Extratemporal functional connectivity impairments at rest are related to memory performance in mesial temporal epilepsy

Abstract

Mesial temporal lobe epilepsy (MTLE) is the most frequent form of focal epilepsy. At rest, there is evidence that brain abnormalities in MTLE are not limited to the epileptogenic region, but extend throughout the whole brain. It is also well established that MTLE patients suffer from episodic memory deficits. Thus, we investigated the relation between the functional connectivity seen at rest in fMRI and episodic memory impairments in MTLE. We focused on resting state BOLD activity and evaluated whether functional connectivity (FC) differences emerge from MTL seeds in left and right MTLE groups, compared with healthy controls. Results revealed significant FC reductions in both patient groups, localized in angular gyri, thalami, posterior cingulum and medial frontal cortex. We found that the FC between the left non-pathologic MTL and the medial frontal cortex was positively correlated with the delayed recall score of a non-verbal memory test in right MTLE patients, suggesting potential adaptive changes to preserve this memory function. In contrast, we observed a negative correlation between a verbal memory test and the FC between the left pathologic MTL and posterior cingulum in left MTLE patients, suggesting potential functional maladaptative changes in the pathologic hemisphere. Overall, the present study provides some indication that left MTLE may be more impairing than right MTLE patients to normative functional connectivity. Our data also indicates that the pattern of extra-temporal FC may vary as a function of episodic memory material and each hemisphere's capacity for cognitive reorganization.

Keywords: connectivity; epilepsy; episodic memory; fMRI; functional reorganization; resting state.

Figure 1

Right (red) and left (blue) MTL seed regions. They are displayed on the MNI template. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Whole brain functional connectivity map with the right MTL seed for the control group (A), the RMTLE group (B), and the LMTLE group (C). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 3

Whole brain functional connectivity map with the left MTL seed for the control group (A), the RMTLE group (B), and the LMTLE group (C). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 4

Regions showing reduced functional connectivity with either the right MTL Seed (A) or the left MTL Seed (B) in patients, relative to controls (see Tables 2 and 3, respectively). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 5

Correlation between FC values with the left seed in RMTLE (A) and in LMTLE (B) with episodic memory scores. A: Reduced FC between left seed (blue) and medial frontal cortex (green, x = −14, y = 56, z = −10; also see Table 3) in RMTLE patients compared with controls (left bottom plot); positive correlation between FC values between these two regions and the FM II (right bottom plot, Spearman correlation, r = 0.78; P = 0.0045). The normative values of the controls are shown through the green data point where the y axis indicates the average FC value of the controls' data and the x axis is the normative value of age‐matched healthy controls of the FM II score [Wechsler, 1997]. Bars indicate standard deviation. B: Reduced FC between left seed (blue) and posterior cingulum (green, x = 2, y = −36, z = 32; also see Table 3) in LMTLE patients compared with controls (left bottom plot); negative correlation between the FC values between these two regions and the ratio LM II/ LM I (right bottom plot, Spearman correlation, r = −0.93; P = 0.001). The normative values of the controls are shown through the green data point where the y axis indicates the average FC value of the controls' data and the x axis is the normative value of age‐matched healthy controls of the LM II/LM I ratio score (Wechsler, 1997). Bars indicate standard deviation. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]