Hippocampal, amygdala, and neocortical synchronization of theta rhythms is related to an immediate recall during rey auditory verbal learning test

Abstract

It is well known that theta rhythms (3-8 Hz) are the fingerprint of hippocampus, and that neural activity accompanying encoding of words differs according to whether the items are later remembered or forgotten ["subsequent memory effect" (SME)]. Here, we tested the hypothesis that temporal synchronization of theta rhythms among hippocampus, amygdala, and neocortex is related to immediate memorization of repeated words. To address this issue, intracerebral electroencephalographic (EEG) activity was recorded in five subjects with drug-resistant temporal lobe epilepsy (TLE), under presurgical monitoring routine. During the recording of the intracerebral EEG activity, the subjects performed a computerized version of Rey auditory verbal learning test (RAVLT), a popular test for the clinical evaluation of the immediate and delayed memory. They heard the same list of 15 common words for five times. Each time, immediately after listening the list, the subjects were required to repeat as many words as they could recall. Spectral coherence of the intracerebral EEG activity was computed in order to assess the temporal synchronization of the theta (about 3-8 Hz) rhythms among hippocampus, amygdala, and temporal-occipital neocortex. We found that theta coherence values between amygdala and hippocampus, and between hippocampus and occipital-temporal cortex, were higher in amplitude during successful than unsuccessful immediate recall. A control analysis showed that this was true also for a gamma band (40-45 Hz). Furthermore, these theta and gamma effects were not observed in an additional (control) subject with drug-resistant TLE and a wide lesion to hippocampus. In conclusion, a successful immediate recall to the RAVLT was associated to the enhancement of temporal synchronization of the theta (gamma) rhythms within a cerebral network including hippocampus, amygdala, and temporal-occipital neocortex.

Figure 1

Magnetic resonance images of axial, coronal, and sagittal brain slices for the four subjects. These images show the location of the stick electrodes used for intracerebral electroencephalographic (EEG) recordings. The real volume of the electrode is about 10% of the displayed artifact. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 2

Intracerebral EEG rhythms (as revealed by power spectra) in the hippocampus during the encoding phase of RAVLT in the four subjects. The RAVLT included a list of 15 common words to be encoded/recalled five times. Each plot shows the intracerebral EEG power density spectra for the selected hippocampal electrode contact for each subject. Thin lines represent the average spectra across the five repetitions of each word of the RAVLT, whereas the thick line represents the mean across all 15 words and five encoding repetitions. See Methods section for further details.

Figure 3

Temporal synchronization of intracerebral EEG rhythms during the encoding/listening of words of the RAVLT in the four subjects. Each bar represents the encoding‐related theta coherence (ERCoh) for the recalled (blue) vs. unrecalled (red) words for the two theta subbands (see methods for further details). The ERCoh values are higher for the recalled than for the unrecalled words with only three exceptions (Subject 1 amygdala‐neocortex, hippocampus‐amygdala and Subject 3 amygdala‐neocortex). [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 4

Average of encoding‐related theta coherence (ERCoh) values of the four subjects referred to the recalled (blue bars) vs. unrecalled (red bars) words for the two theta subbands (see Methods section for further details). The ERCoh values are always higher for successful recalled words. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 5

Temporal synchronization of intracerebral EEG rhythms during the encoding/listening of words of the RAVLT in the five experimental subjects. Each bar represents the encoding‐related coherence (ERCoh) for the recalled (blue) vs. unrecalled (red) words for the gamma band (see Methods section for further details). [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 6

Average of encoding‐related gamma coherence (ERCoh) values of the five experimental subjects referred to the recalled (blue bars) vs. unrecalled (red bars) words for the gamma band (see Methods section for further details). [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 7

(Top) Magnetic resonance images of axial, coronal, and sagittal brain slices for a control TLE subject who had received resection of portions of right hippocampus, amygdala, and temporal neocortex due to pharmacologically resistant seizures. These images show the location of the stick electrodes used for intracerebral EEG recordings. The real volume of the electrode is about 10% of the displayed artifact. (middle) Intracerebral EEG power density spectrum at the hippocampal electrode contacts during the encoding phase of the RAVLT in the control TLE subject. Thin lines represent the average spectra across the five repetitions of each word of the RAVLT, while the tick line represents the mean across all 15 words and five encoding repetitions. (bottom) Temporal synchronization of the theta and gamma rhythms (ERCoh) between hippocampus and temporal‐occipital neocortex in the control subject during the encoding phase of the RAVLT. Each bar represents the encoding‐related theta ERCoh for the recalled (blue) vs. unrecalled (red) words. The highest ERCoh corresponds to unrecalled words. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]