Direct Exploration of the Role of the Ventral Anterior Temporal Lobe in Semantic Memory: Cortical Stimulation and Local Field Potential Evidence From Subdural Grid Electrodes

Abstract

Semantic memory is a crucial higher cortical function that codes the meaning of objects and words, and when impaired after neurological damage, patients are left with significant disability. Investigations of semantic dementia have implicated the anterior temporal lobe (ATL) region, in general, as crucial for multimodal semantic memory. The potentially crucial role of the ventral ATL subregion has been emphasized by recent functional neuroimaging studies, but the necessity of this precise area has not been selectively tested. The implantation of subdural electrode grids over this subregion, for the presurgical assessment of patients with partial epilepsy or brain tumor, offers the dual yet rare opportunities to record cortical local field potentials while participants complete semantic tasks and to stimulate the functionally identified regions in the same participants to evaluate the necessity of these areas in semantic processing. Across 6 patients, and utilizing a variety of semantic assessments, we evaluated and confirmed that the anterior fusiform/inferior temporal gyrus is crucial in multimodal, receptive, and expressive, semantic processing.

Word meaning in the ventral visual path: a perceptual to conceptual gradient of semantic coding

“…Neuroimaging studies focusing on regions in anterior temporal cortex which are activated during semantic tasks also show that semantic 23 proximity of words belonging to the same semantic category correlates with the patterns of activity in left perirhinal cortex (Bruffaerts et al, 2013). Virtual lesions through TMS and cortical stimulation also indicate that interfering with ATL generates trouble in a variety of semantic tasks (Pobric et al, 2010;Shimotake et al, 2014).…”

The Semantic Network at Work and Rest: Differential Connectivity of Anterior Temporal Lobe Subregions

“…The data have been realigned and normalized to MNI space to compute the average TSNR for the group; however, covariates have not been removed because this artificially changes the TSNR. The map is set at a threshold of 40, which is considered to be the minimum TSNR required to detect differences in signal reliably (Murphy et al, 2007;Simmons et al, 2010;Wang et al, 2013), and is displayed as a range from 40 (dark blue) to 200 (bright green). Use of the dual-echo technique meant signal reached the minimum threshold throughout the ATL and inferior frontal regions, with most of the brain far exceeding this with values Ͼ200.…”

“…The aSTG is activated when processing meaningful environmental sounds and intelligible speech, suggesting a role in accessing meaning from auditory input (Scott et al, 2000;Spitsyna et al, 2006;Visser and Lambon Ralph, 2011). In addition, visually presented language can activate the aSTG, perhaps due to the visual language system commandeering the evolutionarily earlier auditory system and automatic conversion of orthography to phonology (Spitsyna et al, 2006;Skipper et al, 2011). Alternatively, both may involve a more general process, such as the use of sequential input to compute timeinvariant meanings .…”

“…Determining the pattern of connectivity across the ATL allows identification of distinct subregions and helps inform their function. Prior investigations of the connectivity of circumscribed polar and lateral ATL regions (Simmons et al, 2010;Turken and Dronkers, 2011;Pascual et al, 2015;Mesulam et al, 2014) were unable to demonstrate this pattern of connectivity for two key reasons. First, only one location was studied so comparison was not possible.…”

“…However, cytoarchitectural differences within the ATL hint at the presence of distinct, yet graded subregions (Brodmann, 2006;Ding et al, 2009). Recent neuroimaging, neurostimulation, electrophysiology, and detailed patient assessments suggest that the center point of the multimodal hub region sits within the ventral ATL (vATL; Lüders et al, 1986;Lüders et al, 1991;Pobric et al, 2007;Butler et al, 2009;Lambon Ralph et al, 2009;Binney et al, 2010;Mion et al, 2010;Visser and Lambon Ralph, 2011;Shimotake et al, 2015). Other ATL subregions may differ from the vATL in terms of function and connectivity in a graded fashion (Visser and Lambon Ralph, 2011;Binney et al, 2012).…”