Muscle Synergies Obtained from Comprehensive Mapping of the Cortical Forelimb Representation Using Stimulus Triggered Averaging of EMG Activity

This work is licensed under a Creative Commons Attribution 4.0 International License.Neuromuscular control of voluntary movement may be simplified using muscle synergies similar to those found using non-negative matrix factorization. We recently identified synergies in electromyography (EMG) recordings associated with both voluntary movement and movement evoked by high-frequency long-duration intracortical microstimulation applied to the forelimb representation of the primary motor cortex (M1). The goal of this study was to use stimulus-triggered averaging (StTA) of EMG activity to investigate the synergy profiles and weighting coefficients associated with poststimulus facilitation, as synergies may be hard-wired into elemental cortical output modules and revealed by StTA. We applied StTA at low (LOW, ∼15 μA) and high intensities (HIGH, ∼110 μA) to 247 cortical locations of the M1 forelimb region in two male rhesus macaques while recording the EMG of 24 forelimb muscles. Our results show that 10–11 synergies accounted for 90% of the variation in poststimulus EMG facilitation peaks from the LOW-intensity StTA dataset while only 4–5 synergies were needed for the HIGH-intensity dataset. Synergies were similar across monkeys and current intensities. Most synergy profiles strongly activated only one or two muscles; all joints were represented and most, but not all, joint directions of motion were represented. Cortical maps of the synergy weighting coefficients suggest only a weak organization. StTA of M1 resulted in highly diverse muscle activations, suggestive of the limiting condition of requiring a synergy for each muscle to account for the patterns observed

Comparison of muscle synergies elicited from transcranial meganetic stimulation (tms) and voluntary movements

A key question in motor control is the redundancy of musculoskeletal elements involved. This problem refers to as the degree of freedom problem. The Muscle Synergy Hypothesis is one of the hypotheses that aim to resolve the problem which defines that a muscle synergy is a combination of a small set of muscles activated at different levels, serving as a building block that constructs motor behaviors. A recent study (Overduin et al. 2012) demonstrated that muscle synergies decomposed by Nonnegative Matrix Factorization (NMF) from EMG patterns evoked by intra-cortical microsimulation (ICMS) in the monkey remarkably matched ones observed in naturalistic reach-and-grasp behaviors. Another study (Ajiboye et al. 2009) showed that synergies elicited from a small number of hand postures can allow prediction of hand postures in general. Inspired by aforementioned studies, the aim of this study was to investigate whether Transcranial Magnetic Stimulation (TMS) can elicit muscle synergies matching ones observed in voluntary movements in healthy human subjects and whether these synergies can serve as frameworks to predict EMG patterns evoked by either TMS or voluntary movements. Five healthy right-handed subjects participated in the study. 8 hand muscles were recorded to capture either TMS-evoked motor evoked potential (MEP) and electromyography (EMG) resulted from subjects’ shaping American Sign Language (ASL) letters and numbers. NMF was utilized to extract synergies from both MEP and EMG data. We observed 5 or 6 synergies can capture 90% of variance of original and matched synergies of two classes. The reconstructions of the original datasets (VTMS: MEP data; Vvol: EMG data; Vrand: Random data as control) from synergies (Hvol synergies elicited from ASL tasks; HTMS synergies elicited from TMS) was done by the nonnegative least-square algorithm, and Proportion of Variance Accounted for (PAV) served as a measure to quantify the quality of the estimation, giving results Hvol -\u3e Vvol: 0.92±0.02; HTMS -\u3e VTMS: 0.94±0.02; Hvol -\u3e Vrand: 0.53±0.03; HTMS -\u3e Vrand: 0.53±0.07; HTMS -\u3e Vvol: 0.70±0.06; Hvol -\u3e VTMS: 0.79±0.06. In conclusion, we argue that cortical components may involve in encoding synergies and we also demonstrate the possibility of synergies serving as frameworks in predicting and explaining human hand postures in general

MICRO-STIMULATION OF NEURONS

This project encompasses the basic understanding of neuropharmacology. Neuropharmacology is the study of how drugs affect cellular function in the nervous system, and the neural mechanisms through which they influence behavior. There are two main branches of neuropharmacology: behavioral and molecular. Behavioral neuropharmacology focuses on the study of how drugs affect human behavior (neuropsychopharmacology), including the study of how drug dependence and addiction affect the human brain.Molecular neuropharmacology involves the study of neurons and their neurochemical interactions, with the overall goal of developing drugs that have beneficial effects on neurological function. Both of these fields are closely connected, since both are concerned with the interactions of neurotransmitters, neuropeptides, neurohormones, neuromodulators, enzymes, second messengers, co-transporters, ion channels, and receptor proteins in the central and peripheral nervous systems. Studying these interactions, researchers are developing drugs to treat many different neurological disorders, including pain, neurodegenerative diseases such as Parkinson's disease and Alzheimer's disease, psychological disorders, addiction, and many others.Before understanding the effect of drugs we studied firing rates of neurons and neural networks. Initially we started off understanding firing rates and at what frequencies spikes will be recorded on the SpikerBox. We found that at low frequencies we can observe spikes. Later we started stimulating muscles in the cockroach’s leg using music. Upon varying bass, treble, etc we noticed the difference in spikes and recorded the same. After understanding the spikes we injected Nicotine and Mono Sodium Glutamate with control (water) at intervals of 2-4 minutes to observe which drug would have an effect on the neurons. MSG is present in 80% networks however for insects we found Nicotine stimulates and MSG does not

Evaluation of Matrix Factorisation Approaches for Muscle Synergy Extraction

The muscle synergy concept provides a widely-accepted paradigm to break down the complexity of motor control. In order to identify the synergies, different matrix factorisation techniques have been used in a repertoire of fields such as prosthesis control and biomechanical and clinical studies. However, the relevance of these matrix factorisation techniques is still open for discussion since there is no ground truth for the underlying synergies. Here, we evaluate factorisation techniques and investigate the factors that affect the quality of estimated synergies. We compared commonly used matrix factorisation methods: Principal component analysis (PCA), Independent component analysis (ICA), Non-negative matrix factorization (NMF) and second-order blind identification (SOBI). Publicly available real data were used to assess the synergies extracted by each factorisation method in the classification of wrist movements. Synthetic datasets were utilised to explore the effect of muscle synergy sparsity, level of noise and number of channels on the extracted synergies. Results suggest that the sparse synergy model and a higher number of channels would result in better-estimated synergies. Without dimensionality reduction, SOBI showed better results than other factorisation methods. This suggests that SOBI would be an alternative when a limited number of electrodes is available but its performance was still poor in that case. Otherwise, NMF had the best performance when the number of channels was higher than the number of synergies. Therefore, NMF would be the best method for muscle synergy extraction.Comment: Keywords: Muscle synergy; Matrix factorisation; Surface electromyogram; Non-negative matrix factorisation; Second-order blind identification; Principal component analysis; Independent component analysi

Critical Points and Traveling Wave in Locomotion: Experimental Evidence and Some Theoretical Considerations

The central pattern generator (CPG) architecture for rhythm generation remains partly elusive. We compare cat and frog locomotion results, where the component unrelated to pattern formation appears as a temporal grid, and traveling wave respectively. Frog spinal cord microstimulation with N-methyl-D-Aspartate (NMDA), a CPG activator, produced a limited set of force directions, sometimes tonic, but more often alternating between directions similar to the tonic forces. The tonic forces were topographically organized, and sites evoking rhythms with different force subsets were located close to the constituent tonic force regions. Thus CPGs consist of topographically organized modules. Modularity was also identified as a limited set of muscle synergies whose combinations reconstructed the EMGs. The cat CPG was investigated using proprioceptive inputs during fictive locomotion. Critical points identified both as abrupt transitions in the effect of phasic perturbations, and burst shape transitions, had biomechanical correlates in intact locomotion. During tonic proprioceptive perturbations, discrete shifts between these critical points explained the burst durations changes, and amplitude changes occurred at one of these points. Besides confirming CPG modularity, these results suggest a fixed temporal grid of anchoring points, to shift modules onsets and offsets. Frog locomotion, reconstructed with the NMDA synergies, showed a partially overlapping synergy activation sequence. Using the early synergy output evoked by NMDA at different spinal sites, revealed a rostrocaudal topographic organization, where each synergy is preferentially evoked from a few, albeit overlapping, cord regions. Comparing the locomotor synergy sequence with this topography suggests that a rostrocaudal traveling wave would activate the synergies in the proper sequence for locomotion. This output was reproduced in a two-layer model using this topography and a traveling wave. Together our results suggest two CPG components: modules, i.e., synergies; and temporal patterning, seen as a temporal grid in the cat, and a traveling wave in the frog. Animal and limb navigation have similarities. Research relating grid cells to the theta rhythm and on segmentation during navigation may relate to our temporal grid and traveling wave results. Winfree’s mathematical work, combining critical phases and a traveling wave, also appears important. We conclude suggesting tracing, and imaging experiments to investigate our CPG model

Neuroplasticity of Ipsilateral Cortical Motor Representations, Training Effects and Role in Stroke Recovery

This thesis examines the contribution of the ipsilateral hemisphere to motor control with the aim of evaluating the potential of the contralesional hemisphere to contribute to motor recovery after stroke. Predictive algorithms based on neurobiological principles emphasize integrity of the ipsilesional corticospinal tract as the strongest prognostic indicator of good motor recovery. In contrast, extensive lesions placing reliance on alternative contralesional ipsilateral motor pathways are associated with poor recovery. Within the predictive algorithms are elements of motor control that rely on contributions from ipsilateral motor pathways, suggesting that balanced, parallel contralesional contributions can be beneficial. Current therapeutic approaches have focussed on the maladaptive potential of the contralesional hemisphere and sought to inhibit its activity with neuromodulation. Using Transcranial Magnetic Stimulation I seek examples of beneficial plasticity in ipsilateral cortical motor representations of expert performers, who have accumulated vast amounts of deliberate practise training skilled bilateral activation of muscles habitually under ipsilateral control. I demonstrate that ipsilateral cortical motor representations reorganize in response to training to acquisition of skilled motor performance. Features of this reorganization are compatible with evidence suggesting ipsilateral importance in synergy representations, controlled through corticoreticulopropriospinal pathways. I demonstrate that ipsilateral plasticity can associate positively with motor recovery after stroke. Features of plastic change in ipsilateral cortical representations are shown in response to robotic training of chronic stroke patients. These findings have implications for the individualization of motor rehabilitation after stroke, and prompt reappraisal of the approach to therapeutic intervention in the chronic phase of stroke

Primate Motor Cortex: Individual and Ensemble Neuron-Muscle Output Relationships

The specific aims of this study were to: 1) investigate the encoding of forelimb muscle activity timing and magnitude by corticomotoneuronal (CM) cells, 2) test the stability of primary motor cortex (M1) output to forelimb muscles under different task conditions, and 3) characterize input/output relationships associated with different intracortical microstimulation (ICMS) methods. Neuronal recording and stimulating methods were used in combination with electromyographic (EMG) recording of 24 forelimb muscles to investigate questions related to M1 control of forelimb muscles. Target muscles of CM neurons were identified by the presence of post-spike facilitation (PSpF) in spike-triggered averages (SpTA) of EMG activity. Post-stimulus output effects were obtained with three different ICMS methods; stimulus-triggered averaging (StTA) of EMG activity, repetitive short duration ICMS (RS-ICMS) and repetitive long duration ICMS (RL-ICMS). Our results demonstrate that CM cells exhibit strong and consistent coactivation with their target muscles. Further, the summed activity of populations of identified CM cells was a better predictor of the common muscle's EMG activity than individual neurons. Our data support the view that M1 output encodes muscle activation related parameters. Regarding stability, we found that output effects in StTAs of EMG activity are remarkably stable and largely independent of changes in joint angle, or limb posture. This further validates the use of StTA for mapping and other studies of cortical motor output. RL-ICMS evoked EMG activity was also stable in sign, strength and distribution independent of starting position of the hand. Our data support a model in which RL-ICMS produces sustained co-activation of multiple agonist and antagonist muscles which then generates joint movements according to the length-tension properties of the muscles until an equilibrium position is achieved. Further, RL-ICMS evoked EMG activity did not sum with the existing level of activity; rather the stimulus forced a new EMG level that was independent of existing voluntary background. Our results further show that post-stimulus output effects on muscle activity obtained with StTA and RS-ICMS closely resemble one another. However, RL-ICMS produces effects that can deviate substantially from those observed with StTA

Deciphering the functional role of spatial and temporal muscle synergies in whole-body movements

International audienceVoluntary movement is hypothesized to rely on a limited number of muscle synergies, the recruitment of which translates task goals into effective muscle activity. In this study, we investigated how to analytically characterize the functional role of different types of muscle synergies in task performance. To this end, we recorded a comprehensive dataset of muscle activity during a variety of whole-body pointing movements. We decomposed the electromyographic (EMG) signals using a space-by-time modularity model which encompasses the main types of synergies. We then used a task decoding and information theoretic analysis to probe the role of each synergy by mapping it to specific task features. We found that the temporal and spatial aspects of the movements were encoded by different temporal and spatial muscle synergies, respectively, consistent with the intuition that there should a correspondence between major attributes of movement and major features of synergies. This approach led to the development of a novel computational method for comparing muscle synergies from different participants according to their functional role. This functional similarity analysis yielded a small set of temporal and spatial synergies that describes the main features of whole-body reaching movements

Contextual control of orienting eye-head gaze shifts in the monkey

Vision is one of the principal methods used by primates to acquire information about the surrounding environment. As a result, both humans and monkeys have a highly evolved oculomotor system that functions to rapidly relocate the line of sight to areas of interest. These orienting movements are called gaze shifts. Gaze shifts commonly include the coordinated movement of the eyes-in-head and the head-in-space. This thesis examines the muscular and neural control of orienting head movements. The contextual control of behavior is important as it allows one to act appropriately in response to different situations. A common task used to examine the contextual control of behavior is the pro- and anti-saccade task. Pro-saccades simply require a subject to look towards a stimulus. Anti-saccades require a subject to inhibit a movement towards a stimulus in favor of a volitional movement to the diametrically opposite position. This task is can reveal capabilities of the oculomotor system and its response to varying behavioral states. To understand the neuromuscular control of orienting head movements during various tasks, we recorded the electromyographic (EMG) activity in ten turner and extensor neck muscles. Recording neck EMGs provides an objective and precise measurement of the neural signals received at the neck muscles, circumventing some of the structural and biomechanical complexities of head motion. Chapter two examines neck muscle activity in a pro- and anti-saccade task. Many neural areas and certain neck muscles become active in response to the presentation of a visual stimulus. This visual response on the neck muscles can result in a head turning synergy that orients the head towards the stimulus. By dissociating the typical stimulus-response paradigm, we can analyze if and how the bottom-up visual activity changes in relation to different contexts. A number of cortical and subcortical areas are involved in the generation of correct anti-saccades. By combining EMG recordings while subjects perform this task, we can examine whether top-down task-related activity is present in the neck muscles. This experiment could reveal flexibility in the eye-head gaze shift system that has previously gone unreported. Chapter three will elucidate the supplementary eye fields (SEF) role in the control of orienting eye-head gaze shifts. Neck EMG activity was recorded while providing electrical microstimulation to the SEF in a pro-saccade task The combination of EMGs and SEF stimulation is the first to systematically study the cephalomotor command during head-restrained and head-unrestrained orienting eye-head gaze shifts. The evoked activity of EMGs could reveal functional properties of the neural circuitry between the SEF and the motor related neurons responsible for eye and head movements. The timing and metrics of evoked EMG activity and eye-head gaze shifts are consistent with other frontal areas suggesting a functional role of the frontal cortex in influencing eye-head gaze shifts. Chapter four will combine EMG recordings with SEF stimulation during a pro- and anti-saccade task. The SEF is thought to serve as an interface between high-level cognitive control of gaze shifts and low-level activity associated with the production of saccades. As will be described later in the thesis, neck muscles demonstrate top-down task related activity during anti-saccades. The SEF is a likely candidate for the generation of task-dependent signals observed during anti-saccades. By combining SEF stimulation and neck EMGs in an anti-saccade task, we can reveal if neck muscle activity is consistent with a role for the SEF in the contextual control of eye-head gaze shifts. In summary, this thesis identifies three central point’s concerning orienting eye-head gaze shifts. First, chapter two emphasizes the complex interaction of sensori-motor processes in orienting head movements. Second, chapter three attests to the consistent nature of certain areas in frontal cortex and their impact on eye-head gaze shifts. Finally, chapter four demonstrates a potential candidate for influencing the contextual control of cephalomotor commands. Combined, these results highlight the complex interactions of sensori-motor transformations in the motor periphery and emphasize the parallel nature of information processing during the contextual control of eye-head gaze shifts

Beyond language: The unspoken sensory-motor representation of the tongue in non-primates, non-human and human primates

The English idiom “on the tip of my tongue” commonly acknowledges that something is known, but it cannot be immediately brought to mind. This phrase accurately describes sensorimotor functions of the tongue, which are fundamental for many tongue-related behaviors (e.g., speech), but often neglected by scientific research. Here, we review a wide range of studies conducted on non-primates, non-human and human primates with the aim of providing a comprehensive description of the cortical representation of the tongue's somatosensory inputs and motor outputs across different phylogenetic domains. First, we summarize how the properties of passive non-noxious mechanical stimuli are encoded in the putative somatosensory tongue area, which has a conserved location in the ventral portion of the somatosensory cortex across mammals. Second, we review how complex self-generated actions involving the tongue are represented in more anterior regions of the putative somato-motor tongue area. Finally, we describe multisensory response properties of the primate and non-primate tongue area by also defining how the cytoarchitecture of this area is affected by experience and deafferentation