Semantic memory is impaired in patients with unilateral anterior temporal lobe resection for temporal lobe epilepsy

Abstract

Contemporary clinical and basic neuroscience studies have increasingly implicated the anterior temporal lobe regions, bilaterally, in the formation of coherent concepts. Mounting convergent evidence for the importance of the anterior temporal lobe in semantic memory is found in patients with bilateral anterior temporal lobe damage (e.g. semantic dementia), functional neuroimaging and repetitive transcranial magnetic stimulation studies. If this proposal is correct, then one might expect patients with anterior temporal lobe resection for long-standing temporal lobe epilepsy to be semantically impaired. Such patients, however, do not present clinically with striking comprehension deficits but with amnesia and variable anomia, leading some to conclude that semantic memory is intact in resection for temporal lobe epilepsy and thus casting doubt over the conclusions drawn from semantic dementia and linked basic neuroscience studies. Whilst there is a considerable neuropsychological literature on temporal lobe epilepsy, few studies have probed semantic memory directly, with mixed results, and none have undertaken the same type of systematic investigation of semantic processing that has been conducted with other patient groups. In this study, therefore, we investigated the semantic performance of 20 patients with resection for chronic temporal lobe epilepsy with a full battery of semantic assessments, including more sensitive measures of semantic processing. The results provide a bridge between the current clinical observations about resection for temporal lobe epilepsy and the expectations from semantic dementia and other neuroscience findings. Specifically, we found that on simple semantic tasks, the patients' accuracy fell in the normal range, with the exception that some patients with left resection for temporal lobe epilepsy had measurable anomia. Once the semantic assessments were made more challenging, by probing specific-level concepts, lower frequency/more abstract items or measuring reaction times on semantic tasks versus those on difficulty-matched non-semantic assessments, evidence of a semantic impairment was found in all individuals. We conclude by describing a unified, computationally inspired framework for capturing the variable degrees of semantic impairment found across different patient groups (semantic dementia, temporal lobe epilepsy, glioma and stroke) as well as semantic processing in neurologically intact participants.

Figure 1

The puzzle of semantic memory in resection for TLE. (A) An example axial MRI for a patient with semantic dementia, with clear bilateral anterior temporal lobe atrophy (orange arrows) underpinning the patient's demonstrable semantic impairment. (B) A comparable axial slice from a patient following anterior temporal lobe unilateral resection for TLE (red arrow). The red region on the lateral view shows the resected area. This overlaps with the anterior temporal lobe regions (1 and 2 in C) activated by normal subjects in our functional MRI semantic studies (Binney et al., 2010) and also with the region (5) that we have stimulated with repetitive transcranial magnetic stimulation in normal participants to produce a selective semantic effect (Pobric et al., 2007; 2010; Lambon Ralph et al., 2009).

Figure 2

Comparison of timed synonym versus number judgements. Dashed lines denote the boundary of control performance (control mean −2 SD for accuracy, or control mean +2 SD for speed).

Figure 3

Influence of frequency and imageability on synonym judgement performance. rTLE = resection for TLE.

Figure 4

Performance on timed picture naming. Dashed line denotes the boundary of control performance (control mean −2 SD for accuracy, or control mean +2 SD for speed).

Figure 5

Performance on specific-level semantic concepts. Dashed line denotes the boundary of control performance (control mean −2 SD for accuracy, or control mean +2 SD for speed).