scholarly journals Predictive encoding of motor behavior in the supplementary motor area is disrupted in parkinsonism

2018 ◽  
Vol 120 (3) ◽  
pp. 1247-1255 ◽  
Author(s):  
Claudia M. Hendrix ◽  
Brett A. Campbell ◽  
Benjamin J. Tittle ◽  
Luke A. Johnson ◽  
Kenneth B. Baker ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Motor Behavior ◽  
Activity Patterns ◽  
Movement Planning ◽  
Motor Area ◽  
Beta Band ◽  
Reaching Task ◽  
Cortical Areas ◽  
Trial Basis

Many studies suggest that Parkinson’s disease (PD) is associated with changes in neuronal activity patterns throughout the basal ganglia-thalamocortical motor circuit. There are limited electrophysiological data, however, describing how parkinsonism impacts the presupplementary motor area (pre-SMA) and SMA proper (SMAp), cortical areas known to be involved in movement planning and motor control. In this study, local field potentials (LFPs) were recorded in the pre-SMA/SMAp of a nonhuman primate during a visually cued reaching task. Recordings were made in the same subject in both the naive and parkinsonian state using the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of parkinsonism. We found that in the naive animal, well before a go-cue providing instruction of reach onset and direction was given, LFP activity was dynamically modulated in both high (20–30 Hz) and low beta (10–20 Hz) bands, and the magnitude of this modulation (e.g., decrease/increase in beta amplitude for each band, respectively) correlated linearly with reaction time (RT) on a trial-to-trial basis, suggesting it may predictively encode for RT. Consistent with this hypothesis, we observed that this activity was more prominent within the pre-SMA compared with SMAp. In the parkinsonian state, however, pre-SMA/SMAp beta band modulation was disrupted, particularly in the high beta band, such that the predictive encoding of RT was significantly diminished. In addition, the predictive encoding of RT preferentially within pre-SMA over SMAp was lost. These findings add to our understanding of the role of pre-SMA/SMAp in motor behavior and suggest a fundamental role of these cortical areas in early preparatory and premovement processes that are altered in parkinsonism. NEW & NOTEWORTHY Goal-directed movements, such as reaching for an object, necessitate temporal preparation and organization of information processing within the basal ganglia-thalamocortical motor network. Impaired movement in parkinsonism is thought to be the result of pathophysiological activity disrupting information flow within this network. This work provides neurophysiological evidence linking altered motor preplanning processes encoded in pre-SMA/SMAp beta band modulation to the pathogenesis of motor disturbances in parkinsonism.

Involvement of Subcortical Structures in the Preparation of Self-Paced Movement

2004 ◽  
Vol 18 (2/3) ◽  
pp. 130-139 ◽  
Author(s):  
Guillermo Paradiso ◽  
Danny Cunic ◽  
Robert Chen
Keyword(s):  
Parkinson’S Disease ◽  
Parkinson's Disease ◽  
Basal Ganglia ◽  
Onset Time ◽  
Movement Planning ◽  
Movement Preparation ◽  
Subcortical Structures ◽  
Postoperative Mri ◽  
Deep Brain

Abstract Although it has long been suggested that the basal ganglia and thalamus are involved in movement planning and preparation, there was little direct evidence in humans to support this hypothesis. Deep brain stimulation (DBS) is a well-established treatment for movement disorders such as Parkinson's disease, tremor, and dystonia. In patients undergoing DBS surgery, we recorded simultaneously from scalp contacts and from electrodes surgically implanted in the subthalamic nucleus (STN) of 13 patients with Parkinson's disease and in the “cerebellar” thalamus of 5 patients with tremor. The aim of our studies was to assess the role of the cortico-basal ganglia-thalamocortical loop through the STN and the cerebello-thalamocortical circuit through the “cerebellar” thalamus in movement preparation. The patients were asked to perform self-paced wrist extension movements. All subjects showed a cortical readiness potential (RP) with onset ranging between 1.5 to 2s before the onset of movement. Subcortical RPs were recorded in 11 of 13 with electrodes in the STN and in 4 of 5 patients with electrodes in the thalamus. The onset time of the STN and thalamic RPs were not significantly different from the onset time of the scalp RP. The STN and thalamic RPs were present before both contralateral and ipsilateral hand movements. Postoperative MRI studies showed that contacts with maximum RP amplitude generally were inside the target nucleus. These findings indicate that both the basal ganglia and the cerebellar circuits participate in movement preparation in parallel with the cortex.

Role of the Human Rostral Supplementary Motor Area and the Basal Ganglia in Motor Sequence Control: Investigations With H2 15O PET

1998 ◽  
Vol 79 (2) ◽  
pp. 1070-1080 ◽  
Author(s):  
H. Boecker ◽  
A. Dagher ◽  
A. O. Ceballos-Baumann ◽  
R. E. Passingham ◽  
M. Samuel ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Primary Motor Cortex ◽  
Supplementary Motor Area ◽  
Motor Area ◽  
Anterior Cingulate ◽  
Central Control ◽  
Motor Sequence ◽  
Finger Movements ◽  
Sequence Complexity

Boecker, H., A. Dagher, A. O. Ceballos-Baumann, R. E. Passingham, M. Samuel, K. J. Friston, J.-B. Poline, C. Dettmers, B. Conrad, and D. J. Brooks. Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: investigations with H2 15O PET. J. Neurophysiol. 79: 1070–1080, 1998. The aim of this study was to investigate the functional anatomy of distributed cortical and subcortical motor areas in the human brain that participate in the central control of overlearned complex sequential unimanual finger movements. On the basis of previous research in nonhuman primates, a principal involvement of basal ganglia (medial premotor loops) was predicted for central control of finger sequences performed automatically. In pertinent areas, a correlation of activation levels with the complexity of a motor sequence was hypothesized. H2 15O positron emission tomography (PET) was used in a group of seven healthy male volunteers [mean age 32.0 ± 10.4 yr] to determine brain regions where levels of regional cerebral blood flow (rCBF) correlated with graded complexity levels of five different key-press sequences. All sequences were overlearned before PET and involved key-presses of fingers II–V of the right hand. Movements of individual fingers were kept constant throughout all five conditions by external pacing at 1-Hz intervals. Positive correlations of rCBF with increasing sequence complexity were identified in the contralateral rostral supplementary motor area (pre-SMA) and the associated pallido-thalamic loop, as well as in right parietal area 7 and ipsilateral primary motor cortex (M1). In contrast, while rCBF in contralateral M1 and and extensive parts of caudal SMA was increased compared with rest during task performance, significant correlated increases of rCBF with sequence complexity were not observed. Inverse correlations of rCBF with increasing sequence complexity were identified in mesial prefrontal-, medial temporal-, and anterior cingulate areas. The findings provide further evidence in humans supporting the notion of a segregation of SMA into functionally distinct subcomponents: although pre-SMA was differentially activated depending on the complexity of a sequence of learned finger movements, such modulation was not detectable in caudal SMA (except the most antero-superior part), implicating a motor executive role. Our observations of complexity-correlated rCBF increases in anterior globus palllidus suggest a specific role for the basal ganglia in the process of sequence facilitation and control. They may act to filter and focus input from motor cortical areas as patterns of action become increasingly complex.

P449 The role of rostral supplementary motor area and basal ganglia in motor sequence control

1996 ◽  
Vol 99 (4) ◽  
pp. 379
Author(s):  
H. Boecker ◽  
A. Dagher ◽  
A. Ceballos-Baumann ◽  
R.E. Passingham ◽  
M. Samuel ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Supplementary Motor Area ◽  
Motor Area ◽  
Motor Sequence

Role of the Basal Ganglia in the Control of Purposive Saccadic Eye Movements

2000 ◽  
Vol 80 (3) ◽  
pp. 953-978 ◽  
Author(s):  
Okihide Hikosaka ◽  
Yoriko Takikawa ◽  
Reiko Kawagoe
Keyword(s):  
Eye Movements ◽  
Basal Ganglia ◽  
Saccadic Eye Movements ◽  
Behavioral Adaptation ◽  
Inhibitory Input ◽  
Behavioral Context ◽  
Critical Determinant ◽  
Cortical Areas ◽  
Cortical Inputs

In addition to their well-known role in skeletal movements, the basal ganglia control saccadic eye movements (saccades) by means of their connection to the superior colliculus (SC). The SC receives convergent inputs from cerebral cortical areas and the basal ganglia. To make a saccade to an object purposefully, appropriate signals must be selected out of the cortical inputs, in which the basal ganglia play a crucial role. This is done by the sustained inhibitory input from the substantia nigra pars reticulata (SNr) to the SC. This inhibition can be removed by another inhibition from the caudate nucleus (CD) to the SNr, which results in a disinhibition of the SC. The basal ganglia have another mechanism, involving the external segment of the globus pallidus and the subthalamic nucleus, with which the SNr-SC inhibition can further be enhanced. The sensorimotor signals carried by the basal ganglia neurons are strongly modulated depending on the behavioral context, which reflects working memory, expectation, and attention. Expectation of reward is a critical determinant in that the saccade that has been rewarded is facilitated subsequently. The interaction between cortical and dopaminergic inputs to CD neurons may underlie the behavioral adaptation toward purposeful saccades.

scholarly journals Dissociable roles of central striatum and anterior lateral motor area in initiating and sustaining naturalistic behavior

2020 ◽  
Author(s):  
Victoria L. Corbit ◽  
Sean C. Piantadosi ◽  
Jesse Wood ◽  
Grace Liu ◽  
Clare J.Y. Choi ◽  
...  
Keyword(s):  
Motor Behavior ◽  
Motor Area ◽  
Grooming Behavior ◽  
Calcium Activity ◽  
Behavioral Selection ◽  
Optogenetic Stimulation ◽  
Corticostriatal Circuits ◽  
Cortical Inputs ◽  
Stimulation Of

AbstractAlthough much is known about how corticostriatal circuits mediate behavioral selection, most previous work has been conducted in highly trained animals engaged in instrumental tasks. Understanding how corticostriatal circuits mediate behavioral selection and initiation in a naturalistic setting is critical to understanding how the brain chooses and executes behavior in unconstrained situations. Central striatum (CS), an understudied region that lies in the middle of the motor-limbic topography, is well-poised to play an important role in these processes since its main cortical inputs (Corbit et al., 2019) have been implicated in behavioral flexibility (lateral orbitofrontal cortex (Kim and Ragozzino, 2005)) and response preparation (anterior lateral motor area, ALM) (Li et al., 2015), However, although CS activity has been associated with conditioned grooming behavior in transgenic mice (Burguiere et al., 2013), the role of CS and its cortical inputs in the selection of spontaneous behaviors has not been explored. We therefore studied the role of CS corticostriatal circuits in behavioral selection in an open field context.Surprisingly, using fiber photometry in this unconstrained environment, we found that population calcium activity in CS was specifically increased at onset of grooming, and not at onset of other spontaneous behaviors such as rearing or locomotion. Supporting a potential selective role for CS in the initiation of grooming, bilateral optogenetic stimulation of CS evoked immediate onset grooming-related movements. However, these movements resembled subcomponents of grooming behavior and not full-fledged grooming bouts, suggesting that additional input(s) are required to appropriately sequence and sustain this complex motor behavior once initiated. Consistent with this idea, optogenetic stimulation of CS inputs from ALM generated sustained grooming responses that evolved on a time-course paralleling CS activation monitored using single-cell calcium imaging. Furthermore, fiber photometry in ALM demonstrated a gradual ramp in calcium activity that peaked at time of grooming termination, supporting a potential role for ALM in encoding length of this spontaneous sequenced behavior. Finally, dual color dual region fiber photometry indicated that CS activation precedes ALM during naturalistic grooming sequences. Taken together, these data support a novel model in which CS activity is sufficient to initiate grooming behavior, but ALM activity is necessary to sustain and encode the length of grooming bouts. Thus, the use of an unconstrained behavioral paradigm has allowed us to uncover surprising roles for CS and ALM in the initiation and maintenance of spontaneous sequenced behaviors.

Individual Measures of Time Perception Predict Performance in a Timed Reaching Task

2017 ◽  
Vol 61 (1) ◽  
pp. 1380-1384
Author(s):  
Elliot Nauert ◽  
Douglas J. Gillan
Keyword(s):  
Time Perception ◽  
Movement Planning ◽  
Movement Speed ◽  
Spatial Accuracy ◽  
Reaching Task ◽  
Time Sensitivity ◽  
Movement Strategies ◽  
Speed Accuracy ◽  
Accuracy Tradeoff

In temporally-constrained reaching tasks, participants make rapid movements to a target while making their movements last a designated length of time. It has been well-established that effective target width, a measure of spatial accuracy, increases linearly with movement speed. This study sought to understand how individual differences in temporal sensitivity affect this speed-accuracy tradeoff. It was found that time sensitivity did not affect spatial components of the timed reaching task, but it was related to temporal components of the task. Ideas regarding the role of time perception in movement planning as well as differences in movement strategies for short and long target intervals are discussed.

The Role of Execution Noise in Movement Variability

2004 ◽  
Vol 91 (2) ◽  
pp. 1050-1063 ◽  
Author(s):  
Robert J. van Beers ◽  
Patrick Haggard ◽  
Daniel M. Wolpert
Keyword(s):  
Movement Planning ◽  
Movement Direction ◽  
Movement Variability ◽  
Movement Execution ◽  
Reaching Task ◽  
Temporal Noise ◽  
Straight Line ◽  
Neural Processes ◽  
Planning Processes

The origin of variability in goal-directed movements is not well understood. Variability can originate from several neural processes such as target localization, movement planning, and movement execution. Here we examine variability resulting from noise in movement execution. In several experiments, subjects moved their unseen hand to visual targets, under conditions which were designed to minimize the variability expected from localization and planning processes. We tested short movements in 32 directions in a center-out reaching task. The variability in the movement endpoints and in the initial movement direction varied systematically with the movement direction, with some directions having up to twice the variability of others. In a second experiment we tested four movements in the same direction but with different extents. Here, the longer movements were systematically curved, and the endpoint ellipses were not aligned with the straight line between starting and end position, but they were roughly aligned with the last part of the trajectory. We show that the variability observed in these experiments cannot be explained by planning noise but is well explained by noise in movement execution. A combination of both signal-dependent and signal-independent noise in the amplitude of the motor commands and temporal noise in their duration can explain the observed variability. Our results suggest that, in general, execution noise accounts for at least a large proportion of movement variability.

scholarly journals Subthalamic Nucleus Neurons Differentially Encode Early and Late Aspects of Speech Production

2017 ◽  
Author(s):  
WJ Lipski ◽  
A Alhourani ◽  
T Pirnia ◽  
PW Jones ◽  
C Dastolfo-Hromack ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Firing Rate ◽  
Speech Production ◽  
Subthalamic Nucleus ◽  
Motor Behavior ◽  
Dependent Inhibition ◽  
Subthalamic Neurons ◽  
Intracranial Recording ◽  
Deep Brain Stimulation Surgery

ABSTRACTBasal ganglia-thalamocortical loops mediate all motor behavior, yet little detail is known about the role of basal ganglia nuclei in speech production. Using intracranial recording during deep brain stimulation surgery, we tested the hypothesis that the firing rate of subthalamic nucleus neurons is modulated in response to both planning and motor execution aspects of speech. Nearly half of 79 recorded units exhibited firing rate modulation, during a syllable reading task administered in 12 subjects. Trial-to-trial timing of changes in subthalamic neuronal activity, relative to cue onset versus production onset, revealed that locking to cue presentation was associated more with units that decreased firing rate, while locking to speech onset was associated more with units that increased firing rate. These uniquely acquired data indicate that subthalamic activity is dynamic during the production of speech, reflecting temporally-dependent inhibition and excitation of separate populations of subthalamic neurons.

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