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The present study explored the relationship between motor-preparatory electroencephalographic (EEG) activity, motivation, and motor performance (specifically premotor reaction time [RT]). Participants performed a RT task by squeezing a hand dynamometer in response to an auditory "go" signal. We recorded EEG and electromyography to index beta-suppression and premotor RT, respectively. Participants' motivation on each trial was modulated by offering monetary incentives at different magnitudes. Mixed-effect linear regression models showed that monetary incentive predicted premotor RT when controlling for beta-suppression, and beta-suppression independently predicted premotor RT. Thus, it appears motivation and beta-suppression can facilitate motor performance independent of one another. A plausible explanation of this effect is that motivation can affect motor performance independent of the motor cortex by influencing subcortical motor circuitry.
In the developing nervous system, ordered neuronal activity patterns can occur even in the absence of sensory input and to investigate how these arise, we have used the model system of the embryonic chicken spinal motor circuit, focusing on motor neurons of the lateral motor column (LMC). At the earliest stages of their molecular differentiation, we can detect differences between medial and lateral LMC neurons in terms of expression of neurotransmitter receptor subunits, including CHRNA5, CHRNA7, GRIN2A, GRIK1, HTR1A and HTR1B, as well as the KCC2 transporter. Using patch-clamp recordings we also demonstrate that medial and lateral LMC motor neurons have subtly different activity patterns that reflect the differential expression of neurotransmitter receptor subunits. Using a combination of patch-clamp recordings in single neurons and calcium-imaging of motor neuron populations, we demonstrate that inhibition of nicotinic, muscarinic or GABA-ergic activity, has profound effects of motor circuit activity during the initial stages of neuromuscular junction formation. Finally, by analysing the activity of large populations of motor neurons at different developmental stages, we show that the asynchronous, disordered neuronal activity that occurs at early stages of circuit formation develops into organised, synchronous activity evident at the stage of LMC neuron muscle innervation. In light of the considerable diversity of neurotransmitter receptor expression, activity patterns in the LMC are surprisingly similar between neuronal types, however the emergence of patterned activity, in conjunction with the differential expression of transmitter systems likely leads to the development of near-mature patterns of locomotor activity by perinatal ages.
Transcranial direct current stimulation (tDCS) is a non-invasive tool, which effectively modulates behavior, and related brain activity. When applied to the primary motor cortex (M1), tDCS affects motor function, enhancing or decreasing performance of both healthy participants and brain-damaged patients. Beyond M1, the posterior parietal cortex (PPC) is also crucially involved in controlling and guiding movement. Therefore, we explored whether the modulation of cortical excitability within PPC can also affect hand motor function in healthy right-handed participants. In Experiment 1, anodal tDCS (2 mA, 10 min) was applied to PPC and to M1 of both hemispheres. Skilled motor function of the non-dominant left hand, measured using the Jebsen-Taylor Hand Function Test (JTT), improved after anodal tDCS of the right, contralateral M1, as well as after the anodal stimulation of the left, ipsilateral PPC. Conversely, in Experiment 2, cathodal tDCS of the left PPC, or of the right M1, reduced motor performance of the left hand. Finally, Experiment 3 shows that the anodal tDCS of the left PPC selectively facilitated action planning, while the anodal tDCS of the right M1 modulated action execution only. This evidence shows that motor improvement induced by left parietal and right motor stimulations relies on substantial different mechanisms, opening up novel perspectives in the neurorehabilitation of stroke patients with motor and apraxic disorders.
Human cognition and action can be influenced by internal bodily processes such as heartbeats. For instance, somatosensory perception is impaired both during the systolic phase of the cardiac cycle and when heartbeats evoke stronger cortical responses. Here, we test whether these cardiac effects originate from overall changes in cortical excitability. Cortical and corticospinal excitability were assessed using electroencephalographic and electromyographic responses to transcranial magnetic stimulation while concurrently monitoring cardiac activity with electrocardiography. Cortical and corticospinal excitability were found to be highest during systole and following stronger neural responses to heartbeats. Furthermore, in a motor task, hand-muscle activity and the associated desynchronization of sensorimotor oscillations were stronger during systole. These results suggest that systolic cardiac signals have a facilitatory effect on motor excitability-in contrast to sensory attenuation that was previously reported for somatosensory perception. Thus, it is possible that distinct time windows exist across the cardiac cycle, optimizing either perception or action.
Bisphenol F (BPF; 4,4'-dihydroxydiphenylmethane) is one of the most frequently used compounds in the manufacture of plastics and epoxy resins. Previous studies have demonstrated that BPF affects locomotor behavior, oxidative stress, and neurodevelopment in zebrafish. However, its neurotoxic effects are controversial, and the underlying mechanisms are unclear. In order to determine whether BPF affects the motor system, we exposed zebrafish embryos to BPF and assessed behavioral, histological, and neurochemical changes. Spontaneous locomotor behavior and startle response were significantly decreased in BPF-treated zebrafish larvae compared with control larvae. BPF induced motor degeneration and myelination defects in zebrafish larvae. In addition, embryonic exposure to BPF resulted in altered metabolic profiles of neurochemicals, including neurotransmitters and neurosteroids, which may impact locomotion and motor function. In conclusion, exposure to BPF has the potential to affect survival, motor axon length, locomotor activity, myelination, and neurochemical levels of zebrafish larvae.
The thalamus is the hub through which neural signals are transmitted from the basal ganglia and cerebellum to the neocortex. However, thalamocortical axonal activity during motor learning remains largely undescribed. We conducted two-photon calcium imaging of thalamocortical axonal activity in the motor cortex of mice learning a self-initiated lever-pull task. Layer 1 (L1) axons came to exhibit activity at lever-pull initiation and termination, while layer 3 (L3) axons did so at lever-pull initiation. L1 population activity had a sequence structure related to both lever-pull duration and reproducibility. Stimulation of the substantia nigra pars reticulata activated more L1 than L3 axons, whereas deep cerebellar nuclei (DCN) stimulation did the opposite. Lesions to either the dorsal striatum or the DCN impaired motor learning and disrupted temporal dynamics in both layers. Thus, layer-specific thalamocortical signals evolve with the progression of learning, which requires both the basal ganglia and cerebellar activities.
Motor imagery is defined as an act wherein an individual contemplates a mental action of motor execution without apparent action. Mental practice executed by repetitive motor imagery can improve motor performance without simultaneous sensory input or overt output. We aimed to investigate cerebral hemodynamics during motor imagery and motor execution of a self-feeding activity using chopsticks. This study included 21 healthy right-handed volunteers. The self-feeding activity task comprised either motor imagery or motor execution of eating sliced cucumber pickles with chopsticks to examine eight regions of interest: pre-supplementary motor area, supplementary motor area, bilateral prefrontal cortex, premotor area, and sensorimotor cortex. The mean oxyhemoglobin levels were detected using near-infrared spectroscopy to reflect cerebral activation. The mean oxyhemoglobin levels during motor execution were significantly higher in the left sensorimotor cortex than in the supplementary motor area and the left premotor area. Moreover, significantly higher oxyhemoglobin levels were detected in the supplementary motor area and the left premotor area during motor imagery, compared to motor execution. Supplementary motor area and premotor area had important roles in the motor imagery of self-feeding activity. Moreover, the activation levels of the supplementary motor area and the premotor area during motor execution and motor imagery are likely affected by intentional cognitive processes. Levels of cerebral activation differed in some areas during motor execution and motor imagery of a self-feeding activity. This study was approved by the Ethical Review Committee of Nagasaki University (approval No. 18110801) on December 10, 2018.
Intracortical Brain-Computer Interfaces (iBCI) use single-unit activity (SUA), multiunit activity (MUA) and local field potentials (LFP) to control neuroprosthetic devices. SUA and MUA are usually extracted from the bandpassed recording through amplitude thresholding, while subthreshold data are ignored. Here, we show that subthreshold data can actually be decoded to determine behavioral variables with test set accuracy of up to 100%. Although the utility of SUA, MUA and LFP for decoding behavioral variables has been explored previously, this study investigates the utility of spike-band subthreshold activity exclusively. We provide evidence suggesting that this activity can be used to keep decoding performance at acceptable levels even when SUA quality is reduced over time. To the best of our knowledge, the signals that we derive from the subthreshold activity may be the weakest neural signals that have ever been extracted from extracellular neural recordings, while still being decodable with test set accuracy of up to 100%. These results are relevant for the development of fully data-driven and automated methods for amplitude thresholding spike-band extracellular neural recordings in iBCIs containing thousands of electrodes.
In motor neocortex, preparatory activity predictive of specific movements is maintained by a positive feedback loop with the thalamus. Motor thalamus receives excitatory input from the cerebellum, which learns to generate predictive signals for motor control. The contribution of this pathway to neocortical preparatory signals remains poorly understood. Here, we show that, in a virtual reality conditioning task, cerebellar output neurons in the dentate nucleus exhibit preparatory activity similar to that in anterolateral motor cortex prior to reward acquisition. Silencing activity in dentate nucleus by photoactivating inhibitory Purkinje cells in the cerebellar cortex caused robust, short-latency suppression of preparatory activity in anterolateral motor cortex. Our results suggest that preparatory activity is controlled by a learned decrease of Purkinje cell firing in advance of reward under supervision of climbing fiber inputs signaling reward delivery. Thus, cerebellar computations exert a powerful influence on preparatory activity in motor neocortex.
Motor-skill learning induces changes in synaptic structure and function in the primary motor cortex through the involvement of a long-term potentiation- (LTP-) like mechanism. Although there is evidence that calcium-dependent release of gliotransmitters by astrocytes plays an important role in synaptic transmission and plasticity, the role of astrocytes in motor-skill learning is not known. To test the hypothesis that astrocytic activity is necessary for motor-skill learning, we perturbed astrocytic function using pharmacological and genetic approaches. We find that perturbation of astrocytes either by selectively attenuating IP3R2 mediated astrocyte Ca(2+) signaling or using an astrocyte specific metabolic inhibitor fluorocitrate (FC) results in impaired motor-skill learning of a forelimb reaching-task in mice. Moreover, the learning impairment caused by blocking astrocytic activity using FC was rescued by administration of the gliotransmitter D-serine. The learning impairments are likely caused by impaired LTP as FC blocked LTP in slices and prevented motor-skill training-induced increases in synaptic AMPA-type glutamate receptor in vivo. These results support the conclusion that normal astrocytic Ca(2+) signaling during a reaching task is necessary for motor-skill learning.
Limbic brain regions drive goal-directed behaviors. These behaviors often require dynamic motor responses, but the functional connectome of limbic structures in the diencephalon that control locomotion is not well known. The A11 region, within the posterior diencephalon has been postulated to contribute to motor function and control of pain. Here we show that the A11 region initiates movement. Photostimulation of channelrhodopsin 2 (ChR2) transfected neurons in A11 slice preparations showed that neurons could follow stimulation at frequencies of 20 Hz. Our data show that photostimulation of ChR2 transfected neurons in the A11 region enhances motor activity often leading to locomotion. Using vGluT2-reporter and vGAT-reporter mice we show that the A11 tyrosine hydroxylase positive (TH) dopaminergic neurons are vGluT2 and vGAT negative. We find that in addition to dopaminergic neurons within the A11 region, there is another neuronal subtype which expresses the monoenzymatic aromatic L-amino acid decarboxylase (AADC), but not TH, a key enzyme involved in the synthesis of catecholamines including dopamine. This monoaminergic-based motor circuit may be involved in the control of motor behavior as part of a broader diencephalic motor region.
Anatomical, stimulation and lesion data implicate vibrissa motor cortex in whisker motor control. Work on motor cortex has focused on movement generation, but correlations between vibrissa motor cortex activity and whisking are weak. The exact role of vibrissa motor cortex remains unknown. We recorded vibrissa motor cortex neurons during various forms of vibrissal touch, which were invariably associated with whisker protraction and movement. Free whisking, object palpation and social touch all resulted in decreased cortical activity. To understand this activity decrease, we performed juxtacellular recordings, nanostimulation and in vivo whole-cell recordings. Social touch resulted in decreased spiking activity, decreased cell excitability and membrane hyperpolarization. Activation of vibrissa motor cortex by intracortical microstimulation elicited whisker retraction, as if to abort vibrissal touch. Various vibrissa motor cortex inactivation protocols resulted in contralateral protraction and increased whisker movements. These data collectively point to movement suppression as a prime function of vibrissa motor cortex activity.
How motor maps are organized while imagining actions is an intensely debated issue. It is particularly unclear whether motor imagery relies on action-specific representations in premotor and posterior parietal cortices. This study tackled this issue by attempting to decode the content of motor imagery from spatial patterns of Blood Oxygen Level Dependent (BOLD) signals recorded in the frontoparietal motor imagery network. During fMRI-scanning, 20 right-handed volunteers worked on three experimental conditions and one baseline condition. In the experimental conditions, they had to imagine three different types of right-hand actions: an aiming movement, an extension-flexion movement, and a squeezing movement. The identity of imagined actions was decoded from the spatial patterns of BOLD signals they evoked in premotor and posterior parietal cortices using multivoxel pattern analysis. Results showed that the content of motor imagery (i.e., the action type) could be decoded significantly above chance level from the spatial patterns of BOLD signals in both frontal (PMC, M1) and parietal areas (SPL, IPL, IPS). An exploratory searchlight analysis revealed significant clusters motor- and motor-associated cortices, as well as in visual cortices. Hence, the data provide evidence that patterns of activity within premotor and posterior parietal cortex vary systematically with the specific type of hand action being imagined.
Modifying established motor skills is a challenging endeavor due to proactive interference from undesired old to desired new actions, calling for high levels of cognitive control. Motor restrictions may facilitate the modification of motor skills by rendering undesired responses physically impossible, thus reducing demands to response inhibition. Here we studied behavioral and EEG effects of rule changes to typing in skilled touch-typists. The respective rule change-typing without using the left index finger-was either implemented per instruction only or with an additional motor restriction. In both groups, the rule change elicited delays and more errors in typing, indicating the occurrence of proactive interference. While stimulus-locked ERPs did not exhibit prominent effects of rule change or group, response-locked ERPs revealed that the time courses of preparatory brain activity preceding typing responses depended on the presence of motor restriction. Although further research is necessary to corroborate our findings, they indicate a novel brain correlate that represents changes in inhibitory response preparation induced by short-term motor restrictions.
The ability to learn motor skills implicates an improvement in accuracy, speed and consistency of movements. Motor control is related to movement execution and involves corticospinal neurons (CSp), which are broadly distributed in layer 5B of the motor and somatosensory cortices. CSp neurons innervate the spinal cord and are functionally diverse. However, whether CSp activity differs between different cortical areas throughout motor learning has been poorly explored. Given the importance and interaction between primary motor (M1) and somatosensory (S1) cortices related to movement, we examined the functional roles of CSp neurons in both areas. We induced the expression of GCaMP7s calcium indicator to perform photometric calcium recordings from layer 5B CSp neurons simultaneously in M1 and S1 cortices and track their activity while adult mice learned and performed a cued lever-press task. We found that during early learning sessions, the population calcium activity of CSp neurons in both cortices during movement did not change significantly. In late learning sessions the peak amplitude and duration of calcium activity CSp neurons increased in both, M1 and S1 cortices. However, S1 and M1 CSp neurons display a different temporal dynamic during movements that occurred when animals learned the task; both M1 and S1 CSp neurons activate before movement initiation, however, M1 CSp neurons continue active during movement performance, reinforcing the idea of the diversity of the CSp system and suggesting that CSp neuron activity in M1 and S1 cortices throughout motor learning have different functional roles for sensorimotor integration.
With disease-modifying approaches under evaluation in ataxia-telangiectasia and other ataxias, there is a need for objective and reliable biomarkers of free-living motor function. In this study, we test the hypothesis that metrics derived from a single wrist sensor worn at home provide accurate, reliable, and interpretable information about neurological disease severity in children with A-T.A total of 15 children with A-T and 15 age- and sex-matched controls wore a sensor with a triaxial accelerometer on their dominant wrist for 1 week at home. Activity intensity measures, derived from the sensor data, were compared with in-person neurological evaluation on the Brief Ataxia Rating Scale (BARS) and performance on a validated computer mouse task.Children with A-T were inactive the same proportion of each day as controls but produced more low intensity movements (p < 0.01; Cohen's d = 1.48) and fewer high intensity movements (p < 0.001; Cohen's d = 1.71). The range of activity intensities was markedly reduced in A-T compared to controls (p < 0.0001; Cohen's d = 2.72). The activity metrics correlated strongly with arm, gait, and total clinical severity (r: 0.71-0.87; p < 0.0001), correlated with specific computer task motor features (r: 0.67-0.92; p < 0.01), demonstrated high reliability (r: 0.86-0.93; p < 0.00001), and were not significantly influenced by age in the healthy control group.Motor activity metrics from a single, inexpensive wrist sensor during free-living behavior provide accurate and reliable information about diagnosis, neurological disease severity, and motor performance. These low-burden measurements are applicable independent of ambulatory status and are potential digital behavioral biomarkers in A-T.
The rotenone-induced animal model of Parkinson's disease (PD) has been used to investigate the pathogenesis of PD. Oxidative stress is one of the main contributors of neurodegeneration in PD. Flavonoids have the potential to modulate neuronal function and combat various neurodegenerative diseases. The pre- and post-supplementation of quercetin (50 mg/kg, p.o) was done in rats injected with rotenone (1.5 mg/kg, s.c). After the treatment, behavioral activities were monitored for motor activity, depression-like behavior, and cognitive changes. Rats were decapitated after behavioral analysis and the brain samples were dissected out for neurochemical and biochemical estimation. Results showed that supplementation of quercetin significantly (p<0.01) restored rotenone-induced motor and non-motor deficits (depression and cognitive impairments), enhanced antioxidant enzyme activities (p<0.01), and attenuated neurotransmitter alterations (p<0.01). It is suggested that quercetin supplementation improves neurotransmitter levels by mitigating oxidative stress via increasing antioxidant enzyme activity and hence improves motor activity, cognitive functions, and reduces depressive behavior. The results of the present study showed that quercetin pre-supplementation produced more significant results as compared to post-supplementation. These findings show that quercetin can be a potential therapeutic agent to reduce the risk and progression of PD.
Enhancements in motor performance have been demonstrated in response to intense stimuli both in healthy subjects and in the form of 'paradoxical kinesis' in patients with Parkinson's disease. Here we identify a mid-latency evoked potential in local field potential recordings from the region of the subthalamic nucleus, which scales in amplitude with both the intensity of the stimulus delivered and corresponding enhancements in biomechanical measures of maximal handgrips, independent of the dopaminergic state of our subjects with Parkinson's disease. Recordings of a similar evoked potential in the related pedunculopontine nucleus - a key component of the reticular activating system - provide support for this neural signature in the subthalmic nucleus being a novel correlate of ascending arousal, propagated from the reticular activating system to exert an 'energizing' influence on motor circuitry. Future manipulation of this system linking arousal and motor performance may provide a novel approach for the non-dopaminergic enhancement of motor performance in patients with hypokinetic disorders such as Parkinson's disease.
A need-supportive environment can provide various motivational benefits to impact children's psychomotor developmental levels. However, very little is known about the effects of need-supportive motor skill intervention on children's motor skill competence and physical activity by gender. Guided by self-determination theory (SDT), this study aimed to (a) investigate the effect of a need-supportive fundamental movement skill (FMS) program on children's FMS competence and moderate-to-vigorous physical activity (MVPA), and (b) explore potential gender differences in these effects. Thirty-six children (63.8% girls; Mage = 6.52 ± 0.97) participated and were divided into two groups: an intervention group (24 need-supportive FMS sessions over eight weeks) and a control group. A repeated-measures multivariate analysis of variance (MANOVA) was used to examine the influence of the motor skill intervention on FMS competence and MVPA over time by group (intervention, control) and gender (boys, girls). The results showed (a) significant group differences between the intervention and control group in FMS competence and MVPA (p < 0.001), (b) non-significant gender differences between boys and girls in FMS competence and MVPA (p = 0.85), and (c) non-significant interaction effects over time (p = 0.52). The findings highlight that a need-supportive FMS program may enhance FMS development and daily physical activity for both genders during the early school years.
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