Direct Electrical Stimulation of Premotor Areas: Different Effects on Hand Muscle Activity during Object Manipulation

Fornia, Luca; Rossi, Marco; Rabuffetti, Marco; Leonetti, Antonella; Puglisi, Guglielmo; Viganò, Luca; Simone, Luciano; Howells, Henrietta; Bellacicca, Andrea; Bello, Lorenzo; Cerri, Gabriella

doi:10.1093/cercor/bhz139

Cited by 33 publications

(37 citation statements)

References 58 publications

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“…As reported in a previous study using the same motor task, DES on PMC interferes with motor execution 12,14,15 . Does the disruption of PMC simultaneously interfere with the patients' motor awareness?…”

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confidence: 74%

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Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions

et al. 2020

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A challenge for neuroscience is to understand the conscious and unconscious processes underlying construction of willed actions. We investigated the neural substrate of human motor awareness during awake brain surgery. In a first experiment, awake patients performed a voluntary hand motor task and verbally monitored their real-time performance, while different brain areas were transiently impaired by direct electrical stimulation (DES). In a second experiment, awake patients retrospectively reported their motor performance after DES. Based on anatomo-clinical evidence from motor awareness disorders following brain damage, the premotor cortex (PMC) was selected as a target area and the primary somatosensory cortex (S1) as a control area. In both experiments, DES on both PMC and S1 interrupted movement execution, but only DES on PMC dramatically altered the patients' motor awareness, making them unconscious of the motor arrest. These findings endorse PMC as a crucial hub in the anatomo-functional network of human motor awareness.

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confidence: 74%

“…(1) A positive effect in altering motor execution was expected based on previous literature employing DES during the same HMt 12,14,15 . (2) A positive effect in altering the motor awareness was expected based on anatomical and functional evidence in AHP patients 2,7-9,48,49 and in healthy subjects 44,45 .…”

Section: Methodsmentioning

confidence: 95%

Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions

et al. 2020

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“…The development of non-invasive functional and connectional imaging techniques has allowed for the construction of similar definitions of motor control pathways also in the human brain (Turella and Lingnau 2014 ), although these are still less clearly defined compared to evidence obtained in the macaque. Functionally distinct cortical sectors have been identified for highly skilled movement using intraoperative stimulation (Viganò et al 2019 ; Fornia et al 2020 ), and the connections have been studied using diffusion MRI tractography (dMRI) (Budisavljevic et al 2016 ; Howells et al 2018 ). Approaches measuring the spontaneous organized fluctuations of brain activity at rest (resting state functional connectivity; rs-FC) may also provide further evidence for large-scale, functionally specialized networks in the human brain (Simone et al 2020 ), although the interpretation of these networks with respect to structural connections is still not clearly defined.…”

Section: Introductionmentioning

confidence: 99%

Reproducing macaque lateral grasping and oculomotor networks using resting state functional connectivity and diffusion tractography

et al. 2020

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Cortico-cortical networks involved in motor control have been well defined in the macaque using a range of invasive techniques. The advent of neuroimaging has enabled non-invasive study of these large-scale functionally specialized networks in the human brain; however, assessing its accuracy in reproducing genuine anatomy is more challenging. We set out to assess the similarities and differences between connections of macaque motor control networks defined using axonal tracing and those reproduced using structural and functional connectivity techniques. We processed a cohort of macaques scanned in vivo that were made available by the open access PRIME-DE resource, to evaluate connectivity using diffusion imaging tractography and resting state functional connectivity (rs-FC). Sectors of the lateral grasping and exploratory oculomotor networks were defined anatomically on structural images, and connections were reproduced using different structural and functional approaches (probabilistic and deterministic whole-brain and seed-based tractography; group template and native space functional connectivity analysis). The results showed that parieto-frontal connections were best reproduced using both structural and functional connectivity techniques. Tractography showed lower sensitivity but better specificity in reproducing connections identified by tracer data. Functional connectivity analysis performed in native space had higher sensitivity but lower specificity and was better at identifying connections between intrasulcal ROIs than group-level analysis. Connections of AIP were most consistently reproduced, although those connected with prefrontal sectors were not identified. We finally compared diffusion MR modelling with histology based on an injection in AIP and speculate on anatomical bases for the observed false negatives. Our results highlight the utility of precise ex vivo techniques to support the accuracy of neuroimaging in reproducing connections, which is relevant also for human studies.

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“…if Canada of USA, country; the results were downloaded onto Brainstorm (a MATLAB toolbox; Tadel, Baillet, Mosher, Pantazis, & Leahy, 2011), obtaining a 3D-MRI reconstruction of each patient MR with all the sites marked as a scout. This was co-registered in the NMI-space [9,22,23]. In "normal"-map patients, the subdivision of the cortical hand-knob region was designed (Figure 3) based on 10 stimulated sites (1,3,5,7,9 covering the anterior region; 2,4,6,8,10 covering the posterior region); in each M1 site the cMT (absolute value/mA) at HF-To5 and HF-To2 was normalized within the subject (Z-score) to allow for a comparison between the anterior and posterior regions with each paradigm [9,22,23].…”

Section: Neurophysiological Data Analysismentioning

confidence: 99%

Targeting Primary Motor Cortex (M1) Functional Components in M1 Gliomas Enhances Safe Resection and Reveals M1 Plasticity Potentials

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Puglisi

et al. 2021

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Primary-Motor-Cortex (M1) hosts two functional components, at its posterior and anterior borders, being the first faster and more excitable. We developed a mapping-technique for M1 components identification and determined their functional cortical-subcortical architecture in M1 gliomas and the impact of their identification on tumor resection and motor performance. A novel advanced mapping technique was used in 102 tumors within M1 or CorticoSpinal-Tract to identify M1-two components. High-Frequency-stimulation (2–5 pulses) with an on-line qualitative and quantitative analysis of motor responses was used; the two components’ cortical/subcortical spatial distribution correlated to clinical, tumor-related factor and patients’ motor outcome; a cohort treated with standard-mapping was used for comparison. The two functional components were always identified on-line; in tumors not affecting M1, its functional segregation was preserved. In M1 tumors, two architectures, both preserving the two components, were disclosed: in 50%, a normal cortical/subcortical architecture emerged, while 50% revealed a distorted architecture with loss of anatomical reference and somatotopy, not associated with tumor histo-molecular features or volume, but with a previous treatment. Motor performance was maintained, suggesting functional compensation. By preserving the highest and resecting the lowest excitability component, the complete-resection increased with low morbidity. The real-time identification of two M1 functional components and the preservation of the highest excitability one increases safe resection, revealing M1 plasticity potentials.

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Direct Electrical Stimulation of Premotor Areas: Different Effects on Hand Muscle Activity during Object Manipulation

Cited by 33 publications

References 58 publications

Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions

Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions

Reproducing macaque lateral grasping and oculomotor networks using resting state functional connectivity and diffusion tractography

Targeting Primary Motor Cortex (M1) Functional Components in M1 Gliomas Enhances Safe Resection and Reveals M1 Plasticity Potentials

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