Homunculus Interruptus: A motor association area in the depth of the central sulcus

Jensen, Michael A.; Huang, Harvey; Valencia, Gabriela Ojeda; Klassen, Bryan T.; Boom, Max van den; Kaufmann, Timothy J.; Schalk, Gerwin; Brunner, Peter; Hermes, Dora; Worrell, Greg M; Miller, Kai J.

doi:10.1101/2022.11.20.517292

Cited by 8 publications

(15 citation statements)

References 33 publications

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“…Human speech BCI studies have suggested that the precentral gyrus between the hand and mouth effectors is essential for phonological-motoric aspects of speech planning 54 , and that speech can also be decoded from a region at the bottom of precentral gyrus 55 . Following our identification of the SCAN, human depth electrode recordings verified that a portion of M1 between the foot and hand effector regions (superior SCAN) is active during foot, hand and mouth movements, strongly supporting its integrative, wholebody function 44 .…”

Section: Human Electrophysiology Evidencementioning

confidence: 64%

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A somato-cognitive action network alternates with effector regions in motor cortex

Gordon

Chauvin

Van

et al. 2023

Nature

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199

104

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Motor cortex (M1) has been thought to form a continuous somatotopic homunculus extending down the precentral gyrus from foot to face representations1,2, despite evidence for concentric functional zones3 and maps of complex actions4. Here, using precision functional magnetic resonance imaging (fMRI) methods, we find that the classic homunculus is interrupted by regions with distinct connectivity, structure and function, alternating with effector-specific (foot, hand and mouth) areas. These inter-effector regions exhibit decreased cortical thickness and strong functional connectivity to each other, as well as to the cingulo-opercular network (CON), critical for action5 and physiological control6, arousal7, errors8 and pain9. This interdigitation of action control-linked and motor effector regions was verified in the three largest fMRI datasets. Macaque and pediatric (newborn, infant and child) precision fMRI suggested cross-species homologues and developmental precursors of the inter-effector system. A battery of motor and action fMRI tasks documented concentric effector somatotopies, separated by the CON-linked inter-effector regions. The inter-effectors lacked movement specificity and co-activated during action planning (coordination of hands and feet) and axial body movement (such as of the abdomen or eyebrows). These results, together with previous studies demonstrating stimulation-evoked complex actions4 and connectivity to internal organs10 such as the adrenal medulla, suggest that M1 is punctuated by a system for whole-body action planning, the somato-cognitive action network (SCAN). In M1, two parallel systems intertwine, forming an integrate–isolate pattern: effector-specific regions (foot, hand and mouth) for isolating fine motor control and the SCAN for integrating goals, physiology and body movement.

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Section: Human Electrophysiology Evidencementioning

confidence: 64%

“…7 and 8; see also ref. 44) to accomplish holistic, whole-body functions in the service of performing actions (Fig. 3e).…”

Section: Effector Isolation Versus Action Integrationmentioning

confidence: 99%

A somato-cognitive action network alternates with effector regions in motor cortex

Gordon

Chauvin

Van

et al. 2023

Nature

Self Cite

199

104

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“…Functional networks, such as those governing speech or movement, often contain redundancy across cortical regions which can substitute for one another to sustain behavior despite focal interruption 31 . This redundancy is a common feature of association cortices 31 , and less likely in primary cortex 16 . Such shared representation is the most probable explanation for channels that demonstrate broadband power increases (TBE +) during behavior but no obvious response to stimulation (Supp Fig 29).…”

Section: Discussionmentioning

confidence: 99%

“…Twenty cues (trials) of each movement type were shuffled in random order and move/rest trial cues were each presented for 3 seconds (Fig 2). This task was chosen based upon prior work, which has produced clear results in sEEG recordings 16 . The BCI2000 software was used for stimulus presentation and data synchronization 21 .…”

Section: Methodsmentioning

confidence: 99%

“…We describe a technique to complement existing mapping approaches by passively recording electrical signals from sEEG while patients perform simple behavioral tasks at bedside. This task-based electrophysiological (TBE) mapping extends an approach originally developed for brain surface electrocorticography measurements 13-15 , that we initially used in sEEG for the scientific exploration of the brain circuitry of movement 16 . Here we illustrate how TBE mapping using sEEG can be applied in a wide variety of patients and pathologies for the functional mapping of speech and sensorimotor networks.…”

Section: Introductionmentioning

confidence: 97%

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Functional Mapping of Movement and Speech Using Task-Based Electrophysiological Changes in Stereoelectroencephalography

Jensen,

Fine,

Kerezoudis

et al. 2024

Preprint

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Introduction: Stereoelectroencephalography (sEEG) has become the predominant method for intracranial seizure localization. When imaging, semiology, and scalp EEG are not in full agreement or definitively localizing, implanted sEEG recordings are used to test candidate seizure onset zones (SOZs). Discovered SOZs may then be targeted for resection, laser ablation, or neurostimulation. If a SOZ is eloquent, resection and ablation are both contraindicated, so identifying functional representation is crucial for therapeutic decision making. Objective: We present a novel functional brain mapping technique that utilizes task-based electrophysiological changes in sEEG during behavioral tasks and test this in pediatric and adult patients. Methods: sEEG was recorded in twenty patients with epilepsy, aged 6-39 (12 female, 18 of 20 patients < 21 years old), who underwent implanted monitoring to identify seizure onset. Each performed 1) visually cued simple repetitive movements of the hand, foot, or tongue while electromyography was recorded, and 2) simple picture naming or verb generation speech tasks while audio was recorded. Broadband changes in the power spectrum of the sEEG were compared between behavior and rest. Results: Electrophysiological functional mapping of movement and/or speech areas was completed in all 20 patients. Eloquent representation was identified in both cortex and white matter, and generally corresponded to classically described functional anatomic organization as well as other clinical mapping results. Robust maps of brain activity were identified in healthy brain, regions of developmental or acquired structural abnormality, and SOZs. Conclusion: Task based electrophysiological mapping using broadband changes in the sEEG signal reliably identifies movement and speech representation in pediatric and adult epilepsy patients.

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A redrawn map for the human motor cortex

Leopold¹

2023

Nature

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Homunculus Interruptus: A motor association area in the depth of the central sulcus

Cited by 8 publications

References 33 publications

A somato-cognitive action network alternates with effector regions in motor cortex

A somato-cognitive action network alternates with effector regions in motor cortex

Functional Mapping of Movement and Speech Using Task-Based Electrophysiological Changes in Stereoelectroencephalography

A redrawn map for the human motor cortex

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