SEEG-white matter stimulation reveals a white matter pathway supporting multimodal semantics
Poster No:
729
Submission Type:
Abstract Submission
Authors:
Davide Giampiccolo1, Ningfei Li2, Alejandro Granados Martinez3, Aidan O’Keeffe4, Lawrence Binding1, Joana Oliveira1, Vladimir Litvak1, Neil Burgess5, Umesh Vivekananda1, Andrew McEvoy6, John Duncan7, Beate Diehl1, Anna Miserocchi6, Fahmida Chowdhury1
Institutions:
1UCL Queen Square Institute of Neurology, London, United Kingdom, 2Charité – Universitätsmedizin Berlin, Berlin, Germany, 3King's College London, London, United Kingdom, 4University of Notthingham, Notthingham, United Kingdom, 5UCL Institute of Cognitive Neuroscience, London, United Kingdom, 6National Hospital for Neurology and Neurosurgery, London, United Kingdom, 7UCL Queen Square Institute of Neurology/National Hospital for Neurology and Neurosurgery, London, United Kingdom
First Author:
Co-Author(s):
John Duncan
UCL Queen Square Institute of Neurology/National Hospital for Neurology and Neurosurgery
London, United Kingdom
UCL Queen Square Institute of Neurology/National Hospital for Neurology and Neurosurgery
London, United Kingdom
Introduction:
Every day, we perform meaningful actions that rely on semantics such as stopping at a red light, recognizing a friend's voice, or selecting the right key for a door. Despite its ubiquity, however, how semantics is organized in the brain at cortical and subcortical level remains poorly understood. The inferior fronto-occipital fasciculus (IFOF) is a long-range white matter tract linking the frontal lobe to parietal, posterior temporal, and occipital cortices (Curran, 1909). Historically associated with the ventral language stream (Tremblay and Dick, 2012), its role has expanded to include executive control functions such as attention, motor cognition, memory, and emotion recognition (Herbet and Duffau, 2020). To examine IFOF's role in semantics, we developed a method combining high-resolution tractography with stereoelectroencephalography (SEEG) in epilepsy patients which leverages SEEG contacts in white matter to perform hypothesis-driven, task-specific tract stimulation with excellent test-retest reliability.
Methods:
We included 16 patients undergoing SEEG for drug-resistant epilepsy (6 left hemisphere, 7 right hemisphere, 3 bilateral). Preoperative high-resolution tractography (1.6 mm isotropic, 118 b-values, 33 b0) was performed. SEEG electrode contacts in white matter-specifically the IFOF (82 contact pairs)-were targeted for stimulation during a 4-second task with acoustic cues. Stimulation parameters included 50 Hz, biphasic pulses, and intensities ranging from 0.5 to 6 mA. Patients completed a neuropsychological battery assessing verbal language, visual semantics, motor cognition and emotion recognition. A total of 3,653 items were presented. Linear regression analysed task impairments and induced phenomena associated with IFOF stimulation.
·Fig. 1. Flow-chart of implantation and IFOF contacts selection
Results:
Stimulation of the IFOF significantly impaired picture naming (p < 0.001), visual semantics (p < 0.001), emotion recognition (p < 0.001), and tool use (p < 0.001). These impairments consistently occurred at different locations along the IFOF within individual patients suggesting this could be evoked at different location of the same tract. Further, IFOF stimulation impacted multiple tasks in the same contacts in 75% of electrodes as compared to only 25% that disrupted a single task (p < 0.001), thus suggesting a common computation among tested functions subserved by this tract. Finally, IFOF stimulation impacted more broadly task-directed perception (9/16 patients experienced visual or auditory hallucinations) or action (6/16 patients experienced perseverations): which was significantly associated with the IFOF when compared to all others stimulation sites (p < 0.001).
·Fig. 2. White matter stimulation in IFOF contacts in P10
Conclusions:
While IFOF stimulation affects language (Duffau, 2005), its broader, multimodal impact on semantics-including visual feature integration and semantic reasoning-aligns with the semantic control network proposed by the controlled semantic cognition framework (Lambon Ralph, 2016; Jackson, 2022). Beside this, we describe SEEG-based white matter stimulation as a powerful approach to disentangle tract-specific contribution to behaviour.
Brain Stimulation:
Invasive Stimulation Methods Other
Higher Cognitive Functions:
Executive Function, Cognitive Control and Decision Making 1
Language:
Language Comprehension and Semantics
Modeling and Analysis Methods:
Connectivity (eg. functional, effective, structural)
Neuroanatomy, Physiology, Metabolism and Neurotransmission:
White Matter Anatomy, Fiber Pathways and Connectivity 2
Keywords:
Atlasing
Cognition
Epilepsy
Sub-Cortical
White Matter
Other - Stereoencephalography
1|2Indicates the priority used for review
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2) Dick, A. S., & Tremblay, P. (2012). Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. Brain, 135(12), 3529-3550.
3) Herbet, G., & Duffau, H. (2020). Revisiting the functional anatomy of the human brain: toward a meta-networking theory of cerebral functions. Physiological Reviews, 100(3), 1181-1228.
4) Duffau, H., Gatignol, P., Mandonnet, E., Peruzzi, P., Tzourio-Mazoyer, N., & Capelle, L. (2005). New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain, 128(4), 797-810
5) Lambon Ralph, M. A.., Jefferies, E., Patterson, K., & Rogers, T. T. (2017). The neural and computational bases of semantic cognition. Nature reviews neuroscience, 18(1), 42-55.
6) Jackson, R. L., Rogers, T. T., & Lambon Ralph, M. A. (2021). Reverse-engineering the cortical architecture for controlled semantic cognition. Nature human behaviour, 5(6), 774-786.