Revealing the Dynamic Modulations That Underpin a Resilient Neural Network for Semantic Cognition: An fMRI Investigation in Patients With Anterior Temporal Lobe Resection

Abstract

One critical feature of any well-engineered system is its resilience to perturbation and minor damage. The purpose of the current study was to investigate how resilience is achieved in higher cognitive systems, which we explored through the domain of semantic cognition. Convergent evidence implicates the bilateral anterior temporal lobes (ATLs) as a conceptual knowledge hub. While bilateral damage to this region produces profound semantic impairment, unilateral atrophy/resection or transient perturbation has a limited effect. Two neural mechanisms might underpin this resilience to unilateral ATL damage: 1) the undamaged ATL upregulates its activation in order to compensate; and/or 2) prefrontal regions involved in control of semantic retrieval upregulate to compensate for the impoverished semantic representations that follow from ATL damage. To test these possibilities, 34 postsurgical temporal lobe epilepsy patients and 20 age-matched controls were scanned whilst completing semantic tasks. Pictorial tasks, which produced bilateral frontal and temporal activation, showed few activation differences between patients and control participants. Written word tasks, however, produced a left-lateralized activation pattern and greater differences between the groups. Patients with right ATL resection increased activation in left inferior frontal gyrus (IFG). Patients with left ATL resection upregulated both the right ATL and right IFG. Consistent with recent computational models, these results indicate that 1) written word semantic processing in patients with ATL resection is supported by upregulation of semantic knowledge and control regions, principally in the undamaged hemisphere, and 2) pictorial semantic processing is less affected, presumably because it draws on a more bilateral network.

Figure 1.

Examples of stimuli from the 4 semantic conditions. Stimuli were presented as pictures or written words.

Figure 2.

Resection overlap map for the 17 left and 17 right TLE patients. Overlap of the resection areas defined by the Seghier et al. (Seghier et al. 2008) method. Left TLE patients overlap is shown on the right of the image, right TLE patients overlap is shown on the left of the image. Color bars indicate the number of patients with resection in that area. Warmer colors = greater overlap, cooler colors = less overlap.

Figure 3.

Whole brain results for the 2 semantic tasks. (A) Whole brain maps for the written word > scrambled word contrast for the 2 control conditions (Top: Matched—red, Speeded—green) and the 2 TLE patient groups (Bottom: left TLE—blue, right TLE—red). Resection areas for the 2 patients groups are shown in cyan; the resection area for the right TLE group is not displayed on the ventral view to illustrate the right vATL activation for the left TLE group. (B) Whole brain maps for the picture > scrambled picture contrast.

Figure 4.

A priori ROI results for the picture and written word semantic tasks. Contrast estimates for each task are shown over the relevant baseline condition for the left and right TLE patients and the 2 control participant conditions (Matched vs. Speeded). Error bars denote standard error. vATL coordinates taken from Binney et al. (2010), IFG (triangularis) coordinates taken from Noonan et al. (2013), IFG (orbitalis) coordinates taken from Badre et al. (2005)—ROI positions are shown in the top right panel. “X” indicates where data are unavailable due to surgical resection. Full line = significant differences between the left or right TLE group and the Controls (Matched) condition, dashed line = significant differences between the 2 control conditions (Matched vs. Speeded).