Differences in spectral profiles between rostral and caudal premotor cortex when hand-eye actions are decoupled

2013 ◽  
Vol 110 (4) ◽  
pp. 952-963 ◽  
Author(s):  
Patricia F. Sayegh ◽  
Kara M. Hawkins ◽  
Kari L. Hoffman ◽  
Lauren E. Sergio

The aim of this research was to understand how the brain controls voluntary movement when not directly interacting with the object of interest. In the present study, we examined the role of premotor cortex in this behavior. The goal of this study was to characterize the oscillatory activity within the caudal and rostral subdivisions of dorsal premotor cortex (PMdc and PMdr) with a change from the most basic reaching movement to one that involves a simple dissociation between the actions of the eyes and hand. We were specifically interested in how PMdr and PMdc respond when the eyes and hand are decoupled by moving along different spatial planes. We recorded single-unit activity and local field potentials within PMdr and PMdc from two rhesus macaques during performance of two types of visually guided reaches. During the standard condition, a visually guided reach was performed whereby the visual stimulus guiding the movement was the target of the reach itself. During the nonstandard condition, the visual stimulus provided information about the direction of the required movement but was not the target of the motor output. We observed distinct task-related and topographical differences between PMdr and PMdc. Our results support functional differences between PMdr and PMdc during visually guided reaching. PMdr activity appears more involved in integrating the rule-based aspects of a visually guided reach, whereas PMdc is more involved in the online updating of the decoupled reach. More broadly, our results highlight the necessity of accounting for the nonstandard nature of a motor task when interpreting movement control research data.

2014 ◽  
Vol 111 (11) ◽  
pp. 2210-2221 ◽  
Author(s):  
Patricia F. Sayegh ◽  
Kara M. Hawkins ◽  
Bogdan Neagu ◽  
J. Douglas Crawford ◽  
Kari L. Hoffman ◽  
...  

Eye-hand coordination is crucial for our ability to interact with the world around us. However, much of the visually guided reaches that we perform require a spatial decoupling between gaze direction and hand orientation. These complex decoupled reaching movements are in contrast to more standard eye and hand reaching movements in which the eyes and the hand are coupled. The superior parietal lobule (SPL) receives converging eye and hand signals; however, what is yet to be understood is how the activity within this region is modulated during decoupled eye and hand reaches. To address this, we recorded local field potentials within SPL from two rhesus macaques during coupled vs. decoupled eye and hand movements. Overall we observed a distinct separation in synchrony within the lower 10- to 20-Hz beta range from that in the higher 30- to 40-Hz gamma range. Specifically, within the early planning phase, beta synchrony dominated; however, the onset of this sustained beta oscillation occurred later during eye-hand decoupled vs. coupled reaches. As the task progressed, there was a switch to low-frequency and gamma-dominated responses, specifically for decoupled reaches. More importantly, we observed local field potential activity to be a stronger task (coupled vs. decoupled) and state (planning vs. execution) predictor than that of single units alone. Our results provide further insight into the computations of SPL for visuomotor transformations and highlight the necessity of accounting for the decoupled eye-hand nature of a motor task when interpreting movement control research data.


2021 ◽  
Vol 118 (37) ◽  
pp. e2100652118
Author(s):  
Alejandra Sel ◽  
Lennart Verhagen ◽  
Katharina Angerer ◽  
Raluca David ◽  
Miriam C. Klein-Flügge ◽  
...  

The origins of oscillatory activity in the brain are currently debated, but common to many hypotheses is the notion that they reflect interactions between brain areas. Here, we examine this possibility by manipulating the strength of coupling between two human brain regions, ventral premotor cortex (PMv) and primary motor cortex (M1), and examine the impact on oscillatory activity in the motor system measurable in the electroencephalogram. We either increased or decreased the strength of coupling while holding the impact on each component area in the pathway constant. This was achieved by stimulating PMv and M1 with paired pulses of transcranial magnetic stimulation using two different patterns, only one of which increases the influence exerted by PMv over M1. While the stimulation protocols differed in their temporal patterning, they were comprised of identical numbers of pulses to M1 and PMv. We measured the impact on activity in alpha, beta, and theta bands during a motor task in which participants either made a preprepared action (Go) or withheld it (No-Go). Augmenting cortical connectivity between PMv and M1, by evoking synchronous pre- and postsynaptic activity in the PMv–M1 pathway, enhanced oscillatory beta and theta rhythms in Go and No-Go trials, respectively. Little change was observed in the alpha rhythm. By contrast, diminishing the influence of PMv over M1 decreased oscillatory beta and theta rhythms in Go and No-Go trials, respectively. This suggests that corticocortical communication frequencies in the PMv–M1 pathway can be manipulated following Hebbian spike-timing–dependent plasticity.


1982 ◽  
Vol 55 (3) ◽  
pp. 1003-1016 ◽  
Author(s):  
B. L. Day ◽  
C. D. Marsden

The principal question asked is whether in a visually-guided motor task, a subject tracking a known target employs a different strategy of movement to that used when tracking an unknown target. 22 subjects performed a series of 150 visual tracking tasks each 5 sec. long. The target-move-ment patterns used for the first 50 trials were all different, but for the remaining 100 trials they were identical. Subjects, however, were not informed of the repetition until the final 50 trials. When the task was made repetitive, even though the subjects were unaware of the repetition, learning occurred as evidenced by a progressive reduction in tracking error, although tracking lag remained above the mean reaction-time. Once subjects were aware of the repetition, tracking lags often reached zero or even negative values and tracking error dropped even further. It is argued that the former learning is confined to subconscious improvement in the intermittent response to visual inspection of tracking error, whereas the latter is achieved by adopting a truly predictive mode of tracking. Further experiments were devised to evaluate the role of visual information in movement control when using the predictive strategy. The main finding was that even when moving predictively, visual information was used to regulate motor output, largely to modify the timing of the predictive response to synchronize with the stimulus.


1991 ◽  
Vol 66 (3) ◽  
pp. 705-718 ◽  
Author(s):  
H. Mushiake ◽  
M. Inase ◽  
J. Tanji

1. Single-cell activity was recorded from three different motor areas in the cerebral cortex: the primary motor cortex (MI), supplementary motor area (SMA), and premotor cortex (PM). 2. Three monkeys (Macaca fuscata) were trained to perform a sequential motor task in two different conditions. In one condition (visually triggered task, VT), they reached to and touched three pads placed in a front panel by following lights illuminated individually from behind the pads. In the other condition (internally guided task, IT), they had to remember a predetermined sequence and press the three pads without visual guidance. In a transitional phase between the two conditions, the animals learned to memorize the correct sequence. Auditory instruction signals (tones of different frequencies) told the animal which mode it was in. After the instruction signals, the animals waited for a visual signal that triggered the first movement. 3. Neuronal activity was analyzed during three defined periods: delay period, premovement period, and movement period. Statistical comparisons were made to detect differences between the two behavioral modes with respect to the activity in each period. 4. Most, if not all, of MI neurons exhibited similar activity during the delay, premovement, and movement periods, regardless of whether the sequential motor task was visually guided or internally determined. 5. More than one-half of the SMA neurons were preferentially or exclusively active in relation to IT during both the premovement (55%) and movement (65%) periods. In contrast, PM neurons were more active (55% and 64% during the premovement and movement periods) in VT. 6. During the instructed-delay period, a majority of SMA neurons exhibited preferential or exclusive relation to IT whereas the activity in PM neurons was observed equally in different modes. 7. Two types of neurons exhibiting properties of special interest were observed. Sequence-specific neurons (active in a particular sequence only) were more common in SMA, whereas transition-specific neurons (active only at the transitional phase) were more common in PM. 8. Although a strict functional dichotomy is not acceptable, these observations support a hypothesis that the SMA is more related to IT, whereas PM is more involved in VT. 9. Some indications pointing to a functional subdivision of PM are obtained.


1994 ◽  
Vol 71 (3) ◽  
pp. 1151-1164 ◽  
Author(s):  
K. Kurata ◽  
D. S. Hoffman

1. A gamma aminobutyric acid (GABAA) receptor agonist, muscimol (Sigma, 5 micrograms/microliters solution), and a GABAB receptor agonist and antagonist, baclofen and phaclofen, respectively, were injected (1.0 microliter) into the dorsal and ventral aspects of the premotor cortex (PM) of two Japanese monkeys (Macaca fuscata), while they were performing a motor task that required wrist flexion or extension to a target. The correct movement was instructed by either 1) a conditional color cue [green or red light emitting diodes (LED)] equidistant from the targets or 2) a directional cue toward extension or flexion (right or left LED). When the green or right LED was illuminated, extension was to be performed. When the red or left LED was illuminated, flexion was required. The movement was triggered by a visual stimulus either simultaneously with the instruction stimulus or after a variable delay. 2. Before drug injection, single-unit recordings were made to select injection sites 1) in the dorsal aspect of the PM (PMd) around the superior precentral sulcus where typical set-related activity was frequently recorded and 2) in the ventral aspect of the PM (PMv) immediately caudal to the genu of the arcuate sulcus where movement-related neurons were densely located. 3. Behavioral deficits were observed primarily at the time muscimol, but not baclofen or phaclofen, was injected. Furthermore, muscimol effects were short-lasting: deficits were most frequently observed during the 10-min injection period but seldom after completion of injection. 4. When muscimol was injected into the PMd, there was an increase in the number of direction errors primarily when the conditional cues were presented. The initiated movements were similar in amplitude and velocity to the preinjection behavior. In contrast, when muscimol was injected into the PMv, many of the initiated movements showed smaller amplitudes and slower velocities, but few direction errors were made. 5. These results suggest that the PMd and PMv play differential roles in motor control: the PMd is more important than PMv in conditional motor behavior and plays a role in the preparation for forthcoming movements. In contrast, the PMv is more specialized for a role in the execution of visually guided movements.


2017 ◽  
Vol 29 (7) ◽  
pp. 1194-1211 ◽  
Author(s):  
Patricia F. Sayegh ◽  
Diana J. Gorbet ◽  
Kara M. Hawkins ◽  
Kari L. Hoffman ◽  
Lauren E. Sergio

Our brain's ability to flexibly control the communication between the eyes and the hand allows for our successful interaction with the objects located within our environment. This flexibility has been observed in the pattern of neural responses within key regions of the frontoparietal reach network. More specifically, our group has shown how single-unit and oscillatory activity within the dorsal premotor cortex (PMd) and the superior parietal lobule (SPL) change contingent on the level of visuomotor compatibility between the eyes and hand. Reaches that involve a coupling between the eyes and hand toward a common spatial target display a pattern of neural responses that differ from reaches that require eye–hand decoupling. Although previous work examined the altered spiking and oscillatory activity that occurs during different types of eye–hand compatibilities, they did not address how each of these measures of neurological activity interacts with one another. Thus, in an effort to fully characterize the relationship between oscillatory and single-unit activity during different types of eye–hand coordination, we measured the spike–field coherence (SFC) within regions of macaque SPL and PMd. We observed stronger SFC within PMdr and superficial regions of SPL (areas 5/PEc) during decoupled reaches, whereas PMdc and regions within SPL surrounding medial intrapareital sulcus had stronger SFC during coupled reaches. These results were supported by meta-analysis on human fMRI data. Our results support the proposal of altered cortical control during complex eye–hand coordination and highlight the necessity to account for the different eye–hand compatibilities in motor control research.


2018 ◽  
Vol 120 (1) ◽  
pp. 239-249 ◽  
Author(s):  
James E. Gehringer ◽  
David J. Arpin ◽  
Elizabeth Heinrichs-Graham ◽  
Tony W. Wilson ◽  
Max J. Kurz

Although it is well appreciated that practicing a motor task updates the associated internal model, it is still unknown how the cortical oscillations linked with the motor action change with practice. The present study investigates the short-term changes (e.g., fast motor learning) in the α- and β-event-related desynchronizations (ERD) associated with the production of a motor action. To this end, we used magnetoencephalography to identify changes in the α- and β-ERD in healthy adults after participants practiced a novel isometric ankle plantarflexion target-matching task. After practicing, the participants matched the targets faster and had improved accuracy, faster force production, and a reduced amount of variability in the force output when trying to match the target. Parallel with the behavioral results, the strength of the β-ERD across the motor-planning and execution stages was reduced after practice in the sensorimotor and occipital cortexes. No pre/postpractice changes were found in the α-ERD during motor planning or execution. Together, these outcomes suggest that fast motor learning is associated with a decrease in β-ERD power. The decreased strength likely reflects a more refined motor plan, a reduction in neural resources needed to perform the task, and/or an enhancement of the processes that are involved in the visuomotor transformations that occur before the onset of the motor action. These results may augment the development of neurologically based practice strategies and/or lead to new practice strategies that increase motor learning. NEW & NOTEWORTHY We aimed to determine the effects of practice on the movement-related cortical oscillatory activity. Following practice, we found that the performance of the ankle plantarflexion target-matching task improved and the power of the β-oscillations decreased in the sensorimotor and occipital cortexes. These novel findings capture the β-oscillatory activity changes in the sensorimotor and occipital cortexes that are coupled with behavioral changes to demonstrate the effects of motor learning.


Stroke ◽  
2021 ◽  
Author(s):  
Robert Schulz ◽  
Marlene Bönstrup ◽  
Stephanie Guder ◽  
Jingchun Liu ◽  
Benedikt Frey ◽  
...  

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.


1996 ◽  
Vol 75 (5) ◽  
pp. 2187-2191 ◽  
Author(s):  
H. Mushiake ◽  
N. Fujii ◽  
J. Tanji

1. We studied neuronal activity in the supplementary eye field (SEF) and frontal eye field (FEF) of a monkey during performance of a conditional motor task that required capturing of a target either with a saccadic eye movement (the saccade-only condition) or with an eye-hand reach (the saccade-and-reach condition), according to visual instructions. 2. Among 106 SEF neurons that showed presaccadic activity, more than one-half of them (54%) were active preferentially under the saccade-only condition (n = 12) or under the saccade-and-reach condition (n = 45), while the remaining 49 neurons were equally active in both conditions. 3. By contrast, most (97%) of the 109 neurons in the FEF exhibited approximately equal activity in relation to saccades under the two conditions. 4. The present results suggest the possibility that SEF neurons, at least in part, are involved in signaling whether the motor task is oculomotor or combined eye-arm movements, whereas FEF neurons are mostly related to oculomotor control.


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