Microstimulation Activates a Handful of Muscle Synergies

Overduin, Simon A.; d’Avella, Andrea; Carmena, Jose M.; Bizzi, Emilio

doi:10.1016/j.neuron.2012.10.018

Cited by 262 publications

(267 citation statements)

References 40 publications

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“…Finally, in apparent contrast with previous observations in monkey (2)(3)(4), in the present study, we did not identify complex neural representations for other ethologically relevant behaviors (e.g., defensive, manipulative) besides hand/mouth synergies. This could be taken as an indication that such representations do not exist in the human PrG, at least in the region we stimulated, but this hypothesis is unlikely.…”

Section: Discussioncontrasting

confidence: 99%

“…However, the generality of this model was recently challenged in nonhuman primates, where reaching, grasping, defensive, and hand/mouth movements have been found to be represented as complex motor primitives in independent circumscribed territories of the precentral gyrus (PrG) (2)(3)(4). To account for this observation, it was suggested that complex motor primitives have emerged during primate evolution to optimize the production of ethologically relevant behaviors (4).…”

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confidence: 99%

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Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus

Desmurget

Richard

Harquel

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Complex motor responses are often thought to result from the combination of elemental movements represented at different neural sites. However, in monkeys, evidence indicates that some behaviors with critical ethological value, such as self-feeding, are represented as motor primitives in the precentral gyrus (PrG). In humans, such primitives have not yet been described. This could reflect well-known interspecies differences in the organization of sensorimotor regions (including PrG) or the difficulty of identifying complex neural representations in peroperative settings. To settle this alternative, we focused on the neural bases of hand/mouth synergies, a prominent example of human behavior with high ethological value. By recording motor-and somatosensory-evoked potentials in the PrG of patients undergoing brain surgery (2-60 y), we show that two complex nested neural representations can mediate hand/mouth actions within this structure: (i) a motor representation, resembling self-feeding, where electrical stimulation causes the closing hand to approach the opening mouth, and (ii) a motor-sensory representation, likely associated with perioral exploration, where cross-signal integration is accomplished at a cortical site that generates hand/arm actions while receiving mouth sensory inputs. The first finding extends to humans' previous observations in monkeys. The second provides evidence that complex neural representations also exist for perioral exploration, a finely tuned skill requiring the combination of motor and sensory signals within a common control loop. These representations likely underlie the ability of human children and newborns to accurately produce coordinated hand/mouth movements, in an otherwise general context of motor immaturity.motor cortex | motor synergies | brain mapping | cortical stimulation

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Section: Discussioncontrasting

confidence: 99%

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confidence: 99%

Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus

Desmurget

Richard

Harquel

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…It seems likely that the spatial scale of clinical stimulation (5 mm) might result in movements closer to the tonic/seizure end of the spectrum, whereas microstimulation (~ 1 mm) may produce finer movements closer to the behavioral end of the spectrum. 8,9,16 Just as in previous human and animal stimulation studies, the observed responses were stereotyped across subjects, allowing for easy classification in most cases.…”

Section: Discussionmentioning

confidence: 80%

“…8 Further support comes from work by Overduin et al, demonstrating that microstimulation-evoked electromyographic patterns in macaques can be decomposed into smaller sets of muscle synergies that closely mirror those generated by natural hand movements. 16 Whether our observed movements are behaviorally relevant is unclear. It seems likely that the spatial scale of clinical stimulation (5 mm) might result in movements closer to the tonic/seizure end of the spectrum, whereas microstimulation (~ 1 mm) may produce finer movements closer to the behavioral end of the spectrum.…”

Section: Discussionmentioning

confidence: 94%

A probabilistic map of the human ventral sensorimotor cortex using electrical stimulation

Breshears¹,

Molinaro

Chang

2015

JNS

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O ver 70 years ago, Penfield (1937) published his seminal work on the somatotopy of the human peri-rolandic cortex, fortifying the notion of the classic sensorimotor homunculus. Surprisingly, few additional investigations with direct electrocortical stimulation (ECS) have been undertaken to study the organization of the ventral half of the sensorimotor cortex (vSMC) in humans, where speech articulators and nearby language centers make this area unique. 1,4 Neuroanatomically, the vSMC is distinct from the dorsal sensorimotor cortex (dSMC). Its neurons project via the corticobulbar pathway to synapse in the brainstem motor nuclei, providing bilateral innervation to the muscles of the upper face, jaw, oropharynx, and vocal tract through cranial nerves (CNs) . diSclOSure Dr. Chang was funded by US National Institutes of Health grants R01-DC012379, R00-NS065120, and DP2-OD00862 and the Ester A. and Joseph Klingenstein Foundation. The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.A probabilistic map of the human ventral sensorimotor cortex using electrical stimulation OBJect The human ventral sensorimotor cortex (vSMC) is involved in facial expression, mastication, and swallowing, as well as the dynamic and highly coordinated movements of human speech production. However, vSMC organization remains poorly understood, and previously published population-driven maps of its somatotopy do not accurately reflect the variability across individuals in a quantitative, probabilistic fashion. The goal of this study was to describe the responses to electrical stimulation of the vSMC, generate probabilistic maps of function in the vSMC, and quantify the variability across individuals. methOdS Photographic, video, and stereotactic MRI data of intraoperative electrical stimulation of the vSMC were collected for 33 patients undergoing awake craniotomy. Stimulation sites were converted to a 2D coordinate system based on anatomical landmarks. Motor, sensory, and speech stimulation responses were reviewed and classified. Probabilistic maps of stimulation responses were generated, and spatial variance was quantified. reSultS In 33 patients, the authors identified 194 motor, 212 sensory, 61 speech-arrest, and 27 mixed responses. Responses were complex, stereotyped, and mostly nonphysiological movements, involving hand, orofacial, and laryngeal musculature. Within individuals, the presence of oral movement representations varied; however, the dorsal-ventral order was always preserved. The most robust motor responses were jaw (probability 0.85), tongue (0.64), lips (0.58), and throat (0.52). Vocalizations were seen in 6 patients (0.18), more dorsally near lip and dorsal throat areas. Sensory responses were spatially dispersed; however, patients' subjective reports were highly precise in localization within the mouth. The most robust responses included tongue (0.82) and lips (0.42). The probability of speech arrest was 0.85, highest 15-20 mm anterior to t...

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“…The laws governing these primitives are constrained by the structure of the muscular system, and the neural systems that control our movements where motor synergies seem to play a major role [59]. Several computational motor control theories incorporate a notion of motor cost in one way or another.…”

Section: The Costs Of Non-verbal Communication Within Social Interactmentioning

confidence: 99%

Interactional leader–follower sensorimotor communication strategies during repetitive joint actions

Candidi

Curioni

Rigoli

et al. 2015

J. R. Soc. Interface.

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Non-verbal communication is the basis of animal interactions. In dyadic leaderfollower interactions, leaders master the ability to carve their motor behaviour in order to 'signal' their future actions and internal plans while these signals influence the behaviour of follower partners, who automatically tend to imitate the leader even in complementary interactions. Despite their usefulness, signalling and imitation have a biomechanical cost, and it is unclear how this cost-benefits trade-off is managed during repetitive dyadic interactions that present learnable regularities. We studied signalling and imitation dynamics (indexed by movement kinematics) in pairs of leaders and followers during a repetitive, rule-based, joint action. Trial-by-trial Bayesian model comparison was used to evaluate the relation between signalling, imitation and pair performance. The different models incorporate different hypotheses concerning the factors (past interactions versus online movements) influencing the leader's signalling (or follower's imitation) kinematics. This approach showed that (i) leaders' signalling strategy improves future couple performance, (ii) leaders used the history of past interactions to shape their signalling, (iii) followers' imitative behaviour is more strongly affected by the online movement of the leader. This study elucidates the ways online sensorimotor communication help individuals align their task representations and ultimately improves joint action performance.

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Microstimulation Activates a Handful of Muscle Synergies

Cited by 262 publications

References 40 publications

Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus

Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus

A probabilistic map of the human ventral sensorimotor cortex using electrical stimulation

Interactional leader–follower sensorimotor communication strategies during repetitive joint actions

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