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

Cerebral Cortex, October 2015;25: 3802–3817 doi: 10.1093/cercor/bhu262 Advance Access Publication Date: 9 December 2014 Original Article ORIGINAL ARTICLE Direct Exploration of the Role of the Ventral Akihiro Shimotake1, Riki Matsumoto2, Taiji Ueno5, Takeharu Kunieda3, Satoru Saito5,6, Paul Hoffman5, Takayuki Kikuchi3, Hidenao Fukuyama4, Susumu Miyamoto3, Ryosuke Takahashi1, Akio Ikeda2, and Matthew A. Lambon Ralph5 1 Department of Neurology, 2Department of Epilepsy, Movement Disorders and Physiology, 3Department of Neurosurgery, 4Human Brain Research Center, Kyoto University Graduate School of Medicine, Kyoto, Japan, 5 Neuroscience and Aphasia Research Unit (NARU), School of Psychological Sciences, University of Manchester, Manchester, UK, and 6Department of Cognitive Psychology in Education, Graduate School of Education, Kyoto University, Kyoto, Japan Address correspondence to Riki Matsumoto, MD, PhD, Department of Epilepsy, Movement Disorders and Physiology, Kyoto University Graduate School of Medicine, 54 Kawaharacho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan. Email: ; Prof. Matthew A. Lambon Ralph, Neuroscience and Aphasia Research Unit (NARU), School of Psychological Sciences (Zochonis Building), Brunswick Street, Manchester M13 9PL, UK. Email: Akio Ikeda and Matthew A. Lambon Ralph contributed equally to this work and thus are joint senior authors. 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. Key words: anterior fusiform, basal temporal language area, semantic memory, subdural electrodes, ventral anterior temporal lobe © The Author 2014. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Anterior Temporal Lobe in Semantic Memory: Cortical Stimulation and Local Field Potential Evidence From Subdural Grid Electrodes Semantic Cognition and the Ventral Anterior Temporal Lobe Introduction | 3803 et al. 2000; Visser et al. 2010). Likewise, repetitive transcranial magnetic stimulation (rTMS) has been used to demonstrate the necessity of left and right lateral ATL areas to multimodal semantic processing in neurologically intact participants (Pobric et al. 2007, 2010a; Lambon Ralph et al. 2009), but, due to its neuroanatomical location, it is impossible to stimulate the ventral ATL directly using TMS. There are some strong hints in the literature that the ventral ATL might play an important role in multimodal semantic representation. Although this region is primarily considered to be the apex of the ventral visual stream (Albright 2012), it is becoming increasingly apparent from connectivity studies and functional neuroimaging that this area is much more transmodal in character. First, not only is the ventral ATL (vATL) connected to primary visual areas, but it is also connected to other temporal, limbic, and frontal regions [as shown in: primate injectionbased tractography (Morán et al. 1987); human white-matter tractography (e.g., Binney et al. 2012); human resting-state fMRI connectivity studies (e.g., Pascual et al. 2015); and human cortico-cortical connectivity (e.g., Matsumoto et al. 2004)]. Secondly, recent fMRI studies, designed to minimize the technical and methodological issues associated with successful imaging of this region, have demonstrated graded variation of semantic function across the ATL reflecting the pattern of connectivity to remote modality-specific association cortices (Visser and Lambon Ralph 2011; Binney et al. 2012) and the coding of semantic category structure (Peelen and Caramazza 2012). Among other regions [for reviews, see Binder et al. (2009); Visser et al. (2010); Noonan et al. (2013)], the ventral ATL (centered on the anterior fusiform/inferior temporal gyrus, ITG: Fig. 1) is activated, irrespective of variations in task or modality—consistent with previous PET-based functional neuroimaging studies (Vandenberghe et al. 1996; Sharp et al. 2004) and raising the possibility that this area is the center point of a transmodal semantic hub (Binney et al. 2010; Visser and Lambon Ralph 2011). Selective investigation of the vATL is needed for at least 2 reasons: (1) Functional neuroimaging generates important hypotheses about the contribution of specific brain regions, but activation by itself does not demonstrate the necessity of those areas (Price and Friston 2002); (2) while the ventral ATL does exhibit early and disproportionate damage (Galton et al. 2001) and hypometabolism in SD (Mion et al. 2010), the patients’ atrophy is not isolated to this specific region (Rohrer et al. 2009). The current study directly tested the contribution of the vATL region to semantic processing through the implantation of subdural electrode grids, for the presurgical evaluation of patients with partial epilepsy and brain tumor. Unlike functional neuroimaging or TMS alone, this method offers dual unique opportunities: by placing a grid over a region of interest (ROI), it is possible not only to evaluate the functionally related cortical activity directly (evoked local field potentials, LFPs), but also to induce temporary disruption of the function at that site, within the same participant. This is not, of course, the first study ever to have used this method to probe the ventral ATL. In clinical neurosurgery, the same region has been regarded as an important language area—the basal temporal language area (BTLA)—ever since electrical stimulation of this cortical region was found to impair reading and naming (Lüders et al. 1986, 1991), and preservation of this area and its fiber pathway resulted in the better verbal memory outcome after neurosurgery (Mikuni et al. 2006). Implanted grid electrodes (...truncated)