Temporal lobe regions essential for preserved picture naming after left temporal epilepsy surgery

Binder, Jeffrey R.; Tong, Jia‐Qing; Pillay, Sara B.; Conant, Lisa L.; Humphries, Colin; Raghavan, Manoj; Mueller, Wade; Busch, Robyn M.; Allen, Linda; Gross, William L.; Anderson, Christopher T.; Carlson, Chad; Lowe, Mark J.; Langfitt, John T.; Tivarus, Madalina E.; Drane, Daniel L.; Loring, David W.; Jacobs, Monica; Morgan, Victoria L.; Allendorfer, Jane B.; Szaflarski, Jerzy P.; Bonilha, Leonardo; Bookheimer, Susan Y.; Grabowski, Thomas J.; Vannest, Jennifer; Swanson, Sara J.; study, fMRI in Anterior Temporal Epilepsy Surgery

doi:10.1111/epi.16643

Cited by 44 publications

(47 citation statements)

References 51 publications

(110 reference statements)

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“…These results together contribute to a better understanding of how semantic cognition drives word retrieval. Previous literature has suggested that the left ventral ATL and occipitotemporal regions may serve the multimodal binding involved in word meaning association (Binney et al, 2010;Pulvermüller, 2013;Forseth et al, 2018;Binder et al, 2020). However, our results revealed that the left inferior occipitotemporal region (i.e., the left OTSm or anterior VWFA) acts as a heteromodal word-meaning binding site.…”

Section: Discussioncontrasting

confidence: 82%

“…These anatomic and functional areas have long been considered heteromodal integration regions, and recent findings corroborate that posterior parts of the lateral MTG, ITG, and middle FG are centrally involved in representing lexical items independently of modalities (Forseth et al, 2018;Evans et al, 2019;Mattioni et al, 2020). Latest studies with epilepsy patients that used naming tasks to tag the word processing uncovered that the middle occipitotemporal cortex (i.e., FG and ITG) may function as lexical semantic hub and play a crucial part in associating words and their meaning (Forseth et al, 2018;Binder et al, 2020).…”

Section: Introductionmentioning

confidence: 86%

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A Heteromodal Word-Meaning Binding Site in the Visual Word Form Area under Top-Down Frontoparietal Control

Qin

Lyu

et al. 2021

J. Neurosci.

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The integral capacity of human language together with semantic memory drives the linkage of words and their meaning, which theoretically is subject to cognitive control. However, it remains unknown whether, across different language modalities and input/output formats, there is a shared system in the human brain for word-meaning binding and how this system interacts with cognitive control. Here, we conducted a functional magnetic resonance imaging experiment based on a large cohort of subjects (50 females, 50 males) to comprehensively measure the brain responses evoked by semantic processing in spoken and written word comprehension and production tasks (listening, speaking, reading, and writing). We found that heteromodal word input and output tasks involved distributed brain regions within a frontal-parietal-temporal network and focally coactivated the anterior lateral visual word form area (VWFA), which is located in the basal occipitotemporal area. Directed connectivity analysis revealed that the VWFA was invariably under significant top-down modulation of the frontoparietal control network and interacts with regions related to attention and semantic representation. This study reveals that the VWFA is a key site subserving general semantic processes linking words and meaning, challenging the predominant emphasis on this area's specific role in reading or more general visual processes. Our findings also suggest that the dynamics between semantic memory and cognitive control mechanisms during word processing are largely independent of the modalities of input or output.

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Section: Discussioncontrasting

confidence: 82%

Section: Introductionmentioning

confidence: 86%

A Heteromodal Word-Meaning Binding Site in the Visual Word Form Area under Top-Down Frontoparietal Control

Qin

Lyu

et al. 2021

J. Neurosci.

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“…It has been shown that laser ablation of the hippocampus and amygdala reduces the risk of postoperative naming impairment in comparison to standard ATL procedures. 52,59,60,61 Concordantly, we did not find a significant association between the hippocampus and naming performance, and less than 3% of voxels included in the significant cluster belonged to the hippocampus. Additionally, the percentage of the hippocampus removed or ablated was not significantly correlated with a change in BNT performance.…”

Section: Discussionsupporting

confidence: 57%

The critical role of the ventral temporal lobe in word retrieval

Snyder

Forseth

Donos

et al. 2021

Preprint

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Deficits in word retrieval are a hallmark of a variety of neurological illnesses spanning from dementia to traumatic injuries. The role of the dominant temporal lobe in fluent naming has been characterized by lesional analyses, functional imaging, and intracranial recordings, but limitations of each of these measures preclude a clear assessment of which specific constituent of the temporal lobe is critical for naming. We studied a large cohort of patients undergoing surgical resections or laser ablations of the dominant temporal lobe for medically intractable epilepsy (n=95). These techniques are exceedingly effective for seizure control but often result in language declines, particularly in confrontation naming, which can be socio-economically disabling. We used a multivariate voxel-based lesion symptom mapping analysis to localize brain regions significantly associated with visual object naming deficits. We observed that posterior inferior temporal regions, centered around the middle fusiform gyrus, were significantly associated with a decline in confrontation naming. Furthermore, we found that the posterior margin of anterior temporal lobectomies was linearly correlated to a decline in visual naming with a clinically significant decline occurring once the resection extended 6 cm from the anterior tip of the temporal lobe. We integrated these findings with electrocorticography during naming in a subset of this population and found that the majority of cortical regions whose resection was associated with a significant decline overlapped with regions that were functionally most active prior to articulation. Importantly, these loci coincide with the sites of susceptibility artifacts during echo-planar imaging, which explains why this region has not previously been implicated. Taken together, these data highlight the crucial contribution of the posterior ventral temporal cortex in lexical access and its important role in the pathophysiology of anomia following temporal lobe resections. Surgical strategies, including the use of laser ablation to target the medial temporal lobe as well as microsurgical approaches, should attempt to preserve this region to mitigate postoperative language deficits.

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“…It is widely accepted that language involves a more distributed network than Broca's and Wernicke's area and that anatomically dissociable regions exist that are specialized for specific linguistic subroutines which interactively support the construct of language (34, 39, 150, 151). Regions spanning the ventral temporal and occipital lobes and fusiform area appear to contribute heavily to recognition (primarily right hemisphere, but some left) of visual objects and faces, while coexisting areas on the left are important for naming (152)(153)(154)(155)(156). Naming itself is a complex (161)].…”

Section: Languagementioning

confidence: 99%

Cognitive and Emotional Mapping With SEEG

et al. 2021

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Mapping of cortical functions is critical for the best clinical care of patients undergoing epilepsy and tumor surgery, but also to better understand human brain function and connectivity. The purpose of this review is to explore existing and potential means of mapping higher cortical functions, including stimulation mapping, passive mapping, and connectivity analyses. We examine the history of mapping, differences between subdural and stereoelectroencephalographic approaches, and some risks and safety aspects, before examining different types of functional mapping. Much of this review explores the prospects for new mapping approaches to better understand other components of language, memory, spatial skills, executive, and socio-emotional functions. We also touch on brain-machine interfaces, philosophical aspects of aligning tasks to brain circuits, and the study of consciousness. We end by discussing multi-modal testing and virtual reality approaches to mapping higher cortical functions.

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Temporal lobe regions essential for preserved picture naming after left temporal epilepsy surgery

Cited by 44 publications

References 51 publications

A Heteromodal Word-Meaning Binding Site in the Visual Word Form Area under Top-Down Frontoparietal Control

A Heteromodal Word-Meaning Binding Site in the Visual Word Form Area under Top-Down Frontoparietal Control

The critical role of the ventral temporal lobe in word retrieval

Cognitive and Emotional Mapping With SEEG

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