometry to ensure that our group of patients had a focal unilateral damage restricted to the hippocampus and especially its medial part. We found a clear deficit for target processing at the behavioral level. In addition, compared to controls, our group of patients presented (i) a reduction of theta event-related synchronization (ERS) for targets and (ii) a reduction and delayed P3a source accompanied by reduced theta and low-beta ERS and alpha event-related synchronization (ERD) for novel stimuli. These results suggest that the integrity of the hippocampus might be crucial for the functioning of the complex cortico-subcortical network involved in the detection of novel and target stimuli.

Figure 1

Voxel-Based Morphometry comparison between groups: (A) control > right TLE + UHS patients and (B) control > left TLE + UHS. Both groups of patients showed a decreased hippocampal grey matter compared to healthy participants. Results are shown in red-yellow at an auxiliary p < 0.005 uncorrected threshold at the voxel level (main peaks in both clusters survived a Family-wise error Correction for Small Volume p < 0.05 threshold). Neurological convention is used with Montreal Neurological Institute (MNI) coordinates at the bottom right of each slice. R, Right Hemisphere; L, Left hemisphere.

Figure 2

Grand mean CSD waveforms for standard (grey line), target (black line) and novel (red line), at midline electrodes (Fz, Cz, and Pz), from –100 to 800 ms, for both the control and the TLE-UHS group. Grey areas indicate the time-windows considered for the analyses. Difference waveforms associated to the target minus standard (black line) and novel minus standard (red line) are showed. Bottom part: scalp distribution of the P3b source (Target minus standard, −24/24 μV/cm²), and of the P3a source (Novel minus standard, −24/24 μV/cm²).

Figure 3

Grand mean CSD event-related spectral perturbation representing changes in power with respect to baseline of standard, target, and novel stimuli at midline electrodes, for the control (left) and the TLE-UHS group (right). The increase/decrease of power is represented from −100 to 800 ms. The black squares indicate the time-windows in the different frequency bands considered for the analyses. Note that standard stimuli elicited significant low-beta ERS and alpha ERD when compared to the baseline. These differences are clearly visible with a reduced scale. Differences in power between target minus standard, and between novel minus standard are depicted at the bottom of the figure. The power distributions of the theta (4–8 hz), alpha (8–12 hz), and low-beta (12–15 hz) activities for target minus standard and for novel minus standard are depicted.