Non-verbal auditory cognition in patients with temporal epilepsy before and after anterior temporal lobectomy

Abstract

For patients with pharmaco-resistant temporal epilepsy, unilateral anterior temporal lobectomy (ATL) - i.e. the surgical resection of the hippocampus, the amygdala, the temporal pole and the most anterior part of the temporal gyri - is an efficient treatment. There is growing evidence that anterior regions of the temporal lobe are involved in the integration and short-term memorization of object-related sound properties. However, non-verbal auditory processing in patients with temporal lobe epilepsy (TLE) has raised little attention. To assess non-verbal auditory cognition in patients with temporal epilepsy both before and after unilateral ATL, we developed a set of non-verbal auditory tests, including environmental sounds. We could evaluate auditory semantic identification, acoustic and object-related short-term memory, and sound extraction from a sound mixture. The performances of 26 TLE patients before and/or after ATL were compared to those of 18 healthy subjects. Patients before and after ATL were found to present with similar deficits in pitch retention, and in identification and short-term memorisation of environmental sounds, whereas not being impaired in basic acoustic processing compared to healthy subjects. It is most likely that the deficits observed before and after ATL are related to epileptic neuropathological processes. Therefore, in patients with drug-resistant TLE, ATL seems to significantly improve seizure control without producing additional auditory deficits.

Keywords: audition; environmental sounds; epilepsy; identification; resection; short-term memory; temporal lobe.

Figure 1

Unilateral anterior temporal lobectomy: usual extent of resection. Post-operative MRI scans: (A) para-sagittal slice; (B) horizontal slice through the temporo-mesial structures; and (C) horizontal slice through the superior temporal gyrus (most superior aspect of the anterior temporal polectomy). The removal of the most anterior part of the superior temporal gyrus (planum polare) can extend more or less posteriorly according to the patient, but never encroached into the Heschl's gyrus. HG, Heschl's gyrus (red); STG, superior temporal gyrus (orange), green arrow: hippocampectomy, yellow star, anterior temporal polectomy.

Figure 2

Mean percentage of correct responses and standard error obtained for each auditory test in each group (PRE in orange, POST in brown and C in white). The significant differences between groups (Mann–Whitney tests) are indicated (*P < 0.05, **P < 0.01, ***P < 0.001). C, control group (n = 18); DETECT, detection; IDENTIF, identification; MEM, short-term memorization; PT, pure tones; PRE, preoperatively tested patient group (n = 11); POST, postoperatively tested patient group (n = 23).

Figure 3

Mean percentage of correct responses and standard error obtained before (in orange) and after (in brown) surgery in the PRE-POST group (n = 8), for each auditory test. No significant difference (Wilcoxon tests) has been found between mean percentage of correct responses before and after surgery. DETECT, detection; IDENTIF, identification; MEM, short-term memorization; PT, pure tones.

Figure 4

Mean percentage of correct responses and standard error obtained for each auditory test in sub-groups of the POST group. (A) The POST group was fractionated into two sub-groups according to the STG resection extent: POST patients with a STG resection equal to 2 cm (orange, n = 11) and POST patients with a STG resection superior or equal to 2.5 cm (brown, n = 11). The only significant difference between these two groups (Mann–Whitney tests) is indicated (*P < 0.05). (B) The POST group was fractionated into two sub-groups according to the postoperative delay: POST patients tested after a short delay between 3 and 4 months (orange, n = 9) and POST patients tested after a long delay superior to 2 years (brown, n = 11). No significant difference (Mann–Whitney tests) has been found between these two groups. DETECT, detection; IDENTIF, identification; MEM, short-term memorization; PT, pure tones; POST, postoperatively tested patients.

Figure 5

Mean percentage and standard error of the different types of incorrect responses in the semantic identification test, in each group (PRE in orange, POST in brown and C in white). Errors could be either acoustically and semantically related to the correct answer, or only acoustically related, or only semantically related, or not related at all, or due to an absence of response. The only significant difference between groups (Mann–Whitney tests) is indicated (*P < 0.05). C, control group (n = 18); PRE, preoperatively tested patient group (n = 11); POST, postoperatively tested patient group (n = 23).