Abstract
The presence and degree of specialization between the anterior temporal lobes (ATLs) is a key issue in debates about the neural architecture of semantic memory. Here, we comprehensively assessed multiple aspects of semantic cognition in a large group of postsurgical temporal lobe epilepsy (TLE) patients with left versus right anterior temporal lobectomy (n = 40). Both subgroups showed deficits in expressive and receptive verbal semantic tasks, word and object recognition, naming and recognition of famous faces and perception of faces and emotions. Graded differences in performance between the left and right groups were secondary to the overall mild semantic impairment; primarily, left resected TLE patients showed weaker performance on tasks that required naming or accessing semantic information from a written word. Right resected TLE patients were relatively more impaired at recognizing famous faces as familiar, although this effect was observed less consistently. These findings unify previous partial, inconsistent results and also align directly with fMRI and transcranial magnetic stimulation results in neurologically intact participants. Taken together, these data support a model in which the 2 ATLs act as a coupled bilateral system for the representation of semantic knowledge, and in which graded hemispheric specializations emerge as a consequence of differential connectivity to lateralized speech production and face perception regions.
Highlights
Semantic memory refers to our knowledge for the meanings of words, objects, people, and emotions (Lambon Ralph 2014; Lambon Ralph et al 2017)
The anterior temporal lobes (ATLs) have been implicated as a transmodal representational “hub” for conceptual knowledge, with strong supportive data reported from patients with semantic dementia (SD) (Snowden et al 1989; Mummery et al 2000; Galton et al 2001; Mion et al 2010; Lambon Ralph et al 2012), functional neuroimaging (Binney et al 2010; Visser et al 2010, 2012) and neurostimulation studies in healthy individuals (Pobric et al 2007, 2010), and cortical-grid neurophysiological investigations (Shimotake et al 2014)
The only instance where resection volume was significantly correlated with behavioral performance and changed the main effect was for accuracy performance on the face-description matching test: before accounting for resection volume there was no group difference between the left and right temporal lobe epilepsy (TLE) patients (F[1, 33] = 0.09, P = 0.76), after accounting for this there was a marginal effect driven by the left TLE group performing less accurately than the right TLE group (Group: F[2, 32] = 2.33, P = 0.14; Covariate of resection volume: F[1, 32] = 4.14, P = 0.05). This investigation comprehensively mapped the status of verbal and nonverbal semantic processing and related abilities in TLE patients with unilateral left versus right ATL resection
Summary
Semantic memory (or conceptual knowledge) refers to our knowledge for the meanings of words, objects, people, and emotions (Lambon Ralph 2014; Lambon Ralph et al 2017). The ATL atrophy in SD can be asymmetric in early cases, the disease is inherently bilateral and the individual contributions of left versus right ATL are hard to infer precisely from studies of this patient group. En bloc resection for the treatment of temporal lobe epilepsy (TLE) provides an entirely unilateral model of left versus right ATL function. The current study comprehensively investigated a large-scale comparative case-series of patients with left versus right ATL resection
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