scholarly journals Neural dynamics of variable grasp movement preparation in the macaque fronto-parietal network

2017 ◽  
Author(s):  
Jonathan A Michaels ◽  
Benjamin Dann ◽  
Rijk W Intveld ◽  
Hansjörg Scherberger

AbstractOur voluntary grasping actions lie on a continuum between immediate action and waiting for the right moment, depending on the context. Therefore, studying grasping requires investigating how preparation time affects this process. Two macaque monkeys (Macaca mulatta) performed a grasping task with a short instruction followed by an immediate or delayed go cue (0-1300 ms) while we recorded in parallel from neurons in the hand area (F5) of the ventral premotor cortex and the anterior intraparietal area (AIP). Initial population dynamics followed a fixed trajectory in the neural state space unique to each grip type, reflecting unavoidable preparation, then diverged depending on the delay. Although similar types of single unit responses were present in both areas, population activity in AIP stabilized within a unique memory state while F5 activity continued to evolve, tracking subjective anticipation of the go cue. Intriguingly, activity during movement initiation clustered into two trajectory clusters, corresponding to movements that were either ‘as fast as possible’ or withheld movements, demonstrating a widespread state shift in the fronto-parietal grasping network when movements must be withheld. Our results reveal how dissociation between static and dynamic components of movement preparation as well as differentiation between cortical areas is possible through population level analysis.Significance StatementMany of our movements must occur with no warning, while others we can prepare in advance. Yet, it’s unclear how planning for movements along the spectrum between these two situations differs in the brain. Two macaque monkeys made reach to grasp movements after varying amounts of preparation time while we recorded from premotor and parietal cortex. We found that the initial response to a grasp instruction was specific to the required movement, but not the preparation time, reflecting required processing. However, when more preparation time was given, neural activity achieved unique states that likely related to withholding movements and anticipation of movement, which was more prevalent in premotor cortex, suggesting differing roles of premotor and parietal cortex in grasp planning.

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Steven Jack Jerjian ◽  
Maneesh Sahani ◽  
Alexander Kraskov

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.


2019 ◽  
Author(s):  
Jerjian S.J. ◽  
Sahani M. ◽  
Kraskov A.

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.


2007 ◽  
Vol 97 (1) ◽  
pp. 348-359 ◽  
Author(s):  
Mark M. Churchland ◽  
Krishna V. Shenoy

We tested the hypothesis that delay-period activity in premotor cortex is essential to movement preparation. During a delayed-reach task, we used subthreshold intracortical microstimulation to disrupt putative “preparatory” activity. Microstimulation led to a highly specific increase in reach reaction time. Effects were largest when activity was disrupted around the time of the go cue. Earlier disruptions, which presumably allowed movement preparation time to recover, had only a weak impact. Furthermore, saccadic reaction time showed little or no increase. Finally, microstimulation of nearby primary motor cortex, even when slightly suprathreshold, had little effect on reach reaction time. These findings provide the first evidence, of a causal and temporally specific nature, that activity in premotor cortex is fundamental to movement preparation. Furthermore, although reaction times were increased, the movements themselves were essentially unperturbed. This supports the suggestion that movement preparation is an active and actively monitored process and that movement can be delayed until inaccuracies are repaired. These results are readily interpreted in the context of the recently developed optimal-subspace hypothesis.


Author(s):  
Katrin Sutter ◽  
Leonie Oostwoud Wijdenes ◽  
Robert J. van Beers ◽  
W. Pieter Medendorp

Faster movements are typically more variable - a speed-accuracy tradeoff known as Fitts' law. Are movements that are initiated faster also more variable? Neurophysiological work has associated larger neural variability during motor preparation with longer reaction time (RT) and larger movement variability, implying that movement variability decreases with increasing RT. Here, we recorded over 30000 reaching movements in eleven human participants who moved to visually-cued targets. Half of the visual cues was accompanied by a beep to evoke a wide RT range in each participant. Results show that initial reach variability decreases with increasing RT, for voluntarily produced RTs up to ~300 ms, while other kinematic aspects and endpoint accuracy remained unaffected. We conclude that movement preparation time determines initial movement variability. We suggest that the chosen movement preparation time reflects a trade-off between movement initiation and precision.


2019 ◽  
Author(s):  
Guanghao Sun ◽  
Shaomin Zhang ◽  
Ruixue Wang ◽  
Yaoyao Hao ◽  
Weidong Chen ◽  
...  

AbstractReaching to grasp movement is thought to rely upon two independent brain pathways. The dorsomedial one is involved in reaching while the dorsolateral one is dealing with grasping. However, some recent evidences suggested that the dorsomedial pathway might participate in grasp movement. Therefore, it is important to investigate whether PMd is involved in grasp planning, and if participating, what kind of role PMd played in grasp planning. In this study, two macaques monkeys were trained to grasp same object by instructing or freely choosing one of two grips, power grip or hook grip. A 96-channel microelectrode array was implanted to collect the population activity of PMd in each subject. Both single unit activity and population activity were analyzed. We found that nearly 21.0% and 26.8% units in PMd of two monkeys displayed grip selectivity during gesture planning in both instructing or freely choosing conditions. These units exhibit selectivity for different gestures when facing the identical visual stimuli (freely choosing condition). At the same time, similar activity patterns are displayed for the same gesture when faced with different selection strategies (freely choosing condition vs. instructing condition). These results show that some neurons of PMd are mainly involved in the hand shape preparation and have no obvious relationship with external visual stimuli and selection strategies.


2009 ◽  
Vol 20 (6) ◽  
pp. 1323-1331 ◽  
Author(s):  
G. Liuzzi ◽  
V. Horniss ◽  
J. Hoppe ◽  
K. Heise ◽  
M. Zimerman ◽  
...  

2006 ◽  
Vol 95 (2) ◽  
pp. 922-931 ◽  
Author(s):  
David E. Vaillancourt ◽  
Mary A. Mayka ◽  
Daniel M. Corcos

The cerebellum, parietal cortex, and premotor cortex are integral to visuomotor processing. The parameters of visual information that modulate their role in visuomotor control are less clear. From motor psychophysics, the relation between the frequency of visual feedback and force variability has been identified as nonlinear. Thus we hypothesized that visual feedback frequency will differentially modulate the neural activation in the cerebellum, parietal cortex, and premotor cortex related to visuomotor processing. We used functional magnetic resonance imaging at 3 Tesla to examine visually guided grip force control under frequent and infrequent visual feedback conditions. Control conditions with intermittent visual feedback alone and a control force condition without visual feedback were examined. As expected, force variability was reduced in the frequent compared with the infrequent condition. Three novel findings were identified. First, infrequent (0.4 Hz) visual feedback did not result in visuomotor activation in lateral cerebellum (lobule VI/Crus I), whereas frequent (25 Hz) intermittent visual feedback did. This is in contrast to the anterior intermediate cerebellum (lobule V/VI), which was consistently active across all force conditions compared with rest. Second, confirming previous observations, the parietal and premotor cortices were active during grip force with frequent visual feedback. The novel finding was that the parietal and premotor cortex were also active during grip force with infrequent visual feedback. Third, right inferior parietal lobule, dorsal premotor cortex, and ventral premotor cortex had greater activation in the frequent compared with the infrequent grip force condition. These findings demonstrate that the frequency of visual information reduces motor error and differentially modulates the neural activation related to visuomotor processing in the cerebellum, parietal cortex, and premotor cortex.


2017 ◽  
Vol 117 (1) ◽  
pp. 65-78 ◽  
Author(s):  
Kévin Marche ◽  
Paul Apicella

Recent works highlight the importance of local inhibitory interneurons in regulating the function of the striatum. In particular, fast-spiking interneurons (FSIs), which likely correspond to a subgroup of GABAergic interneurons, have been involved in the control of movement by exerting strong inhibition on striatal output pathways. However, little is known about the exact contribution of these presumed interneurons in movement preparation, initiation, and execution. We recorded the activity of FSIs in the striatum of monkeys as they performed reaching movements to a visual target under two task conditions: one in which the movement target was presented at unsignaled left or right locations, and another in which advance information about target location was available, thus allowing monkeys to react faster. Modulations of FSI activity around the initiation of movement (53% of 55 neurons) consisted mostly of increases reaching maximal firing immediately before or, less frequently, after movement onset. Another subset of FSIs showed decreases in activity during movement execution. Rarely did movement-related changes in FSI firing depend on response direction and movement speed. Modulations of FSI activity occurring relatively early in relation to movement initiation were more influenced by the preparation for movement, compared with those occurring later. Conversely, FSI activity remained unaffected, as monkeys were preparing a movement toward a specific location and instead moved to the opposite direction when the trigger occurred. These results provide evidence that changes in activity of presumed GABAergic interneurons of the primate striatum could make distinct contributions to processes involved in movement generation. NEW & NOTEWORTHY We explored the functional contributions of striatal fast-spiking interneurons (FSIs), presumed GABAergic interneurons, to distinct steps of movement generation in monkeys performing a reaching task. The activity of individual FSIs was modulated before and during the movement, consisting mostly of increased in firing rates. Changes in activity also occurred during movement preparation. We interpret this variety of modulation types at different moments of task performance as reflecting differential FSI control over distinct phases of movement.


2014 ◽  
Vol 111 (12) ◽  
pp. 2560-2569 ◽  
Author(s):  
Pranav Parikh ◽  
Marco Davare ◽  
Patrick McGurrin ◽  
Marco Santello

Control of digit forces for grasping relies on sensorimotor memory gained from prior experience with the same or similar objects and on online sensory feedback. However, little is known about neural mechanisms underlying digit force planning. We addressed this question by quantifying the temporal evolution of corticospinal excitability (CSE) using single-pulse transcranial magnetic stimulation (TMS) during two reach-to-grasp tasks. These tasks differed in terms of the magnitude of force exerted on the same points on the object to isolate digit force planning from reach and grasp planning. We also addressed the role of intracortical circuitry within primary motor cortex (M1) by quantifying the balance between short intracortical inhibition and facilitation using paired-pulse TMS on the same tasks. Eighteen right-handed subjects were visually cued to plan digit placement at predetermined locations on the object and subsequently to exert either negligible force (“low-force” task, LF) or 10% of their maximum pinch force (“high-force” task, HF) on the object. We found that the HF task elicited significantly smaller CSE than the LF task, but only when the TMS pulse coincided with the signal to initiate the reach. This force planning-related CSE modulation was specific to the muscles involved in the performance of both tasks. Interestingly, digit force planning did not result in modulation of M1 intracortical inhibitory and facilitatory circuitry. Our findings suggest that planning of digit forces reflected by CSE modulation starts well before object contact and appears to be driven by inputs from frontoparietal areas other than M1.


2022 ◽  
Author(s):  
Kaushik J Lakshminarasimhan ◽  
Eric Avila ◽  
Xaq Pitkow ◽  
Dora E Angelaki

Success in many real-world tasks depends on our ability to dynamically track hidden states of the world. To understand the underlying neural computations, we recorded brain activity in posterior parietal cortex (PPC) of monkeys navigating by optic flow to a hidden target location within a virtual environment, without explicit position cues. In addition to sequential neural dynamics and strong interneuronal interactions, we found that the hidden state -- monkey's displacement from the goal -- was encoded in single neurons, and could be dynamically decoded from population activity. The decoded estimates predicted navigation performance on individual trials. Task manipulations that perturbed the world model induced substantial changes in neural interactions, and modified the neural representation of the hidden state, while representations of sensory and motor variables remained stable. The findings were recapitulated by a task-optimized recurrent neural network model, suggesting that neural interactions in PPC embody the world model to consolidate information and track task-relevant hidden states.


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