Spatio-Temporal Patterning in Primary Motor Cortex at Movement Onset.
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ABSTRACT:
SUBMITTER: Best MD
PROVIDER: S-EPMC6375055 | biostudies-literature | 2017 Feb
REPOSITORIES: biostudies-literature
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Project description:A complex action can be described as the composition of a set of elementary movements. While both kinematic and dynamic elements have been proposed to compose complex actions, the structure of movement decomposition and its neural representation remain unknown. Here, we examined movement decomposition by modeling the temporal dynamics of neural populations in the primary motor cortex of macaque monkeys performing forelimb reaching movements. Using a hidden Markov model, we found that global transitions in the neural population activity are associated with a consistent segmentation of the behavioral output into acceleration and deceleration epochs with directional selectivity. Single cells exhibited modulation of firing rates between the kinematic epochs, with abrupt changes in spiking activity timed with the identified transitions. These results reveal distinct encoding of acceleration and deceleration phases at the level of M1, and point to a specific pattern of movement decomposition that arises from the underlying neural activity. A similar approach can be used to probe the structure of movement decomposition in different brain regions, possibly controlling different temporal scales, to reveal the hierarchical structure of movement composition.
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Project description:Before primary motor cortex (M1) develops its motor functions, it functions like a somatosensory area. Here, by recording from neurons in the forelimb representation of M1 in postnatal day (P) 8-12 rats, we demonstrate a rapid shift in its sensory responses. At P8-10, M1 neurons respond overwhelmingly to feedback from sleep-related twitches of the forelimb, but the same neurons do not respond to wake-related movements. By P12, M1 neurons suddenly respond to wake movements, a transition that results from opening the sensory gate in the external cuneate nucleus. Also at P12, fewer M1 neurons respond to individual twitches, but the full complement of twitch-related feedback observed at P8 is unmasked through local disinhibition. Finally, through P12, M1 sensory responses originate in the deep thalamorecipient layers, not primary somatosensory cortex. These findings demonstrate that M1 initially establishes a sensory framework upon which its later-emerging role in motor control is built.
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Project description:Abnormalities in the movement-related activation of the primary motor cortex (M1) are thought to be a major contributor to the motor signs of Parkinson's disease. The existing evidence, however, variably indicates that M1 is under-activated with movement, overactivated (due to a loss of functional specificity) or activated with abnormal timing. In addition, few models consider the possibility that distinct cortical neuron subtypes may be affected differently. Those gaps in knowledge were addressed by studying the extracellular activity of antidromically-identified lamina 5b pyramidal-tract type neurons (n = 153) and intratelencephalic-type corticostriatal neurons (n = 126) in the M1 of two monkeys as they performed a step-tracking arm movement task. We compared movement-related discharge before and after the induction of parkinsonism by administration of MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) and quantified the spike rate encoding of specific kinematic parameters of movement using a generalized linear model. The fraction of M1 neurons with movement-related activity declined following MPTP but only marginally. The strength of neuronal encoding of parameters of movement was reduced markedly (mean 29% reduction in the coefficients from the generalized linear model). This relative decoupling of M1 activity from kinematics was attributable to reductions in the coefficients that estimated the spike rate encoding of movement direction (-22%), speed (-40%), acceleration (-49%) and hand position (-33%). After controlling for MPTP-induced changes in motor performance, M1 activity related to movement itself was reduced markedly (mean 36% hypoactivation). This reduced activation was strong in pyramidal tract-type neurons (-50%) but essentially absent in corticostriatal neurons. The timing of M1 activation was also abnormal, with earlier onset times, prolonged response durations, and a 43% reduction in the prevalence of movement-related changes beginning in the 150-ms period that immediately preceded movement. Overall, the results are consistent with proposals that under-activation and abnormal timing of movement-related activity in M1 contribute to parkinsonian motor signs but are not consistent with the idea that a loss of functional specificity plays an important role. Given that pyramidal tract-type neurons form the primary efferent pathway that conveys motor commands to the spinal cord, the dysfunction of movement-related activity in pyramidal tract-type neurons is likely to be a central factor in the pathophysiology of parkinsonian motor signs.
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Project description:Motor cortical beta oscillations have been reported for decades, yet their behavioral correlates remain unresolved. Some studies link beta oscillations to changes in underlying neural activity, but the specific behavioral manifestations of these reported changes remain elusive. To investigate how changes in population neural activity, beta oscillations, and behavior are linked, we recorded multi-scale neural activity from motor cortex while three macaques performed a novel neurofeedback task. Subjects volitionally brought their beta oscillatory power to an instructed state and subsequently executed an arm reach. Reaches preceded by a reduction in beta power exhibited significantly faster movement onset times than reaches preceded by an increase in beta power. Further, population neural activity was found to shift farther from a movement onset state during beta oscillations that were neurofeedback-induced or naturally occurring during reaching tasks. This finding establishes a population neural basis for slowed movement onset following periods of beta oscillatory activity.
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Project description:Motor performance is improved by stimulation of the agonist muscle during movement. However, related brain mechanisms remain unknown. In this work, we perform a functional magnetic resonance imaging (fMRI) study in 21 healthy subjects under three different conditions: (1) movement of right ankle alone; (2) movement and simultaneous stimulation of the agonist muscle; or (3) movement and simultaneous stimulation of a control area. We constructed weighted brain networks for each condition by using functional connectivity. Network features were analyzed using graph theoretical approaches. We found that: (1) the second condition evokes the strongest and most widespread brain activations (5147 vs. 4419 and 2320 activated voxels); and (2) this condition also induces a unique network layout and changes hubs and the modular structure of the brain motor network by activating the most "silent" links between primary somatosensory centers and the motor cortex, particularly weak links from the thalamus to the left primary motor cortex (M1). Significant statistical differences were found when the strength values of the right cerebellum (P < 0.001) or the left thalamus (P = 0.006) were compared among the three conditions. Over the years, studies reported a small number of projections from the thalamus to the motor cortex. This is the first work to present functions of these pathways. These findings reveal mechanisms for enhancing motor function with somatosensory stimulation, and suggest that network function cannot be thoroughly understood when weak ties are disregarded.
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Project description:Pyramidal tract neurons (PTNs) within macaque rostral ventral premotor cortex (F5) and (M1) provide direct input to spinal circuitry and are critical for skilled movement control. Contrary to initial hypotheses, they can also be active during action observation, in the absence of any movement. A population-level understanding of this phenomenon is currently lacking. We recorded from single neurons, including identified PTNs, in (M1) (n = 187), and F5 (n = 115) as two adult male macaques executed, observed, or withheld (NoGo) reach-to-grasp actions. F5 maintained a similar representation of grasping actions during both execution and observation. In contrast, although many individual M1 neurons were active during observation, M1 population activity was distinct from execution, and more closely aligned to NoGo activity, suggesting this activity contributes to withholding of self-movement. M1 and its outputs may dissociate initiation of movement from representation of grasp in order to flexibly guide behaviour.
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Project description:Background:Spatio-temporal patterns of movement can characterize relationships between organisms and their surroundings, and address gaps in our understanding of species ecology, activity budgets, bioenergetics, and habitat resource management. Highly mobile waterfowl, which can exploit resources over large spatial extents, are excellent models to understand relationships between movements and resource usage, landscape interactions and specific habitat needs. Methods:We tracked 3 species of dabbling ducks with GPS-GSM transmitters in 2015-17 to examine fine-scale movement patterns over 24?h periods (30?min interval), dividing movement pathways into temporally continuous segments and spatially contiguous patches. We quantified distances moved, area used and time allocated across the day, using linear and generalized linear mixed models. We investigated behavior through relationships between these variables. Results:Movements and space-use were small, and varied by species, sex and season. Gadwall (Mareca strepera) generally moved least (FFDs: 0.5-0.7?km), but their larger foraging patches resulted from longer within-area movements. Pintails (Anas acuta) moved most, were more likely to conduct flights >?300?m, had FFDs of 0.8-1.1?km, used more segments and patches per day that they revisited more frequently, resulting in the longest daily total movements. Females and males differed only during the post-hunt season when females moved more. 23.6% of track segments were short duration (1-2 locations), approximately 1/3 more than would be expected if they occurred randomly, and were more dispersed in the landscape than longer segments. Distance moved in 30?min shortened as segment duration increased, likely reflecting phases of non-movement captured within segments. Conclusions:Pacific Flyway ducks spend the majority of time using smaller foraging and resting areas than expected or previously reported, implying that foraging areas may be highly localized, and nutrients obtainable from smaller areas. Additionally, movement reductions over time demonstrates behavioral adjustments that represent divergent energetic demands, the detection of which is a key advantage of higher frequency data. Ducks likely use less energy for movement than currently predicted and management, including distribution and configuration of essential habitat, may require reconsideration. Our study illustrates how fine-scale movement data from tracking help understand and inform various other fields of research.
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