Biology subjects

Ariani, G.

Publications and source records attributed to Ariani, G..

7 recordsLinked to original sources

bioRxiv2023

Cortical areas for planning sequences before and during movement

Production of rapid movement sequences relies on preparation before (pre-planning) and during (online planning) movement. Here, we asked how different cortical sensorimotor areas contribute to these processes. Human participants performed three single-finger and three multi-finger sequences in a delayed movement paradigm. During preparation, 7T functional MRI revealed that primary motor (M1) and somatosensory (S1) areas showed pre-activation of the first movement, even though the overall activation level did not change from baseline. During production, the activity in M1 and S1 could be explained by temporal summation of activity patterns corresponding to constituent fingers. In contrast, dorsal premotor (PMd) and anterior superior parietal lobule (aSPL) showed substantial activation during preparation of multi-finger as compared to single-finger sequences. The same regions were also more activated during production of multi-finger sequences, suggesting that the same areas are involved in both pre- and online planning. Nonetheless, we observed small but robust differences between the two contrasts, suggesting preferential involvements of these areas in pre- and online planning. Multivariate analysis revealed sequence-specific representations in both PMd and aSPL, which remained stable across both preparation and production phases. This suggests that these areas maintain a sequence-specific representation before and during sequence production, likely guiding the execution-related areas. Significance StatementUnderstanding how the brain orchestrates complex behavior remains a core challenge in human neuroscience. Here, we combine high-resolution neuroimaging and a carefully crafted design to study the neural control of rapid sequential finger movements, like typing or playing the piano. Advancing prior research, we show that the brain areas involved in planning these movements maintain those representations throughout the execution of the sequence. This representational stability across planning and execution suggests an intricate connection between these processes. Our results shed light on the nuanced contributions of different cortical areas to different aspects of coordinating skilled movement. This work is well placed to inform future research in animal models and the development of targeted interventions against movement disorders.

neuroscience↗

bioRxiv2023

Neural correlates of online action preparation

When performing movements in rapid succession, the brain needs to coordinate preparation of an upcoming action with ongoing execution. Here we identify the processes and brain areas involved in this ability. Human participants performed pairs of single-finger presses or three-finger chords in settings where they had to prepare the second movement before or after the first response. Despite matched perceptual and movement requirements, 7T functional MRI revealed increased brain activity in regions along the intra-parietal sulcus and ventral visual stream when actions overlapped. Multivariate analyses suggested that these areas were involved in stimulus identification and action selection. In contrast, the dorsal premotor cortex, known to be involved in planning upcoming movements, showed no discernible signs of heightened activity. This observation suggests that the bottleneck during simultaneous action control and preparation arises at the level of stimulus identification and action selection, whereas movement planning in the premotor cortex can unfold concurrently with execution without interference between the two processes. SummaryThe brains ability to prepare for upcoming actions while controlling ongoing movements is a crucial evolutionary adaptation of the action system. However, the neural basis of online action preparation remains largely unknown. We found that superior-parietal and occipito-temporal areas exhibited heightened activation during online preparation. Surprisingly, the dorsal premotor cortex, known to be a crucial structure in motor planning, did not display additional activation for overlapping actions. These findings imply that while motor planning within the premotor cortex can occur in parallel with the execution of ongoing movement, the parallel stimulus identification and action selection in the posterior parietal cortex requires additional neural processes. HighlightsO_LIIndividuals prepare upcoming actions while simultaneously controlling ongoing movement C_LIO_LIWhen these two processes overlap, superior-parietal and occipito-temporal areas show increased activation C_LIO_LIMultivariate analysis suggests that increased activation arises to resolve simultaneous stimulus identification and action selection C_LIO_LIThe premotor cortex, known to be involved in motor planning, coordinates simultaneous planning and execution without extra neural engagement C_LI

neuroscience↗

bioRxiv2023

Interaction of multiple future movement plans in sequential reaching

Real world actions often comprise of a series of movements that cannot be entirely planned before initiation. When these actions are executed rapidly, the planning of multiple future movements needs to occur simultaneously with the ongoing action. How the brain solves this task remains unknown. Here we address this question with a new sequential arm reaching paradigm that manipulates how many future reaches are available for planning while controlling execution of the ongoing reach. We show that participants plan at least two future reaches simultaneously with an ongoing reach. Further, the planning processes of the two future reaches are not independent of one another. Evidence that the planning processes interact is two-fold. First, correcting for a visual perturbation of the ongoing reach target is slower when more future reaches are planned. Second, the curvature of the current reach is modified based on the next reach only when their planning processes temporally overlap. These interactions between future planning processes may enable smooth production of sequential actions by linking individual segments of a long sequence at the level of motor planning.

neuroscience↗

bioRxiv2020

Motor planning brings human primary somatosensory cortex into movement-specific preparatory states

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. Significance statementMotor planning is important for good behavioral performance, yet it is unclear which neural processes underlie the preparation of the nervous system for an upcoming movement. Using high-resolution functional neuroimaging, we investigated how motor planning for finger presses changes the activity state in primary motor and primary somatosensory cortex, and how brain responses during planning and execution relate to each other. We show that planning leads to finger-specific activation in both M1 and S1, which is highly similar to the finger-specific activity patterns elicited during execution. Our findings suggest that S1 is being specifically prepared for an upcoming action, either to actively contribute to the outflowing motor command or to enable action-specific sensory gating.

neuroscience↗

bioRxiv2020

The planning horizon for movement sequences

When performing a long chain of actions in rapid sequence, future movements need to be planned concurrently with ongoing action. However, how far ahead we plan, and whether this ability improves with practice, is currently unknown. Here we designed an experiment in which healthy volunteers produced sequences of 14 finger presses quickly and accurately on a keyboard in response to numerical stimuli. On every trial, participants were only shown a fixed number of stimuli ahead of the current keypress. The size of this viewing window varied between 1 (next digit revealed with the pressing of the current key) and 14 (full view of the sequence). Participants practiced the task for five days and their performance was continuously assessed on random sequences. Our results indicate that participants used the available visual information to plan multiple actions into the future, but that the planning horizon was limited: receiving information about more than 3 movements ahead did not result in faster sequence production. Over the course of practice, we found larger performance improvements for larger viewing windows and an expansion of the planning horizon. These findings suggest that the ability to plan future responses during ongoing movement constitutes an important aspect of skillful movement. Based on the results, we propose a framework to investigate the neuronal processes underlying simultaneous planning and execution. Significance StatementAlthough skill learning has typically focused on the training of specific movement sequences, practice improves performance even for random sequences. Here we hypothesize that a fundamental aspect of skilled sequential behavior is the ability to plan multiple actions into the future, both before and during execution. By controlling the amount of visual information available for motor planning, we show that people plan at least three movements beyond current action and that this planning horizon expands with practice. Our findings suggest that coordinating ongoing movement and planning of future actions is an essential component of skilled sequential behavior and offer testable predictions for the neural implementation of online motor planning.

neuroscience↗

bioRxiv2019

Repetita iuvant: repetition facilitates online planning of sequential movements

Beyond being essential for long-term motor-skill development, movement repetition has immediate benefits on performance, increasing speed and accuracy of a second execution. While repetition effects have been reported for single reaching movements, it has yet to be determined whether they also occur for movement sequences, and what aspects of sequence production are improved. We addressed these questions in two behavioral experiments using a discrete sequence production (DSP) task in which human volunteers had to perform short sequences of finger movements. In Experiment 1, we presented participants with randomly varying sequences and manipulated 1) whether the same sequence was repeated on successive trials, and 2) whether participants had to execute the sequence (Go), or not (No-Go). We establish that sequence repetition led to immediate improvements in speed without associated accuracy costs. The largest benefit was observed in the middle part of a sequence, suggesting that sequence repetition facilitated online planning. This claim was further supported by Experiment 2, in which we kept a set of sequences fixed throughout the experiment, thus allowing participants to develop sequence-specific learning: once the need for online planning decreased, the benefit of repetition disappeared. Finally, we found that repetition-related improvements only occurred for the trials that had been preceded by sequence production, suggesting that action selection and sequence pre-planning may not be sufficient to reap the benefits of repetition. Together, these results show that repetition can enhance representations at the level of movement sequences (rather than of individual movements) and facilitate online planning. New & NoteworthyEven for overlearned motor skills such as reaching, movement repetition improves performance. How brain processes associated with motor planning or execution benefit from repetition, however, remains unclear. Here we report the novel finding of repetition effects for sequential movements. Our results show that repetition benefits are tied to improved online planning of upcoming sequence elements. We also highlight how actual movement experience appears to be more beneficial than mental rehearsal for observing short-term repetition effects.

neuroscience↗

bioRxiv2019

Sequence learning is driven by improvements in motor planning

The ability to perform complex sequences of movements quickly and accurately is critical for many motor skills. While training improves performance in a large variety of motor-sequence tasks, the precise mechanisms behind such improvements are poorly understood. Here we investigated the contribution of single-action selection, sequence pre-planning, online planning, and motor execution to performance in a discrete sequence production (DSP) task. Five visually-presented numbers cued a sequence of five finger presses, which had to be executed as quickly and accurately as possible. To study how sequence planning influenced sequence production, we manipulated the amount of time that participants were given to prepare each sequence by using a forced-response paradigm. Over 4 days, participants were trained on 10 sequences and tested on 80 novel sequences. Our results revealed that participants became faster in selecting individual finger presses. They also preplanned 3-4 sequence items into the future, and the speed of pre-planning improved for trained, but not for untrained, sequences. Because pre-planning capacity remained limited, the remaining sequence elements had to be planned online during sequence execution, a process that also improved with sequence-specific training. Overall, our results support the view that motor sequence learning effects are best characterized by improvements in planning processes that occur both before and concurrently with motor execution.\n\nNew & NoteworthyComplex skills often require the production of sequential movements. While practice improves performance, it remains unclear how these improvements are achieved. Our findings show that learning effects in a sequence production task can be attributed to an enhanced ability to plan upcoming movements. These results shed new light on planning processes in the context of movement sequences, and have important implications for our understanding of the neural mechanisms that underlie skill acquisition.

neuroscience↗