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The Journal of Neuroscience : the... Apr 2021It is generally supposed that primary motor cortex (M1) receives somatosensory input predominantly via primary somatosensory cortex (S1). However, a growing body of...
It is generally supposed that primary motor cortex (M1) receives somatosensory input predominantly via primary somatosensory cortex (S1). However, a growing body of evidence indicates that M1 also receives direct sensory input from the thalamus, independent of S1; such direct input is particularly evident at early ages before M1 contributes to motor control. Here, recording extracellularly from the forelimb regions of S1 and M1 in unanesthetized rats at postnatal day (P)8 and P12, we compared S1 and M1 responses to self-generated (i.e., reafferent) forelimb movements during active sleep and wake, and to other-generated (i.e., exafferent) forelimb movements. At both ages, reafferent responses were processed in parallel by S1 and M1; in contrast, exafferent responses were processed in parallel at P8 but serially, from S1 to M1, at P12. To further assess this developmental difference in processing, we compared exafferent responses to proprioceptive and tactile stimulation. At both P8 and P12, proprioceptive stimulation evoked parallel responses in S1 and M1, whereas tactile stimulation evoked parallel responses at P8 and serial responses at P12. Independent of the submodality of exafferent stimulation, pairs of S1-M1 units exhibited greater coactivation during active sleep than wake. These results indicate that S1 and M1 independently develop somatotopy before establishing the interactive relationship that typifies their functionality in adults. Learning any new motor task depends on the ability to use sensory information to update motor outflow. Thus, to understand motor learning, we must also understand how animals process sensory input. Primary somatosensory cortex (S1) and primary motor cortex (M1) are two interdependent structures that process sensory input throughout life. In adults, the functional relationship between S1 and M1 is well established; however, little is known about how S1 and M1 begin to transmit or process sensory information in early life. In this study, we investigate the early development of S1 and M1 as a sensory processing unit. Our findings provide new insights into the fundamental principles of sensory processing and the development of functional connectivity between these important sensorimotor structures.
Topics: Animals; Female; Forelimb; Male; Motor Cortex; Movement; Rats; Rats, Sprague-Dawley; Sleep; Somatosensory Cortex; Touch Perception; Wakefulness
PubMed: 33622773
DOI: 10.1523/JNEUROSCI.2614-20.2021 -
Human Brain Mapping May 2022Sensorimotor coordination requires orchestrated network activity in the brain, mediated by inter- and intra-hemispheric interactions that may be affected by...
Sensorimotor coordination requires orchestrated network activity in the brain, mediated by inter- and intra-hemispheric interactions that may be affected by aging-related changes. We adopted a theoretical model, according to which intra-hemispheric inhibition from premotor to primary motor cortex is mandatory to compensate for inter-hemispheric excitation through the corpus callosum. To test this as a function of age we acquired electroencephalography (EEG) simultaneously with functional magnetic resonance imaging (fMRI) in two groups of healthy adults (younger N = 13: 20-25 year and older N = 14: 59-70 year) while learning a unimanual motor task. On average, quality of performance of older participants stayed significantly below that of the younger ones. Accompanying decreases in motor-event-related EEG β-activity were lateralized toward contralateral motor regions, albeit more so in younger participants. In this younger group, the mean β-power during motor task execution was significantly higher in bilateral premotor areas compared to the older adults. In both groups, fMRI blood oxygen level dependent (BOLD) signals were positively correlated with source-reconstructed β-amplitudes: positive in primary motor and negative in premotor cortex. This suggests that β-amplitude modulation is associated with primary motor cortex "activation" (positive BOLD response) and premotor "deactivation" (negative BOLD response). Although the latter results did not discriminate between age groups, they underscore that enhanced modulation in primary motor cortex may be explained by a β-associated excitatory crosstalk between hemispheres.
Topics: Aged; Aging; Cohort Studies; Electroencephalography; Humans; Magnetic Resonance Imaging; Motor Cortex
PubMed: 35133058
DOI: 10.1002/hbm.25791 -
Journal of Neurophysiology Sep 2017Primary motor cortex has been studied for more than a century, yet a consensus on its functional contribution to movement control is still out of reach. In particular,... (Review)
Review
Primary motor cortex has been studied for more than a century, yet a consensus on its functional contribution to movement control is still out of reach. In particular, there remains controversy as to the level of control produced by motor cortex ("low-level" movement dynamics vs. "high-level" movement kinematics) and the role of sensory feedback. In this review, we present different perspectives on the two following questions: What does activity in motor cortex reflect? and How do planned motor commands interact with incoming sensory feedback during movement? The four authors each present their independent views on how they think the primary motor cortex (M1) controls movement. At the end, we present a dialogue in which the authors synthesize their views and suggest possibilities for moving the field forward. While there is not yet a consensus on the role of M1 or sensory feedback in the control of upper limb movements, such dialogues are essential to take us closer to one.
Topics: Animals; Biomechanical Phenomena; Feedback, Physiological; Humans; Motor Cortex; Movement
PubMed: 28615340
DOI: 10.1152/jn.00795.2016 -
Proceedings of the National Academy of... Apr 2023Corticostriatal activity is an appealing target for nonpharmacological treatments of brain disorders. In humans, corticostriatal activity may be modulated with...
Corticostriatal activity is an appealing target for nonpharmacological treatments of brain disorders. In humans, corticostriatal activity may be modulated with noninvasive brain stimulation (NIBS). However, a NIBS protocol with a sound neuroimaging measure demonstrating a change in corticostriatal activity is currently lacking. Here, we combine transcranial static magnetic field stimulation (tSMS) with resting-state functional MRI (fMRI). We first present and validate the ISAAC analysis, a well-principled framework that disambiguates functional connectivity between regions from local activity within regions. All measures of the framework suggested that the region along the medial cortex displaying greater functional connectivity with the striatum is the supplementary motor area (SMA), where we applied tSMS. We then use a data-driven version of the framework to show that tSMS of the SMA modulates the local activity in the SMA proper, in the adjacent sensorimotor cortex, and in the motor striatum. We finally use a model-driven version of the framework to clarify that the tSMS-induced modulation of striatal activity can be primarily explained by a change in the shared activity between the modulated motor cortical areas and the motor striatum. These results suggest that corticostriatal activity can be targeted, monitored, and modulated noninvasively in humans.
Topics: Humans; Corpus Striatum; Sensorimotor Cortex; Neostriatum; Motor Cortex; Transcranial Magnetic Stimulation; Magnetic Resonance Imaging
PubMed: 37023134
DOI: 10.1073/pnas.2219693120 -
Journal of Visualized Experiments : JoVE Jul 2019Mapping the motor cortex with transcranial magnetic stimulation (TMS) has potential to interrogate motor cortex physiology and plasticity but carries unique challenges...
Mapping the motor cortex with transcranial magnetic stimulation (TMS) has potential to interrogate motor cortex physiology and plasticity but carries unique challenges in children. Similarly, transcranial direct current stimulation (tDCS) can improve motor learning in adults but has only recently been applied to children. The use of tDCS and emerging techniques like high-definition tDCS (HD-tDCS) require special methodological considerations in the developing brain. Robotic TMS motor mapping may confer unique advantages for mapping, particularly in the developing brain. Here, we aim to provide a practical, standardized approach for two integrated methods capable of simultaneously exploring motor cortex modulation and motor maps in children. First, we describe a protocol for robotic TMS motor mapping. Individualized, MRI-navigated 12x12 grids centered on the motor cortex guide a robot to administer single-pulse TMS. Mean motor evoked potential (MEP) amplitudes per grid point are used to generate 3D motor maps of individual hand muscles with outcomes including map area, volume, and center of gravity. Tools to measure safety and tolerability of both methods are also included. Second, we describe the application of both tDCS and HD-tDCS to modulate the motor cortex and motor learning. An experimental training paradigm and sample results are described. These methods will advance the application of non-invasive brain stimulation in children.
Topics: Adult; Brain Mapping; Evoked Potentials, Motor; Hand; Humans; Magnetic Resonance Imaging; Motor Cortex; Muscle, Skeletal; Robotics; Transcranial Direct Current Stimulation; Transcranial Magnetic Stimulation
PubMed: 31305529
DOI: 10.3791/59594 -
Movement Disorders : Official Journal... Nov 2018There is abundant evidence that the pathophysiology of Parkinson's disease (PD) is not confined to the nigrostriatal dopaminergic pathway but propagates along the... (Review)
Review
There is abundant evidence that the pathophysiology of Parkinson's disease (PD) is not confined to the nigrostriatal dopaminergic pathway but propagates along the cortico-basal ganglia-thalamo-cortical neural network. A critical node in this functional circuit impacted by PD is the primary motor cortex (M1), which plays a key role in generating neural impulses that regulate movements. The past several decades have lay witness to numerous in vivo neuroimaging techniques that provide a window into the function and structure of M1. A consistent observation from numerous studies is that during voluntary movement, but also at rest, the functional activity of M1 is altered in PD relative to healthy individuals, and it relates to many of the motor signs. Although this abnormal functional activity can be partially restored with acute dopaminergic medication, it continues to deteriorate with disease progression and may predate structural degeneration of M1. The current review discusses the evidence that M1 is fundamental to the pathophysiology of PD, as measured by neuroimaging techniques such as positron emission tomography, single-photon emission computed tomography, electroencephalography, magnetoencephalography, and functional and structural MRI. Although novel treatments that target the cortex will not cure PD, they could significantly slow down and alter the progressive course of the disease and thus improve clinical care for this degenerative disease. © 2018 The Authors. Movement Disorders published by Wiley Periodicals, Inc. on behalf of International Parkinson and Movement Disorder Society.
Topics: Animals; Basal Ganglia; Humans; Motor Cortex; Neuroimaging; Parkinson Disease
PubMed: 30280416
DOI: 10.1002/mds.102 -
Cerebellum (London, England) Jun 2017Transcranial magnetic and electric stimulation of the brain are novel and highly promising techniques currently employed in both research and clinical practice.... (Review)
Review
Transcranial magnetic and electric stimulation of the brain are novel and highly promising techniques currently employed in both research and clinical practice. Improving or rehabilitating brain functions by modulating excitability with these noninvasive tools is an exciting new area in neuroscience. Since the cerebellum is closely connected with the cerebral regions subserving motor, associative, and affective functions, the cerebello-thalamo-cortical pathways are an interesting target for these new techniques. Targeting the cerebellum represents a novel way to modulate the excitability of remote cortical regions and their functions. This review brings together the studies that have applied cerebellar stimulation, magnetic and electric, and presents an overview of the current knowledge and unsolved issues. Some recommendations for future research are implemented as well.
Topics: Cerebellum; Electric Stimulation; Humans; Motor Cortex; Recovery of Function; Rehabilitation; Transcranial Magnetic Stimulation
PubMed: 28032321
DOI: 10.1007/s12311-016-0840-7 -
Journal of Neurophysiology Feb 2021The mammalian motor cortex is topographically organized into representations of discrete body parts (motor maps). Studies in adult rats using long-duration intracortical...
The mammalian motor cortex is topographically organized into representations of discrete body parts (motor maps). Studies in adult rats using long-duration intracortical microstimulation (LD-ICMS) reveal that forelimb motor cortex is functionally organized into several spatially distinct areas encoding complex, multijoint movement sequences: elevate, advance, grasp, and retract. The topographical arrangement of complex movements during development and the influence of skilled learning are unknown. Here, we determined the emergence and topography of complex forelimb movement representations in rats between () and . We further investigated the expression of the maps for complex movements under conditions of reduced cortical inhibition and whether skilled forelimb motor training could alter their developing topography. We report that simple forelimb movements are first evoked at and are confined to the caudal forelimb area (CFA), whereas complex movements first reliably appear at and are observed in both the caudal and rostral forelimb areas (RFA). During development, the topography of complex movement representations undergoes reorganization with "grasp" and "elevate" movements predominantly observed in the RFA and all four complex movements observed in CFA. Under reduced cortical inhibition, simple and complex movements were first observed in the CFA on and , respectively, and the topography is altered relative to a saline control. Further, skilled motor learning was associated with increases in "grasp" and "retract" representations specific to the trained limb. Our results demonstrate that early-life motor experience during development can modify the topography of complex forelimb movement representations. The motor cortex is topographically organized into maps of different body parts. We used to think that the function of motor cortex was to drive individual muscles, but more recently we have learned that it is also organized to make complex movements. However, the development and plasticity of those complex movements is completely unknown. In this paper, the emergence and topography of complex movement representation, as well as their plasticity during development, is detailed.
Topics: Animals; Evoked Potentials, Motor; Forelimb; Male; Motor Cortex; Motor Skills; Neural Inhibition; Neurogenesis; Neuronal Plasticity; Rats; Rats, Long-Evans
PubMed: 33471611
DOI: 10.1152/jn.00531.2020 -
Progress in Neurobiology Sep 2023The ventral premotor cortex (PMv) is an important component of cortico-cortical pathways mediating prefrontal control over primary motor cortex (M1) function. Paired...
The ventral premotor cortex (PMv) is an important component of cortico-cortical pathways mediating prefrontal control over primary motor cortex (M1) function. Paired associative stimulation (ccPAS) is known to change PMv influence over M1 in humans, which manifests differently depending on the behavioural context. Here we show that these changes in influence are functionally linked to PMv-M1 phase synchrony changes induced by repeated paired stimulation of the two areas. PMv-to-M1 ccPAS leads to increased phase synchrony in alpha and beta bands, while reversed order M1-to-PMv ccPAS leads to decreased theta phase synchrony. These changes are visible at rest but are predictive of changes in oscillatory power in the same frequencies during movement execution and inhibition, respectively. The results unveil a link between the physiology of the motor network and the resonant frequencies mediating its interactions and provide a putative mechanism underpinning the relationship between synaptic efficacy and brain oscillations.
Topics: Humans; Motor Cortex; Transcranial Magnetic Stimulation; Neural Pathways; Movement; Communication
PubMed: 37353108
DOI: 10.1016/j.pneurobio.2023.102487 -
Nature Reviews. Neuroscience Aug 2020The human motor cortex comprises a microcircuit of five interconnected layers with different cell types. In this Review, we use a layer-specific and cell-specific... (Review)
Review
The human motor cortex comprises a microcircuit of five interconnected layers with different cell types. In this Review, we use a layer-specific and cell-specific approach to integrate physiological accounts of this motor cortex microcircuit with the pathophysiology of neurodegenerative diseases affecting motor functions. In doing so we can begin to link motor microcircuit pathology to specific disease stages and clinical phenotypes. Based on microcircuit physiology, we can make future predictions of axonal loss and microcircuit dysfunction. With recent advances in high-resolution neuroimaging we can then test these predictions in humans in vivo, providing mechanistic insights into neurodegenerative disease.
Topics: Animals; Humans; Motor Cortex; Neural Pathways; Neurodegenerative Diseases
PubMed: 32555340
DOI: 10.1038/s41583-020-0315-1