scholarly journals Motor planning brings human primary somatosensory cortex into action-specific preparatory states

eLife ◽  
2022 ◽  
Vol 11 ◽  
Author(s):  
Giacomo Ariani ◽  
J Andrew Pruszynski ◽  
Jörn Diedrichsen

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here we used 7T functional magnetic resonance imaging (fMRI) and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger action. Surprisingly, these activity patterns were as informative as those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger press, while activity in both regions is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons.

2020 ◽  
Author(s):  
Giacomo Ariani ◽  
J. Andrew Pruszynski ◽  
Jörn Diedrichsen

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here we used 7T functional magnetic resonance imaging (fMRI) and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger movements. Surprisingly, these activity patterns were similarly strong to those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during movement execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger movement, while activity in S1 and M1 is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons.


1993 ◽  
Vol 70 (3) ◽  
pp. 985-996 ◽  
Author(s):  
L. D. Lin ◽  
G. M. Murray ◽  
B. J. Sessle

1. Studies using ablation, intracortical microstimulation (ICMS) and surface stimulation, and single-neuron recordings have suggested that the primate primary somatosensory cortex (SI) may play an important role in movement control. Our aim was to determine whether bilateral inactivation of face SI would indeed interfere with the control of tongue or jaw-closing movements. 2. Effects of reversible inactivation by cooling of face SI was investigated in two monkeys trained to perform both a tongue-protrusion task and a biting task. The cooling experiments were carried out after the orofacial representation within SI was identified by systematically defining the mechanoreceptive field of single neurons recorded in face SI. The deficits in the tongue or jaw-closing movement were evaluated by the success rates for the monkeys' performance of both tasks and by the force and electromyographic (EMG) activity recorded from the masseter, genioglossus, and digastric muscles associated with the tasks. 3. During bilateral cooling of face SI, there was a statistically significant reduction in the success rates for the performance of the tongue-protrusion task in comparison with control series of trials while the thermodes used to cool face SI were kept at 37 degrees C. Detailed analyses of force and EMG activity showed that the principal deficit was the inability of the monkeys to maintain a steady tongue-protrusive force in the force holding period during each trial and to exert a consistent tongue-protrusion force between different trials. The task performance returned to control protocol levels at 4 min after commencement of rewarming. 4. Identical cooling conditions did not significantly affect the success rates for the performance of the biting task. Although the extent of the deficit was not severe enough to cause a significant reduction in successful rates for the biting task, cooling did significantly affect the ability of the monkeys to maintain a steady force in the holding period during each trial and to exert a consistent force between different trials. In one monkey the success rate of the biting task was also not affected by bilaterally cooling of face SI with a pair of larger thermodes placed on the dura over most of the face SI, face primary motor cortex (face MI), and adjacent cortical regions.(ABSTRACT TRUNCATED AT 400 WORDS)


2019 ◽  
Vol 121 (1) ◽  
pp. 152-162 ◽  
Author(s):  
Nicholas Paul Holmes ◽  
Luigi Tamè

Transcranial magnetic stimulation (TMS) over human primary somatosensory cortex (S1), unlike over primary motor cortex (M1), does not produce an immediate, objective output. Researchers must therefore rely on one or more indirect methods to position the TMS coil over S1. The “gold standard” method of TMS coil positioning is to use individual functional and structural magnetic resonance imaging (f/sMRI) alongside a stereotactic navigation system. In the absence of these facilities, however, one common method used to locate S1 is to find the scalp location that produces twitches in a hand muscle (e.g., the first dorsal interosseus, M1-FDI) and then move the coil posteriorly to target S1. There has been no systematic assessment of whether this commonly reported method of finding the hand area of S1 is optimal. To do this, we systematically reviewed 124 TMS studies targeting the S1 hand area and 95 fMRI studies involving passive finger and hand stimulation. Ninety-six TMS studies reported the scalp location assumed to correspond to S1-hand, which was on average 1.5–2 cm posterior to the functionally defined M1-hand area. Using our own scalp measurements combined with similar data from MRI and TMS studies of M1-hand, we provide the estimated scalp locations targeted in these TMS studies of the S1-hand. We also provide a summary of reported S1 coordinates for passive finger and hand stimulation in fMRI studies. We conclude that S1-hand is more lateral to M1-hand than assumed by the majority of TMS studies.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Wanying Zhang ◽  
Randy M Bruno

Layer (L) 2/3 pyramidal neurons in the primary somatosensory cortex (S1) are sparsely active, spontaneously and during sensory stimulation. Long-range inputs from higher areas may gate L2/3 activity. We investigated their in vivo impact by expressing channelrhodopsin in three main sources of feedback to rat S1: primary motor cortex, secondary somatosensory cortex, and secondary somatosensory thalamic nucleus (the posterior medial nucleus, POm). Inputs from cortical areas were relatively weak. POm, however, more robustly depolarized L2/3 cells and, when paired with peripheral stimulation, evoked action potentials. POm triggered not only a stronger fast-onset depolarization but also a delayed all-or-none persistent depolarization, lasting up to 1 s and exhibiting alpha/beta-range oscillations. Inactivating POm somata abolished persistent but not initial depolarization, indicating a recurrent circuit mechanism. We conclude that secondary thalamus can enhance L2/3 responsiveness over long periods. Such timescales could provide a potential modality-specific substrate for attention, working memory, and plasticity.


2021 ◽  
Vol 13 ◽  
Author(s):  
Elana R. Goldenkoff ◽  
Rachel N. Logue ◽  
Susan H. Brown ◽  
Michael Vesia

Age-related changes in cortico-cortical connectivity in the human motor network in older adults are associated with declines in hand dexterity. Posterior parietal cortex (PPC) is strongly interconnected with motor areas and plays a critical role in many aspects of motor planning. Functional connectivity measures derived from dual-site transcranial magnetic stimulation (dsTMS) studies have found facilitatory inputs from PPC to ipsilateral primary motor cortex (M1) in younger adults. In this study, we investigated whether facilitatory inputs from PPC to M1 are altered by age. We used dsTMS in a conditioning-test paradigm to characterize patterns of functional connectivity between the left PPC and ipsilateral M1 and a standard pegboard test to assess skilled hand motor function in 13 young and 13 older adults. We found a PPC-M1 facilitation in young adults but not older adults. Older adults also showed a decline in motor performance compared to young adults. We conclude that the reduced PPC-M1 facilitation in older adults may be an early marker of age-related decline in the neural control of movement.


2016 ◽  
Vol 115 (5) ◽  
pp. 2681-2691 ◽  
Author(s):  
Christina B. Jones ◽  
Tea Lulic ◽  
Aaron Z. Bailey ◽  
Tanner N. Mackenzie ◽  
Yi Qun Mi ◽  
...  

Theta-burst stimulation (TBS) over human primary motor cortex evokes plasticity and metaplasticity, the latter contributing to the homeostatic balance of excitation and inhibition. Our knowledge of TBS-induced effects on primary somatosensory cortex (SI) is limited, and it is unknown whether TBS induces metaplasticity within human SI. Sixteen right-handed participants (6 females, mean age 23 yr) received two TBS protocols [continuous TBS (cTBS) and intermittent TBS (iTBS)] delivered in six different combinations over SI in separate sessions. TBS protocols were delivered at 30 Hz and were as follows: a single cTBS protocol, a single iTBS protocol, cTBS followed by cTBS, iTBS followed by iTBS, cTBS followed by iTBS, and iTBS followed by cTBS. Measures included the amplitudes of the first and second somatosensory evoked potentials (SEPs) via median nerve stimulation, their paired-pulse ratio (PPR), and temporal order judgment (TOJ). Dependent measures were obtained before TBS and at 5, 25, 50, and 90 min following stimulation. Results indicate similar effects following cTBS and iTBS; increased amplitudes of the second SEP and PPR without amplitude changes to SEP 1, and impairments in TOJ. Metaplasticity was observed such that TOJ impairments following a single cTBS protocol were abolished following consecutive cTBS protocols. Additionally, consecutive iTBS protocols altered the time course of effects when compared with a single iTBS protocol. In conclusion, 30-Hz cTBS and iTBS protocols delivered in isolation induce effects consistent with a TBS-induced reduction in intracortical inhibition within SI. Furthermore, cTBS- and iTBS-induced metaplasticity appear to follow homeostatic and nonhomeostatic rules, respectively.


2007 ◽  
Vol 97 (1) ◽  
pp. 70-82 ◽  
Author(s):  
Marc H. Schieber ◽  
Gil Rivlis

Primary motor cortex (M1) neurons traditionally have been viewed as “upper motor neurons” that directly drive spinal motoneuron pools, particularly during finger movements. We used spike-triggered averages (SpikeTAs) of electromyographic (EMG) activity to select M1 neurons whose spikes signaled the arrival of input in motoneuron pools, and examined the degree of similarity between the activity patterns of these M1 neurons and their target muscles during 12 individuated finger and wrist movements. Neuron–EMG similarity generally was low. Similarity was unrelated to the strength of the SpikeTA effect, to whether the effect was pure versus synchrony, or to the number of muscles influenced by the neuron. Nevertheless, the sum of M1 neuron activity patterns, each weighted by the sign and strength of its SpikeTA effect, could be more similar to the EMG than the average similarity of individual neurons. Significant correlations between the weighted sum of M1 neuron activity patterns and EMG were obtained in six of 17 muscles, but showed R2 values ranging from only 0.26 to 0.42. These observations suggest that additional factors—including inputs from sources other than M1 and nonlinear summation of inputs to motoneuron pools—also contributed substantially to EMG activity patterns. Furthermore, although each of these M1 neurons produced SpikeTA effects with a significant peak or trough 6–16 ms after the triggering spike, shifting the weighted sum of neuron activity to lead the EMG by 40–60 ms increased their similarity, suggesting that the influence of M1 neurons that produce SpikeTA effects includes substantial synaptic integration that in part may reach the motoneuron pools over less-direct pathways.


2011 ◽  
Vol 21 (9) ◽  
pp. 2113-2121 ◽  
Author(s):  
Kaspar Meyer ◽  
Jonas T. Kaplan ◽  
Ryan Essex ◽  
Hanna Damasio ◽  
Antonio Damasio

2021 ◽  
Author(s):  
Najet Serradj ◽  
Francesca Marino ◽  
Yunuen Moreno-López ◽  
Sydney Agger ◽  
Andrew Sloan ◽  
...  

AbstractThe learning of motor skills relies on plasticity of the primary motor cortex as task acquisition drives the remodeling of cortical motor networks1,2. Large scale cortical remodeling of evoked motor outputs occurs in response to the learning of skilled, corticospinal-dependent behavior, but not simple, unskilled tasks1. Here we determine the response of corticospinal neurons to both skilled and unskilled motor training and assess the role of corticospinal neuron activity in the execution of the trained behaviors. Using in vivo calcium imaging, we found that refinement of corticospinal activity correlated with the development of skilled, but not unskilled, motor expertise. Animals that failed to learn our skilled task exhibited a limited repertoire of dynamic movements and a corresponding absence of network modulation. Transection of the corticospinal tract and aberrant activation of corticospinal neurons show the necessity for corticospinal network activity patterns in the execution of skilled, but not unskilled, movement. We reveal a critical role for corticospinal network modulation in the learning and execution of skilled motor movements. The integrity of the corticospinal tract is essential to the recovery of voluntary movement after central nervous system injuries and these findings should help to shape translational approaches to motor recovery.


2019 ◽  
Author(s):  
Atsushi Fukui ◽  
Hironobu Osaki ◽  
Yoshifumi Ueta ◽  
Yoshihiro Muragaki ◽  
Takakazu Kawamata ◽  
...  

AbstractPrimary motor cortex (M1) infarction occasionally causes sensory impairment. Because sensory signal plays an important role in motor control, sensory impairment compromises recovery and rehabilitation from motor disability. Despite the importance of sensory-motor integration for rehabilitation after M1 infarction, the neural mechanism of the sensory impairment is poorly understood. We show that the sensory processing in the primary somatosensory cortex (S1) was impaired in the acute phase of M1 infarction and recovered in a layer-specific manner in the subacute phase. This layer dependent recovery process and the anatomical connection pattern from M1 to S1 suggested the functional connectivity from M1 to S1 plays a key role in the impairment of sensory processing in S1. The simulation study demonstrated that the loss of inhibition from M1 to S1 in the acute phase of M1 infarction could cause the sensory processing impairment in S1, and the complementation of inhibition could recover the temporal coding. Taken together, we revealed how focal stroke of M1 alters cortical network activity of sensory processing, in which inhibitory input from M1 to S1 may be involved.


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