Impaired action recognition in brain tumor patients induced by direct electrical stimulation
Poster No:
34
Submission Type:
Abstract Submission
Authors:
Laura de Frutos-Sagastuy1,2, Ileana Quinones3,4,5, Santiago Gil-Robles6, Iñigo Pomposo7, Garazi Bermudez7, Manuel Carreiras3,4, Lucía Amoruso3,8,4
Institutions:
1Basque Center on Cognition, Brain and Language, Donostia - San Sebastian, Gipuzkoa, 2University of the Basque Country, Bilbao, Spain, 3Basque Center on Cognition, Brain and Language, Donostia - San Sebastián, Gipuzkoa, 4Ikerbasque, Basque Foundation for Science, Bilbao, Spain, 5Biogipuzkoa Health Research Institute, San Sebastian, Spain, 6Universitary Hospital Quironsalud Madrid, Madrid, Madrid, 7BioCruces Research Institute, Bilbao, Bilbao, 8Cognitive Neuroscience Center, Buenos Aires, Argentina
First Author:
Laura de Frutos-Sagastuy
Basque Center on Cognition, Brain and Language|University of the Basque Country
Donostia - San Sebastian, Gipuzkoa|Bilbao, Spain
Basque Center on Cognition, Brain and Language|University of the Basque Country
Donostia - San Sebastian, Gipuzkoa|Bilbao, Spain
Co-Author(s):
Ileana Quinones
Basque Center on Cognition, Brain and Language|Ikerbasque, Basque Foundation for Science|Biogipuzkoa Health Research Institute
Donostia - San Sebastián, Gipuzkoa|Bilbao, Spain|San Sebastian, Spain
Basque Center on Cognition, Brain and Language|Ikerbasque, Basque Foundation for Science|Biogipuzkoa Health Research Institute
Donostia - San Sebastián, Gipuzkoa|Bilbao, Spain|San Sebastian, Spain
Manuel Carreiras
Basque Center on Cognition, Brain and Language|Ikerbasque, Basque Foundation for Science
Donostia - San Sebastián, Gipuzkoa|Bilbao, Spain
Basque Center on Cognition, Brain and Language|Ikerbasque, Basque Foundation for Science
Donostia - San Sebastián, Gipuzkoa|Bilbao, Spain
Lucía Amoruso
Basque Center on Cognition, Brain and Language|Cognitive Neuroscience Center|Ikerbasque, Basque Foundation for Science
Donostia - San Sebastián, Gipuzkoa|Buenos Aires, Argentina|Bilbao, Spain
Basque Center on Cognition, Brain and Language|Cognitive Neuroscience Center|Ikerbasque, Basque Foundation for Science
Donostia - San Sebastián, Gipuzkoa|Buenos Aires, Argentina|Bilbao, Spain
Introduction:
Intraoperative functional mapping during awake brain surgery is the first therapeutic option for tumor resection. Indeed, ~80% of these tumors involve eloquent areas, that is, regions of high functional expressivity that need to be spared from resection. This underscores the need for intraoperative sensitive tasks to map and preserve these regions, avoiding postoperative sequelae.
Classically, functional mapping has focused on overt functions in the dominant hemisphere, namely, motricity and language in the left hemisphere. However, there are other distributed functions crucial for daily life that are challenging to map but need preservation [1]. One example is action comprehension, a vital social ability supported by the Action Observation Network (AON). Neuroanatomically, the AON involves dorsal bilateral fronto-parietal regions, including the inferior frontal cortex, premotor cortex, inferior parietal lobe, and superior temporal sulcus [2]. These regions are interconnected subcortically, primarily through the superior longitudinal fasciculus (SLF) and anterior thalamic radiations [3].
Classically, functional mapping has focused on overt functions in the dominant hemisphere, namely, motricity and language in the left hemisphere. However, there are other distributed functions crucial for daily life that are challenging to map but need preservation [1]. One example is action comprehension, a vital social ability supported by the Action Observation Network (AON). Neuroanatomically, the AON involves dorsal bilateral fronto-parietal regions, including the inferior frontal cortex, premotor cortex, inferior parietal lobe, and superior temporal sulcus [2]. These regions are interconnected subcortically, primarily through the superior longitudinal fasciculus (SLF) and anterior thalamic radiations [3].
Methods:
The AON mapping task comprises a series of images depicting a model engaged in incomplete, ongoing actions. Participants must infer the overarching motor goal behind the observed movement by selecting between two alternatives (e.g., to drink or to clean). Actions are observed in naturalistic contexts that can either facilitate or hinder action recognition [4,5].
Four patients diagnosed with brain tumors in the right hemisphere underwent awake surgery for tumor resection along with intraoperative functional mapping of the AON. Patient A had a parietal cavernoma, patient B had a glioma in the insula, patient C had an insular astrocytoma and patient D had a insular glioma.
Cortical and subcortical mapping were performed by combining direct electrical stimulation (DES) with a bipolar stimulation electrode, while the patient performed the AON task. If the patient produces an error in at least 2 out of 3 non-consecutive stimulation trials, it indicates that the stimulated region has a functional role and should be preserved from resection. A trial is considered erroneous if, due to stimulation, the patient misinterprets the intentionality of the action or if the response is delayed or absent. It is also considered an error when the patient rectifies the answer only after the stimulation has ended. This task was video recorded during the course of the awake craniotomy for posterior behavioural analysis.
Four patients diagnosed with brain tumors in the right hemisphere underwent awake surgery for tumor resection along with intraoperative functional mapping of the AON. Patient A had a parietal cavernoma, patient B had a glioma in the insula, patient C had an insular astrocytoma and patient D had a insular glioma.
Cortical and subcortical mapping were performed by combining direct electrical stimulation (DES) with a bipolar stimulation electrode, while the patient performed the AON task. If the patient produces an error in at least 2 out of 3 non-consecutive stimulation trials, it indicates that the stimulated region has a functional role and should be preserved from resection. A trial is considered erroneous if, due to stimulation, the patient misinterprets the intentionality of the action or if the response is delayed or absent. It is also considered an error when the patient rectifies the answer only after the stimulation has ended. This task was video recorded during the course of the awake craniotomy for posterior behavioural analysis.
Results:
In patient A, both horizontal (SLF) and vertical (thalamocortical fibers) connectivity were consistently disrupted, leading to slowed response times and semantic errors. In patient C, cortical positive stimulation sites were identified in the insula and the roof of the ventricle of the temporal horn, resulting in delayed or incorrect responses.
·Positive stimulation sites in the Action Observation Network.
Conclusions:
Overall, our findings provide causal evidence for the role of cortical (e.g., IFG) and subcortical (e.g., SLF) AON nodes in facilitating action recognition. At the clinical level, these results validate the effectiveness of the AON task as a valuable tool for mapping social abilities in the right hemisphere, a key element that is currently missing in the surgical management of eloquent areas in the non-dominant hemisphere.
Brain Stimulation:
Direct Electrical/Optogenetic Stimulation 1
Emotion, Motivation and Social Neuroscience:
Social Cognition 2
Keywords:
Other - Action recognition; brain tumors; direct electrical stimulation; intraoperative mapping; right hemisphere
1|2Indicates the priority used for review
Provide references using author date format
Caspers, S. (2010). ALE meta-analysis of action observation and imitation in the human brain. NeuroImage 50, 1148-1167
Wang, et al. 2018. White matter pathways and social cognition. Neuroscience and biobehavioral reviews 90, 350-370.
Amoruso, L. (2016). Tracking the Time Course of Top-Down Contextual Effects on Motor Responses during Action Comprehension. Journal of Neuroscience. 36-46, pp.11590-11600.
Amoruso, L. (2020). Spatial frequency tuning of motor responses reveals differential contribution of dorsal and ventral systems to action comprehension. Proceedings of the National Academy of Sciences (PNAS), 117 (23), 13151-13161.