Microstimulation of dorsal premotor and primary motor cortex delays the volitional commitment to an action choice

Humans and other animals are faced with decisions about actions on a daily basis. These typically include a period of deliberation that ends with the commitment to a choice, which then leads to the overt expression of that choice through action. Previous studies with monkeys have demonstrated that neural activity in sensorimotor areas correlates with the deliberation process and reflects the moment of commitment before movement initiation, but the causal roles of these regions are challenging to establish. Here, we tested whether dorsal premotor (PMd) and primary motor cortex (M1) are causally involved in the volitional commitment to a reaching choice. We found that brief subthreshold microstimulation in PMd or M1 delayed commitment to an action but not the initiation of the action itself. Importantly, microstimulation only had a significant effect when it was delivered close to and before commitment time. These results are consistent with the proposal that PMd and M1 participate in the commitment process, which occurs when a critical firing rate difference is reached between cells voting for the selected option and those voting for the competing one. NEW & NOTEWORTHY The neural substrates of decisions between actions are typically investigated by correlating neural activity and subjects’ decision behavior, but this does not establish causality. In a reaching decision task, we demonstrate that subthreshold microstimulation of the monkey dorsal premotor cortex or primary motor cortex delays the deliberation duration if applied shortly before choice commitment. This result suggests a causal role of the sensorimotor cortex in the determination of decisions between actions.

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Chronic Stability of Single-Channel Neurophysiological Correlates of Gross and Fine Reaching Movements in the Rat

10.1101/674101 ◽

2019 ◽

Author(s):

David T. Bundy ◽

David J Guggenmos ◽

Maxwell D Murphy ◽

Randolph J. Nudo

Keyword(s):

Motor Cortex ◽

Local Field ◽

Neural Activity ◽

Local Field Potential ◽

Primary Motor Cortex ◽

Spectral Power ◽

Premotor Cortex ◽

Field Potential ◽

Motor Recovery ◽

Reaching Movements

AbstractFollowing injury to motor cortex, reorganization occurs throughout spared brain regions and is thought to underlie motor recovery. Unfortunately, the standard neurophysiological and neuroanatomical measures of post-lesion plasticity are only indirectly related to observed changes in motor execution. While substantial task-related neural activity has been observed during motor tasks in rodent primary motor cortex and premotor cortex, the long-term stability of these responses in healthy rats is uncertain, limiting the interpretability of longitudinal changes in the specific patterns of neural activity during motor recovery following injury. This study examined the stability of task-related neural activity associated with execution of reaching movements in healthy rodents. Rats were trained to perform a novel reaching task combining a ‘gross’ lever press and a ‘fine’ pellet retrieval. In each animal, two chronic microelectrode arrays were implanted in motor cortex spanning the caudal forelimb area (rodent primary motor cortex) and the rostral forelimb area (rodent premotor cortex). We recorded multiunit spiking and local field potential activity from 10 days to 7-10 weeks post-implantation to characterize the patterns of neural activity observed during each task component and analyzed the consistency of channel-specific task-related neural activity. Task-related changes in neural activity were observed on the majority of channels. While the task-related changes in multi-unit spiking and local field potential spectral power were consistent over several weeks, spectral power changes were more stable, despite the trade-off of decreased spatial and temporal resolution. These results show that rodent primary and premotor cortex are both involved in reaching movements with stable patterns of task-related activity across time, establishing the relevance of the rodent for future studies designed to examine changes in task-related neural activity during recovery from focal cortical lesions.

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Vacillation, indecision and hesitation in moment-by-moment decoding of monkey motor cortex

eLife ◽

10.7554/elife.04677 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 47

Author(s):

Matthew T Kaufman ◽

Mark M Churchland ◽

Stephen I Ryu ◽

Krishna V Shenoy

Keyword(s):

Motor Cortex ◽

Neural Activity ◽

Free Choice ◽

Primary Motor Cortex ◽

Brain State ◽

Decision Task ◽

Final Choice ◽

The Rich ◽

Individual Decisions ◽

Monkey Motor Cortex

When choosing actions, we can act decisively, vacillate, or suffer momentary indecision. Studying how individual decisions unfold requires moment-by-moment readouts of brain state. Here we provide such a view from dorsal premotor and primary motor cortex. Two monkeys performed a novel decision task while we recorded from many neurons simultaneously. We found that a decoder trained using ‘forced choices’ (one target viable) was highly reliable when applied to ‘free choices’. However, during free choices internal events formed three categories. Typically, neural activity was consistent with rapid, unwavering choices. Sometimes, though, we observed presumed ‘changes of mind’: the neural state initially reflected one choice before changing to reflect the final choice. Finally, we observed momentary ‘indecision’: delay forming any clear motor plan. Further, moments of neural indecision accompanied moments of behavioral indecision. Together, these results reveal the rich and diverse set of internal events long suspected to occur during free choice.

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Movement initiation and grasp representation in premotor and primary motor cortex mirror neurons

10.1101/2019.12.17.880237 ◽

2019 ◽

Author(s):

Jerjian S.J. ◽

Sahani M. ◽

Kraskov A.

Keyword(s):

Motor Cortex ◽

Mirror Neurons ◽

Primary Motor Cortex ◽

Action Observation ◽

Premotor Cortex ◽

Movement Control ◽

Reach To Grasp ◽

Movement Initiation ◽

Population Activity ◽

Ventral Premotor Cortex

AbstractPyramidal tract neurons (PTNs) within macaque rostral ventral premotor cortex (F5) and primary motor cortex (M1) provide direct input to spinal circuitry and are critical for skilled movement control, but surprisingly, can also be active during passive action observation. We recorded from single neurons, including identified PTNs in the hand and arm area of primary motor cortex (M1) (n=189), and in premotor area F5 (n=115) of two adult male macaques, while they executed, observed, or simply withheld (NoGo) reach-to-grasp and hold actions. We found that F5 maintains a more sustained, similar representation of grasping actions during both execution and observation. In contrast, although some M1 neurons mirrored during the grasp and hold, M1 population activity during observation contained signatures of a withholding state. This suggests that M1 and its output may dissociates signals required for the initiation of movement from those associated with the representation of grasp in order to flexibly guide behaviour.Significance StatementVentral premotor cortex (area F5) maintains a similar representation of grasping actions during both execution and observation. Primary motor cortex and its outputs dissociate between movement and non-movement states.

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Trial-to-trial adjustments of speed-accuracy trade-offs in premotor and primary motor cortex

Journal of Neurophysiology ◽

10.1152/jn.00726.2016 ◽

2017 ◽

Vol 117 (2) ◽

pp. 665-683 ◽

Cited By ~ 3

Author(s):

David Thura ◽

Guido Guberman ◽

Paul Cisek

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Premotor Cortex ◽

Decision Task ◽

Trade Off ◽

Task Support ◽

Trade Offs ◽

Sensory Evidence ◽

Speed Accuracy ◽

After Error

Recent studies have shown that activity in sensorimotor structures varies depending on the speed-accuracy trade-off (SAT) context in which a decision is made. Here we tested the hypothesis that the same areas also reflect a more local adjustment of SAT established between individual trials, based on the outcome of the previous decision. Two monkeys performed a reaching decision task in which sensory evidence continuously evolves during the time course of a trial. In two SAT contexts, we compared neural activity in trials following a correct choice vs. those following an error. In dorsal premotor cortex (PMd), we found that 23% of cells exhibited significantly weaker baseline activity after error trials, and for ∼30% of these this effect persisted into the deliberation epoch. These cells also contributed to the process of combining sensory evidence with the growing urgency to commit to a choice. We also found that the activity of 22% of PMd cells was increased after error trials. These neurons appeared to carry less information about sensory evidence and time-dependent urgency. For most of these modulated cells, the effect was independent of whether the previous error was expected or unexpected. We found similar phenomena in primary motor cortex (M1), with 25% of cells decreasing and 34% increasing activity after error trials, but unlike PMd, these neurons showed less clear differences in their response properties. These findings suggest that PMd and M1 belong to a network of brain areas involved in SAT adjustments established using the recent history of reinforcement. NEW & NOTEWORTHY Setting the speed-accuracy trade-off (SAT) is crucial for efficient decision making. Previous studies have reported that subjects adjust their SAT after individual decisions, usually choosing more conservatively after errors, but the neural correlates of this phenomenon are only partially known. Here, we show that neurons in PMd and M1 of monkeys performing a reach decision task support this mechanism by adequately modulating their firing rate as a function of the outcome of the previous decision.

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Cerebellar rTMS and PAS effectively induce cerebellar plasticity

Scientific Reports ◽

10.1038/s41598-021-82496-7 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Martje G. Pauly ◽

Annika Steinmeier ◽

Christina Bolte ◽

Feline Hamami ◽

Elinor Tzvi ◽

...

Keyword(s):

Motor Cortex ◽

Healthy Subjects ◽

Primary Motor Cortex ◽

Cortical Excitability ◽

Motor Evoked Potentials ◽

Repetitive Transcranial Magnetic Stimulation ◽

Premotor Cortex ◽

Motor Pathways ◽

Non Invasive ◽

Cerebellar Plasticity

AbstractNon-invasive brain stimulation techniques including repetitive transcranial magnetic stimulation (rTMS), continuous theta-burst stimulation (cTBS), paired associative stimulation (PAS), and transcranial direct current stimulation (tDCS) have been applied over the cerebellum to induce plasticity and gain insights into the interaction of the cerebellum with neo-cortical structures including the motor cortex. We compared the effects of 1 Hz rTMS, cTBS, PAS and tDCS given over the cerebellum on motor cortical excitability and interactions between the cerebellum and dorsal premotor cortex / primary motor cortex in two within subject designs in healthy controls. In experiment 1, rTMS, cTBS, PAS, and tDCS were applied over the cerebellum in 20 healthy subjects. In experiment 2, rTMS and PAS were compared to sham conditions in another group of 20 healthy subjects. In experiment 1, PAS reduced cortical excitability determined by motor evoked potentials (MEP) amplitudes, whereas rTMS increased motor thresholds and facilitated dorsal premotor-motor and cerebellum-motor cortex interactions. TDCS and cTBS had no significant effects. In experiment 2, MEP amplitudes increased after rTMS and motor thresholds following PAS. Analysis of all participants who received rTMS and PAS showed that MEP amplitudes were reduced after PAS and increased following rTMS. rTMS also caused facilitation of dorsal premotor-motor cortex and cerebellum-motor cortex interactions. In summary, cerebellar 1 Hz rTMS and PAS can effectively induce plasticity in cerebello-(premotor)-motor pathways provided larger samples are studied.

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Periinfarct rewiring supports recovery after primary motor cortex stroke

Journal of Cerebral Blood Flow & Metabolism ◽

10.1177/0271678x211002968 ◽

2021 ◽

pp. 0271678X2110029

Author(s):

Mitsouko van Assche ◽

Elisabeth Dirren ◽

Alexia Bourgeois ◽

Andreas Kleinschmidt ◽

Jonas Richiardi ◽

...

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Spatial Scales ◽

Premotor Cortex ◽

Core Network ◽

Small Spatial Scale ◽

The Core ◽

Hand Dexterity ◽

Motor Network ◽

Motor Improvement

After stroke restricted to the primary motor cortex (M1), it is uncertain whether network reorganization associated with recovery involves the periinfarct or more remote regions. We studied 16 patients with focal M1 stroke and hand paresis. Motor function and resting-state MRI functional connectivity (FC) were assessed at three time points: acute (<10 days), early subacute (3 weeks), and late subacute (3 months). FC correlates of recovery were investigated at three spatial scales, (i) ipsilesional non-infarcted M1, (ii) core motor network (M1, premotor cortex (PMC), supplementary motor area (SMA), and primary somatosensory cortex), and (iii) extended motor network including all regions structurally connected to the upper limb representation of M1. Hand dexterity was impaired only in the acute phase ( P = 0.036). At a small spatial scale, clinical recovery was more frequently associated with connections involving ipsilesional non-infarcted M1 (Odds Ratio = 6.29; P = 0.036). At a larger scale, recovery correlated with increased FC strength in the core network compared to the extended motor network (rho = 0.71; P = 0.006). These results suggest that FC changes associated with motor improvement involve the perilesional M1 and do not extend beyond the core motor network. Core motor regions, and more specifically ipsilesional non-infarcted M1, could hence become primary targets for restorative therapies.

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Interactions between pairs of transcranial magnetic stimuli over the human left dorsal premotor cortex differ from those seen in primary motor cortex

The Journal of Physiology ◽

10.1113/jphysiol.2006.123562 ◽

2007 ◽

Vol 578 (2) ◽

pp. 551-562 ◽

Cited By ~ 74

Author(s):

Giacomo Koch ◽

Michele Franca ◽

Hitoshi Mochizuki ◽

Barbara Marconi ◽

Carlo Caltagirone ◽

...

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Premotor Cortex ◽

Dorsal Premotor Cortex

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Corticospinal Tract Microstructure Correlates With Beta Oscillatory Activity in the Primary Motor Cortex After Stroke

Stroke ◽

10.1161/strokeaha.121.034344 ◽

2021 ◽

Author(s):

Robert Schulz ◽

Marlene Bönstrup ◽

Stephanie Guder ◽

Jingchun Liu ◽

Benedikt Frey ◽

...

Keyword(s):

Motor Cortex ◽

Fractional Anisotropy ◽

Primary Motor Cortex ◽

Supplementary Motor Area ◽

Premotor Cortex ◽

Motor Impairment ◽

Motor Area ◽

Oscillatory Activity ◽

Premotor Area ◽

Beta Power

Background and Purpose: Cortical beta oscillations are reported to serve as robust measures of the integrity of the human motor system. Their alterations after stroke, such as reduced movement-related beta desynchronization in the primary motor cortex, have been repeatedly related to the level of impairment. However, there is only little data whether such measures of brain function might directly relate to structural brain changes after stroke. Methods: This multimodal study investigated 18 well-recovered patients with stroke (mean age 65 years, 12 males) by means of task-related EEG and diffusion-weighted structural MRI 3 months after stroke. Beta power at rest and movement-related beta desynchronization was assessed in 3 key motor areas of the ipsilesional hemisphere that are the primary motor cortex (M1), the ventral premotor area and the supplementary motor area. Template trajectories of corticospinal tracts (CST) originating from M1, premotor cortex, and supplementary motor area were used to quantify the microstructural state of CST subcomponents. Linear mixed-effects analyses were used to relate tract-related mean fractional anisotropy to EEG measures. Results: In the present cohort, we detected statistically significant reductions in ipsilesional CST fractional anisotropy but no alterations in EEG measures when compared with healthy controls. However, in patients with stroke, there was a significant association between both beta power at rest ( P =0.002) and movement-related beta desynchronization ( P =0.003) in M1 and fractional anisotropy of the CST specifically originating from M1. Similar structure-function relationships were neither evident for ventral premotor area and supplementary motor area, particularly with respect to their CST subcomponents originating from premotor cortex and supplementary motor area, in patients with stroke nor in controls. Conclusions: These data suggest there might be a link connecting microstructure of the CST originating from M1 pyramidal neurons and beta oscillatory activity, measures which have already been related to motor impairment in patients with stroke by previous reports.

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Motor Cortical Activity During Drawing Movements: Population Representation During Spiral Tracing

Journal of Neurophysiology ◽

10.1152/jn.1999.82.5.2693 ◽

1999 ◽

Vol 82 (5) ◽

pp. 2693-2704 ◽

Cited By ~ 114

Author(s):

Daniel W. Moran ◽

Andrew B. Schwartz

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Prediction Interval ◽

Premotor Cortex ◽

Cortical Activity ◽

Simultaneous Action ◽

Emg Activity ◽

Radius Of Curvature ◽

Time Interval ◽

Population Vector

Monkeys traced spirals on a planar surface as unitary activity was recorded from either premotor or primary motor cortex. Using the population vector algorithm, the hand's trajectory could be accurately visualized with the cortical activity throughout the task. The time interval between this prediction and the corresponding movement varied linearly with the instantaneous radius of curvature; the prediction interval was longer when the path of the finger was more curved (smaller radius). The intervals in the premotor cortex fell into two groups, whereas those in the primary motor cortex formed a single group. This suggests that the change in prediction interval is a property of a single population in primary motor cortex, with the possibility that this outcome is due to the different properties generated by the simultaneous action of separate subpopulations in premotor cortex. Electromyographic (EMG) activity and joint kinematics were also measured in this task. These parameters varied harmonically throughout the task with many of the same characteristics as those of single cortical cells. Neither the lags between joint-angular velocities and hand velocity nor the lags between EMG and hand velocity could explain the changes in prediction interval between cortical activity and hand velocity. The simple spatial and temporal relationship between cortical activity and finger trajectory suggests that the figural aspects of this task are major components of cortical activity.

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