RESUMEN
The activity of frontal motor areas during hand-object interaction is coordinated by dense communication along specific white matter pathways. This architecture allows the continuous shaping of voluntary motor output but, despite extensive investigation in non-human primate studies, remains poorly understood in humans. Disclosure of this system is crucial for predicting and treatment of motor deficits after brain lesions. For this purpose, we investigated the effect of direct electrical stimulation on white matter pathways within the frontal lobe on hand-object manipulation. This was tested in 34 patients (15 left hemisphere, mean age 42 years, 17 male, 15 with tractography) undergoing awake neurosurgery for frontal lobe tumour removal with the aid of the brain mapping technique. The stimulation outcome was quantified based on hand-muscle activity required by task execution. The white matter pathways responsive to stimulation with an interference on muscles were identified by means of probabilistic density estimation of stimulated sites, tract-based lesion-symptom (disconnectome) analysis and diffusion tractography on the single patient level. Finally, we assessed the effect of permanent tract disconnection on motor outcome in the immediate postoperative period using a multivariate lesion-symptom mapping approach. The analysis showed that stimulation disrupted hand-muscle activity during task execution at 66 sites within the white matter below dorsal and ventral premotor regions. Two different EMG interference patterns associated with different structural architectures emerged: (i) an 'arrest' pattern, characterized by complete impairment of muscle activity associated with an abrupt task interruption, occurred when stimulating a white matter area below the dorsal premotor region. Local middle U-shaped fibres, superior fronto-striatal, corticospinal and dorsal fronto-parietal fibres intersected with this region. (ii) a 'clumsy' pattern, characterized by partial disruption of muscle activity associated with movement slowdown and/or uncoordinated finger movements, occurred when stimulating a white matter area below the ventral premotor region. Ventral fronto-parietal and inferior fronto-striatal tracts intersected with this region. Finally, only resections partially including the dorsal white matter region surrounding the supplementary motor area were associated with transient upper-limb deficit (P = 0.05; 5000 permutations). Overall, the results identify two distinct frontal white matter regions possibly mediating different aspects of hand-object interaction via distinct sets of structural connectivity. We suggest the dorsal region, associated with arrest pattern and postoperative immediate motor deficits, to be functionally proximal to motor output implementation, while the ventral region may be involved in sensorimotor integration required for task execution.
Asunto(s)
Mano , Corteza Motora , Mapeo Encefálico/métodos , Imagen de Difusión Tensora , Lóbulo Frontal/fisiología , Mano/fisiología , Humanos , Masculino , Corteza Motora/fisiología , Músculo Esquelético/fisiología , Vías Nerviosas/fisiologíaRESUMEN
Fine motor skills rely on the control of hand muscles exerted by a region of primary motor cortex (M1) that has been extensively investigated in monkeys. Although neuroimaging enables the exploration of this system also in humans, indirect measurements of brain activity prevent causal definitions of hand motor representations, which can be achieved using data obtained during brain mapping in tumor patients. High-frequency direct electrical stimulation delivered at rest (HF-DES-Rest) on the hand-knob region of the precentral gyrus has identified two sectors showing differences in cortical excitability. Using quantitative analysis of motor output elicited with HF DES-Rest, we characterized two sectors based on their excitability, higher in the posterior and lower in the anterior sector. We studied whether the different cortical excitability of these two regions reflected differences in functional connectivity (FC) and structural connectivity (SC). Using healthy adults from the Human Connectome Project (HCP), we computed FC and SC of the anterior and the posterior hand-knob sectors identified within a large cohort of patients. The comparison of FC of the two seeds showed that the anterior hand-knob, relative to the posterior hand-knob, showed stronger functional connections with a bilateral set of parietofrontal areas responsible for integrating perceptual and cognitive hand-related sensorimotor processes necessary for goal-related actions. This was reflected in different patterns of SC between the two sectors. Our results suggest that the human hand-knob is a functionally and structurally heterogeneous region organized along a motor-cognitive gradient.SIGNIFICANCE STATEMENT The capability to perform complex manipulative tasks is one of the major characteristics of primates and relies on the fine control of hand muscles exerted by a highly specialized region of the precentral gyrus, often termed the "hand-knob" sector. Using intraoperative brain mapping, we identify two hand-knob sectors (posterior and anterior) characterized by differences in cortical excitability. Based on resting-state functional connectivity (FC) and tractography in healthy subjects, we show that posterior and anterior hand-knob sectors differ in their functional connectivity (FC) and structural connectivity (SC) with frontoparietal regions. Thus, anteroposterior differences in cortical excitability are paralleled by differences in FC and SC that likely reflect a motor (posterior) to cognitive (anterior) organization of this cortical region.
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Mano/fisiología , Destreza Motora/fisiología , Músculo Esquelético/fisiología , Adolescente , Adulto , Anciano , Corteza Cerebral/diagnóstico por imagen , Corteza Cerebral/fisiología , Cognición , Conectoma , Potenciales Evocados Motores/fisiología , Femenino , Lóbulo Frontal/diagnóstico por imagen , Lóbulo Frontal/fisiología , Mano/inervación , Humanos , Periodo Intraoperatorio , Imagen por Resonancia Magnética , Masculino , Persona de Mediana Edad , Corteza Motora , Músculo Esquelético/inervación , Vías Nerviosas/fisiología , Estimulación Transcraneal de Corriente Directa , Percepción Visual/fisiología , Adulto JovenRESUMEN
In primates, the parietal cortex plays a crucial role in hand-object manipulation. However, its involvement in object manipulation and related hand-muscle control has never been investigated in humans with a direct and focal electrophysiological approach. To this aim, during awake surgery for brain tumors, we studied the impact of direct electrical stimulation (DES) of parietal lobe on hand-muscles during a hand-manipulation task (HMt). Results showed that DES applied to fingers-representation of postcentral gyrus (PCG) and anterior intraparietal cortex (aIPC) impaired HMt execution. Different types of EMG-interference patterns were observed ranging from a partial (task-clumsy) or complete (task-arrest) impairment of muscles activity. Within PCG both patterns coexisted along a medio (arrest)-lateral (clumsy) distribution, while aIPC hosted preferentially the task-arrest. The interference patterns were mainly associated to muscles suppression, more pronounced in aIPC with respect to PCG. Moreover, within PCG were observed patterns with different level of muscle recruitment, not reported in the aIPC. Overall, EMG-interference patterns and their probabilistic distribution suggested the presence of different functional parietal sectors, possibly playing different roles in hand-muscle control during manipulation. We hypothesized that task-arrest, compared to clumsy patterns, might suggest the existence of parietal sectors more closely implicated in shaping the motor output.
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Estimulación Eléctrica , Mano/fisiología , Actividad Motora/fisiología , Músculo Esquelético/fisiología , Lóbulo Parietal/fisiología , Corteza Somatosensorial/fisiología , Adulto , Anciano , Electromiografía , Femenino , Humanos , Masculino , Persona de Mediana EdadRESUMEN
Dorsal and ventral premotor (dPM and vPM) areas are crucial in control of hand muscles during object manipulation, although their respective role in humans is still debated. In patients undergoing awake surgery for brain tumors, we studied the effect of direct electrical stimulation (DES) of the premotor cortex on the execution of a hand manipulation task (HMt). A quantitative analysis of the activity of extrinsic and intrinsic hand muscles recorded during and in absence of DES was performed. Results showed that DES applied to premotor areas significantly impaired HMt execution, affecting task-related muscle activity with specific features related to the stimulated area. Stimulation of dorsal vPM induced both a complete task arrest and clumsy task execution, characterized by general muscle suppression. Stimulation of ventrocaudal dPM evoked a complete task arrest mainly due to a dysfunctional recruitment of hand muscles engaged in task execution. These results suggest that vPM and dPM contribute differently to the control of hand muscles during object manipulation. Stimulation of both areas showed a significant impact on motor output, although the different effects suggest a stronger relationship of dPM with the corticomotoneuronal circuit promoting muscle recruitment and a role for vPM in supporting sensorimotor integration.
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Mano/fisiología , Actividad Motora/fisiología , Corteza Motora/fisiología , Músculo Esquelético/fisiología , Adulto , Anciano , Estimulación Eléctrica , Electromiografía , Fuerza de la Mano , Humanos , Persona de Mediana EdadRESUMEN
The development of awake intraoperative brain-mapping procedures for resection of brain tumors is of growing interest in neuroscience, because it enables direct testing of brain tissue, previously only possible in non-human primates. In a recent study performed in this setting specific effects can be induced by direct electrical stimulation on different sectors of premotor cortex during the execution of a hand manipulation task. Specifically, direct electrical stimulation applied on a dorsal sector of precentral cortex led to an increase in motor unit recruitment in hand muscles during execution of a hand manipulation task (Recruitment sector). The opposite effect was elicited when electrical stimulation was delivered more ventrally on the precentral cortex (Suppression sector). We studied whether the different effects on motor behavior induced by direct electrical stimulation applied on the two sites of the precentral cortex underlie differences in their functional connectivity with other brain areas, measured using resting state fMRI. Using healthy adults scanned as part of the Human Connectome Project, we computed the functional connectivity of each sector used as seeds. The functional connectivity patterns of the two intraoperative seeds was similar but cross-comparison revealed that the left and right Recruitment sectors had stronger functional connections with the hand region of the sensorimotor cortex, while the right Suppression region displayed stronger functional connectivity with a bilateral set of parieto-frontal areas crucial for the integration of perceptual and cognitive hand-related sensorimotor processes required for goal-related hand actions. Our results suggest that analyzing data obtained in the intraoperative setting with resting state functional magnetic resonance imaging in healthy brains can yield useful insight into the roles of different premotor sectors directly involved in hand-object interaction.
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Neoplasias Encefálicas/cirugía , Conectoma , Lóbulo Frontal/fisiología , Mano/fisiología , Actividad Motora/fisiología , Músculo Esquelético/fisiología , Red Nerviosa/fisiología , Reclutamiento Neurofisiológico/fisiología , Corteza Sensoriomotora/fisiología , Adolescente , Adulto , Anciano , Estimulación Eléctrica , Lóbulo Frontal/diagnóstico por imagen , Humanos , Monitorización Neurofisiológica Intraoperatoria , Imagen por Resonancia Magnética , Persona de Mediana Edad , Corteza Motora/diagnóstico por imagen , Corteza Motora/fisiología , Red Nerviosa/diagnóstico por imagen , Corteza Sensoriomotora/diagnóstico por imagen , Adulto JovenRESUMEN
A key aspect of cognitive control is the management of conflicting incoming information to achieve a goal, termed 'interference control'. Although the role of the right frontal lobe in interference control is evident, the white matter tracts subserving this cognitive process remain unclear. To investigate this, we studied the effect of transient network disruption (by means of direct electrical stimulation) and permanent disconnection (resulting from neurosurgical resection) on interference control processes, using the Stroop test in the intraoperative and extraoperative neurosurgical setting. We evaluated the sites at which errors could be produced by direct electrical stimulation during an intraoperative Stroop test in 34 patients with frontal right hemisphere glioma. Lesion-symptom mapping was used to evaluate the relationship between the resection cavities and postoperative performance on the Stroop test of this group compared with an additional 29 control patients who did not perform the intraoperative test (63 patients in total aged 17-77 years; 28 female). We then examined tract disruption and disconnection in a subset of eight patients who underwent both the intraoperative Stroop test and high angular resolution diffusion imaging (HARDI) tractography. The results showed that, intraoperatively, the majority of sites associated with errors during Stroop test performance and concurrent subcortical stimulation clustered in a region of white matter medial to the right inferior frontal gyrus, lateral and superior to the striatum. Patients who underwent the intraoperative test maintained cognitive control ability at the 1-month follow-up (P = 0.003). Lesion-symptom analysis showed resection of the right inferior frontal gyrus was associated with slower postoperative Stroop test ability (corrected for multiple comparisons, 5000 permutations). The stimulation sites associated with intraoperative errors most commonly corresponded with the inferior fronto-striatal tracts and anterior thalamic radiation (over 75% of patients), although the latter was commonly resected without postoperative deficits on the Stroop test (in 60% of patients). Our results show converging evidence to support a critical role for the inferior frontal gyrus in interference control processes. The intraoperative data combined with tractography suggests that cortico-subcortical tracts, over cortico-cortical connections, may be vital in maintaining efficiency of cognitive control processes. This suggests the importance of their preservation during resection of right frontal tumours.
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Neoplasias Encefálicas/cirugía , Función Ejecutiva/fisiología , Lóbulo Frontal/fisiología , Glioma/cirugía , Monitorización Neurofisiológica Intraoperatoria/métodos , Adolescente , Adulto , Anciano , Mapeo Encefálico/métodos , Cognición/fisiología , Imagen de Difusión Tensora , Femenino , Humanos , Masculino , Persona de Mediana Edad , Vías Nerviosas/fisiología , Test de Stroop , Adulto JovenRESUMEN
BACKGROUND: Data on human brain function obtained with direct electrical stimulation (DES) in neurosurgical patients have been recently integrated and combined with modern neuroimaging techniques, allowing a connectome-based approach fed by intraoperative DES data. Within this framework is crucial to develop reliable methods for spatial localization of DES-derived information to be integrated within the neuroimaging workflow. NEW METHOD: To this aim, we applied the Kernel Density Estimation for modelling the distribution of DES sites from different patients into the MNI space. The algorithm has been embedded in a MATLAB-based User Interface, Peaglet. It allows an accurate probabilistic weighted and unweighted estimation of DES sites location both at cortical level, by using shortest path calculation along the brain 3D geometric topology, and subcortical level, by using a volume-based approach. RESULTS: We applied Peaglet to investigate spatial estimation of cortical and subcortical stimulation sites provided by recent brain tumour studies. The resulting NIfTI maps have been anatomically investigated with neuroimaging open-source tools. COMPARISON WITH EXISTING METHODS: Peaglet processes differently cortical and subcortical data following their distinguishing geometrical features, increasing anatomical specificity of DES-related results and their reliability within neuroimaging environments. CONCLUSIONS: Peaglet provides a robust probabilistic estimation of the cortical and subcortical distribution of DES sites going beyond a region of interest approach, respecting cortical and subcortical intrinsic geometrical features. Results can be easily integrated within the neuroimaging workflow to drive connectomic analysis.
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Algoritmos , Humanos , Neoplasias Encefálicas/diagnóstico por imagen , Neoplasias Encefálicas/fisiopatología , Conectoma/métodos , Encéfalo/diagnóstico por imagen , Encéfalo/fisiología , Estimulación Eléctrica , Imagen por Resonancia Magnética/métodos , Neuroimagen/métodos , Corteza Cerebral/fisiología , Corteza Cerebral/diagnóstico por imagenRESUMEN
The cortical area within the human primary motor cortex (M1) that hosts the representation of the hand and fingers is known as the 'hand-knob' and is essential for voluntary hand movement. The anatomo-functional heterogeneity described within the monkey primary motor cortex (M1) in a rostro-caudal direction suggests an internal subdivision in two sectors originating different systems of connections to the spinal cord. Direct investigation of the human hand-knob has been prevented, so far, by methodological constraints. The unique setting of brain tumour resection with the brain mapping technique in awake patients enables direct electrophysiological investigation of the functional properties of the human hand-knob. Motor-evoked potentials (MEPs) elicited by Direct Electrical Stimulation (DES) at high frequency (HF-DES) delivered along the hand-knob in rostro-caudal direction, i.e., from the central to the precentral sulcus, were recorded from the hand/arm muscles in patients at rest. The sites located near the precentral sulcus identified with HF-DES were then stimulated with low-frequency DES (LF-DES) during a hand manipulation task (HMt) to assess whether DES affected task execution. From the stimulated sites, corticofugal projections and U-shaped tracts connecting with adjacent gyri were traced using diffusion tensor and spherical deconvolution tractography. Analysis of MEPs showed a rostro-caudal gradient of cortical excitability along the hand-knob (the rostral sector being less excitable). Stimulation of rostral sites during the HMt impaired the task by inducing dysfunctional recruitment or, alternatively, suppression of distal muscles. Diffusion tractography showed different patterns of rostro-caudal connectivity for the U-shaped tracts. Overall data suggests, in humans, the anatomo-functional subdivision of the human hand-knob in two sectors, possibly subserving different roles in motor control.
Asunto(s)
Corteza Motora/fisiología , Movimiento/fisiología , Adolescente , Adulto , Anciano , Mapeo Encefálico/métodos , Estimulación Eléctrica , Electromiografía , Femenino , Mano , Humanos , Masculino , Persona de Mediana Edad , Corteza Motora/anatomía & histología , Músculo Esquelético/fisiología , Desempeño Psicomotor/fisiología , Adulto JovenRESUMEN
We describe the memristive properties of cluster-assembled gold films. We show that resistive switching is observed in pure metallic nanostructured films at room temperature and atmospheric pressure, in response to applied voltage inputs. In particular, we observe resistance changes up to 400% and archetypal switching events that have remarkable symmetry with the applied voltage. We associated this symmetry with 'potentiation' and 'anti-potentiation' processes involving the activation of synapses and of pathways comprising multiple synapses. The stability and reproducibility of the resistance switching, which lasted over many hours, make these devices ideal test-beds for exploration of the basic mechanisms of the switching processes, and allow convenient fabrication of devices that may have neuromorphic properties.
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Soft robots should move in an unstructured environment and explore it and, to do so, they should be able to measure and distinguish proprioceptive and exteroceptive stimuli. This can be done by embedding mechanosensing systems in the body of the robot. Here, we present a polydimethylsiloxane block sensorized with an electro-optical system and a resistive strain gauge made with the supersonic cluster beam implantation (SCBI) technique. We show how to integrate these sensing elements during the whole fabrication process of the soft body and we demonstrate that their presence does not change the mechanical properties of the bulk material. Exploiting the position of both sensing systems and a proper combination of the output signals, we present a strategy to measure simultaneously external pressure and positive/negative bending of the body. In particular, the optical system can reveal any mechanical stimulation (external from the soft block or due to its own deformation), while the resistive strain gauge is insensitive to the external pressure, but sensitive to the bending of the body. This solution, here applied to a simple block of soft material, could be extended to the whole body of a soft robot. This approach provides detection and discrimination of the two stimuli (pressure and bending), with low computational effort and without significant mechanical constraint.
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Electroactive ionic gel/metal nanocomposites are produced by implanting supersonically accelerated neutral gold nanoparticles into a novel chemically crosslinked ion conductive soft polymer. The ionic gel consists of chemically crosslinked poly(acrylic acid) and polyacrylonitrile networks, blended with halloysite nanoclays and imidazolium-based ionic liquid. The material exhibits mechanical properties similar to that of elastomers (Young's modulus ≈ 0.35 MPa) together with high ionic conductivity. The fabrication of thin (≈100 nm thick) nanostructured compliant electrodes by means of supersonic cluster beam implantation (SCBI) does not significantly alter the mechanical properties of the soft polymer and provides controlled electrical properties and large surface area for ions storage. SCBI is cost effective and suitable for the scaleup manufacturing of electroactive soft actuators. This study reports the high-strain electromechanical actuation performance of the novel ionic gel/metal nanocomposites in a low-voltage regime (from 0.1 to 5 V), with long-term stability up to 76 000 cycles with no electrode delamination or deterioration. The observed behavior is due to both the intrinsic features of the ionic gel (elasticity and ionic transport capability) and the electrical and morphological features of the electrodes, providing low specific resistance (<100 Ω cm-2 ), high electrochemical capacitance (≈mF g-1 ), and minimal mechanical stress at the polymer/metal composite interface upon deformation.
RESUMEN
A thermally shrinkable and conductive nanocomposite material is prepared by supersonic cluster beam implantation (SCBI) of neutral Au nanoparticles (Au NPs) into a commercially available thermo-retractable polystyrene (PS) sheet. Micronanowrinkling is obtained during shrinking, which is studied by means of SEM, TEM and AFM imaging. Characteristic periodicity is determined and correlated with nanoparticle implantation dose, which permits us to tune the topographic pattern. Remarkable differences emerged with respect to the well-known case of wrinkling of bilayer metal-polymer. Wrinkled composite surfaces are characterized by a peculiar multiscale structuring that promises potential technological applications in the field of catalytic surfaces, sensors, biointerfaces, and optics, among others.