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Production of rapid movement sequences relies on preparation before (preplanning) and during (online planning) movement. Here, we compared these processes and asked whether they recruit different cortical areas. Human participants performed three single-finger and three multifinger sequences in a delayed-movement paradigm while undergoing a 7 T functional MRI. During preparation, primary motor (M1) and somatosensory (S1) areas showed preactivation of the first movement, even without increases in overall activation. During production, the temporal summation of activity patterns corresponding to constituent fingers explained activity in these areas (M1 and S1). In contrast, the dorsal premotor cortex (PMd) and anterior superior parietal lobule (aSPL) showed substantial activation during the preparation (preplanning) of multifinger compared with single-finger sequences. These regions (PMd and aSPL) were also more active during production of multifinger sequences, suggesting that pre- and online planning may recruit the same regions. However, we observed small but robust differences between the two contrasts, suggesting distinct contributions to pre- and online planning. Multivariate analysis revealed sequence-specific representations in both PMd and aSPL, which remained stable across both preparation and production phases. Our analyses show that these areas maintain a sequence-specific representation before and during sequence production, likely guiding the execution-related areas in the production of rapid movement sequences. [ABSTRACT FROM AUTHOR]

Plasticity in the subcortical motor basal ganglia--thalamo--cerebellar network plays a key role in the acquisition and control of long-term memory for new procedural skills, from the formation of population trajectories controlling trained motor skills in the striatum to the adaptation of sensorimotor maps in the cerebellum. However, recent findings demonstrate the involvement of a wider cortical and subcortical brain network in the consolidation and control of well-trained actions, including a brain region traditionally associated with declarative memory--the hippocampus. Here, we probe which role these subcortical areas play in skilled motor sequence control, from sequence feature selection during planning to their integration during sequence execution. An fMRI dataset (N = 24; 14 females) collected after participants learnt to produce four finger press sequences entirely from memory with high movement and timing accuracy over several days was examined for both changes in BOLD activity and their informational content in subcortical regions of interest. Although there was a widespread activity increase in effector-related striatal, thalamic, and cerebellar regions, in particular during sequence execution, the associated activity did not contain information on the motor sequence identity. In contrast, hippocampal activity increased during planning and predicted the order of the upcoming sequence of movements. Our findings suggest that the hippocampus preorders movements for skilled action sequences, thus contributing to the higher-order control of skilled movements that require flexible retrieval. These findings challenge the traditional taxonomy of episodic and procedural memory and carry implications for the rehabilitation of individuals with neurodegenerative disorders. [ABSTRACT FROM AUTHOR]

The neural mechanisms of motor planning have been extensively studied in rodents. Preparatory activity in the frontal cortex predicts upcoming choice, but limitations of typical tasks have made it challenging to determine whether the spatial information is in a selfcentered direction reference frame or a world-centered position reference frame. Here, we trained male rats to make delayed visually guided orienting movements to six different directions, with four different target positions for each direction, which allowed us to disentangle direction versus position tuning in neural activity. We recorded single unit activity from the rat frontal orienting field (FOF) in the secondary motor cortex, a region involved in planning orienting movements. Population analyses revealed that the FOF encodes two separate 2D maps of space. First, a 2D map of the planned and ongoing movement in a self-centered direction reference frame. Second, a 2Dmap of the animal's current position on the port wall in a world-centered reference frame. Thus, preparatory activity in the FOF represents self-centered upcoming movement directions, but FOF neurons multiplex both self- and world-reference frame variables at the level of single neurons. Neural network model comparison supports the view that despite the presence of world-centered representations, the FOF receives the target information as self-centered input and generates self-centered planning signals. [ABSTRACT FROM AUTHOR]

When performing movements in rapid succession, the brain needs to coordinate ongoing execution with the preparation of an upcoming action. Here we identify the processes and brain areas involved in this ability of online preparation. Human participants (both male and female) performed pairs of single-finger presses or three-finger chords in rapid succession, while 7T fMRI was recorded. In the overlap condition, they could prepare the second movement during the first response and in the nonoverlap condition only after the first response was completed. Despite matched perceptual and movement requirements, fMRI revealed increased brain activity in the overlap condition in regions along the intraparietal sulcus and ventral visual stream. Multivariate analyses suggested that these areas are 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 execution and preparation arises at the level of stimulus identification and action selection, whereas movement planning in the premotor cortex can unfold concurrently with the execution of a current action without requiring additional neural activity. [ABSTRACT FROM AUTHOR]

Human motor behavior involves planning and execution of actions, some more frequently. Manipulating probability distribution of a movement through intensive direction-specific repetition causes physiological bias toward that direction, which can be cortically evoked by transcranial magnetic stimulation (TMS). However, because evoked movement has not been used to distinguish movement execution and plan histories to date, it is unclear whether the bias is because of frequently executed movements or recent planning of movement. Here, in a cohort of 40 participants (22 female), we separately manipulate the recent history of movement plans and execution and probe the resulting effects on physiological biases using TMS and on the default plan for goal-directed actions using a timed-response task. Baseline physiological biases shared similar low-level kinematic properties (direction) to a default plan for upcoming movement. However, manipulation of recent execution history via repetitions toward a specific direction significantly affected physiological biases, but not plan-based goal-directed movement. To further determine whether physiological biases reflect ongoing motor planning, we biased plan history by increasing the likelihood of a specific target location and found a significant effect on the default plan for goal-directed movements. However, TMS-evoked movement during preparation did not become biased toward the most frequent plan. This suggests that physiological biases may either provide a readout of the default state of primary motor cortex population activity in the movement-related space, but not ongoing neural activation in the planning-related space, or that practice induces sensitization of neurons involved in the practiced movement, calling into question the relevance of cortically evoked physiological biases to voluntary movements. [ABSTRACT FROM AUTHOR]

Contemporary motor control theories propose competition between multiple motor plans before the winning command is executed. While most competitions are completed before movement onset, movements are often initiated before the competition has been resolved. An example of this is saccadic averaging, wherein the eyes land at an intermediate location between two visual targets. Behavioral and neurophysiological signatures of competing motor commands have also been reported for reaching movements, but debate remains about whether such signatures attest to an unresolved competition, arise from averaging across many trials, or reflect a strategy to optimize behavior given task constraints. Here, we recorded EMG activity from an upper limb muscle (m. pectoralis) while 12 (8 female) participants performed an immediate response reach task, freely choosing between one of two identical and suddenly presented visual targets. On each trial, muscle recruitment showed two distinct phases of directionally tuned activity. In the first wave, time-locked ;100 ms of target presentation, muscle activity was clearly influenced by the nonchosen target, reflecting a competition between reach commands that was biased in favor of the ultimately chosen target. This resulted in an initial movement intermediate between the two targets. In contrast, the second wave, time-locked to voluntary reach onset, was not biased toward the nonchosen target, showing that the competition between targets was resolved. Instead, this wave of activity compensated for the averaging induced by the first wave. Thus, single-trial analysis reveals an evolution in how the nonchosen target differentially influences the first and second wave of muscle activity. [ABSTRACT FROM AUTHOR]

The planning and execution of head-beak movements are vital components of bird behavior. They require integration of sensory input and internal processes with goal-directed motor output. Despite its relevance, the neurophysiological mechanisms underlying action planning and execution outside of the song system are largely unknown. We recorded single-neuron activity from the associative endbrain area nidopallium caudolaterale (NCL) of two male carrion crows (Corvus corone) trained to plan and execute head-beak movements in a spatial delayed response task. The crows were instructed to plan an impending movement toward one of eight possible targets on the left or right side of a touchscreen. In a fraction of trials, the crows were prompted to plan a movement toward a self-chosen target. NCL neurons signaled the impending motion direction in instructed trials. Tuned neuronal activity during motor planning categorically represented the target side, but also specific target locations. As a marker of intentional movement preparation, neuronal activity reliably predicted both target side and specific target location when the crows were free to select a target. In addition, NCL neurons were tuned to specific target locations during movement execution. A subset of neurons was tuned during both planning and execution period; these neurons experienced a sharpening of spatial tuning with the transition from planning to execution. These results show that the avian NCL not only represents high-level sensory and cognitive task components, but also transforms behaviorally-relevant information into dynamic action plans and motor execution during the volitional perception-action cycle of birds. [ABSTRACT FROM AUTHOR]

Neurobehavioral studies in humans have long concentrated on changes in local activity levels during repetitive executions of a task. Spontaneous neural coupling within extended networks has latterly been found to also influence performance. Here, we intend to uncover the underlying mechanisms, the relative importance, and the interaction between spontaneous coupling and task-induced activations. To do so, we recorded two groups of healthy participants (male and female) during rest and while they performed either a visual perception or a motor sequence task. We demonstrate that, for both tasks, stronger activations during the task as well as greater network coupling through spontaneous α rhythms at rest predict performance. However, high performers present an absence of classical task-induced activations and, instead, stronger spontaneous network coupling. Activations were thus a compensation mechanism needed only in subjects with lower spontaneous network interactions. This challenges classical models of neural processing and calls for new strategies in attempts to train and enhance performance. [ABSTRACT FROM AUTHOR]

A central function of the brain is to plan, predict, and imagine the effect of movement in a dynamically changing environment. Here we show that in mice head-fixed in a plus-maze, floating on air, and trained to pick lanes based on visual stimuli, the asymmetric movement, and position of whiskers on the two sides of the face signals whether the animal is moving, turning, expecting reward, or licking. We show that (1) whisking asymmetry is coordinated with behavioral state, and that behavioral state can be decoded and predicted based on asymmetry, (2) even in the absence of tactile input, whisker positioning and asymmetry nevertheless relate to behavioral state, and (3) movement of the nose correlates with asymmetry, indicating that facial expression of the mouse is itself correlated with behavioral state. These results indicate that the movement of whiskers, a behavior that is not instructed or necessary in the task, can inform an observer about what a mouse is doing in the maze. Thus, the position of these mobile tactile sensors reflects a behavioral and movementpreparation state of the mouse. [ABSTRACT FROM AUTHOR]

The posterior parietal cortex (PPC) in rodents is reciprocally connected to primary somatosensory and vibrissal motor cortices. The PPC neuronal circuitry could thus encode and potentially integrate incoming somatosensory information and whisker motor output. However, the information encoded across PPC layers during refined sensorimotor behavior remains largely unknown. To uncover the sensorimotor features represented in PPC during voluntary whisking and object touch, we performed loose-patch single-unit recordings and extracellular recordings of ensemble activity, covering all layers of PPC in anesthetized and awake, behaving male rats. First, using single-cell receptive field mapping, we revealed the presence of coarse somatotopy along the mediolateral axis in PPC. Second, we found that spiking activity was modulated during exploratory whisking in layers 2- 4 and layer 6, but not in layer 5 of awake, behaving rats. Population spiking activity preceded actual movement, and whisker trajectory endpoints could be decoded by population spiking, suggesting that PPC is involved in movement planning. Finally, population spiking activity further increased in response to active whisker touch but only in PPC layers 2-4. Thus, we find layer-specific processing, which emphasizes the computational role of PPC during whisker sensorimotor behavior. [ABSTRACT FROM AUTHOR]

Humans are particularly good at copying novel and meaningless gestures. The mechanistic and anatomical basis for this specialized imitation ability remains largely unknown. One idea is that imitation occurs by matching body configurations. Here we propose an alternative route to imitation that depends on a body-independent representation of the trajectory path of the end-effector. We studied a group of patients with strokes in the left frontoparietal cortices. We found that they were equally impaired at imitating movement trajectories using the ipsilesional limb (i.e., the nonparetic side) that were cued either by an actor using their whole arm or just by a cursor, suggesting that body configuration information is not always critical for imitation and that a representation of abstract trajectory shape may suffice. In addition, imitation ability was uncorrelated to the ability to identify the trajectory shape, suggesting that imitation deficits were unlikely to arise from perceptual impairments. Finally, a lesion-symptom mapping analysis found that imitation deficits were associated with lesions in left dorsal premotor but not parietal cortex. Together, these findings suggest a novel body-independent route to imitation that relies on the ability to plan abstract movement trajectories within dorsal premotor cortex. [ABSTRACT FROM AUTHOR]

Neurons in multiple brain regions fire trains of action potentials anticipating specific movements, but this "preparatory activity" has not been systematically compared across behavioral tasks. We compared preparatory activity in auditory and tactile delayed-response tasks in male mice. Skilled, directional licking was the motor output. The anterior lateral motor cortex (ALM) is necessary for motor planning in both tasks. Multiple features of ALM preparatory activity during the delay epoch were similar across tasks. First, most neurons showed direction-selective activity and spatially intermingled neurons were selective for either movement direction. Second, many cells showed mixed coding of sensory stimulus and licking direction, with a bias toward licking direction. Third, delay activity was monotonic and low-dimensional. Fourth, pairs of neurons with similar direction selectivity showed high spike-count correlations. Our study forms the foundation to analyze the neural circuit mechanisms underlying preparatory activity in a genetically tractable model organism. [ABSTRACT FROM AUTHOR]

The parietal reach region (PRR) is known to be involved in the preparation of visually guided arm movements to single targets. We explored whether PRR encodes only the target of the next movement or, alternatively, also a subsequent goal in a double-reach sequence. Two monkeys were trained to memorize the locations of two peripheral cues and to prepare for a memory-guided delayed double-reach sequence. On a GO-signal they had to reach in a predefined order to both remembered target locations without breaking eye fixation. The movement goals were arranged such that either the first or the second target was inside the response field of an isolated neuron. We analyzed the neural activity of single cells in PRR during the late memory period between cue offset and the GO-signal. During this memory period, most PRR cells encoded the first as well as the second goal of the planned reaching sequence. The results indicate that the posterior parietal cortex is involved in the spatial planning of more complex action patterns and represents immediate and subsequent movement goals. [ABSTRACT FROM AUTHOR]

To reach for something we see, the brain must integrate the target location with the limb to be used for reaching. Neuronal activity in the parietal reach region (PRR) located in the posterior parietal cortex represents targets for reaching. Does this representation depend on the limb to be used? We found a continuum of limb-dependent and limb-independent responses: some neurons represented targets for movements of either limb, whereas others represented only contralateral-limb targets. Only a few cells represented ipsilateral-limb targets. Furthermore, these representations were not dependent on preferred direction. Additional experiments provide evidence that the PRR is specifically involved in contralateral-limb movements: firing rates are correlated with contralateral- but not ipsilateral-limb reaction times. The current study therefore provides novel evidence that the PRR operates as a limb-dependent stage that lies further along the sensory-motor transformation for visually guided reaching than previously expected. [ABSTRACT FROM AUTHOR]

People generally select a similar speed for a given motor task, such as reaching for a cup. One well established determinant of movement time is the speed--accuracy trade-off: movement time increases with the accuracy requirement. A second possible determinant is the energetic cost of making a movement. Parkinson's disease (PD), a condition characterized by generalized movement slowing (bradykinesia), provides the opportunity to directly explore this second possibility. We compared reaching movements of patients with PD with those of control subjects in a speed--accuracy trade-off task comprising conditions of increasing difficulty. Subjects completed as many trials as necessary to make 20 movements within a required speed range (trials to criterion, Nc). Difficulty was reflected in endpoint accuracy and Nc. Patients were as accurate as control subjects in all conditions (i.e., PD did not affect the speed--accuracy trade-off). However, Nc was consistently higher in patients, indicating reluctance to move fast although accuracy was not compromised. Specifically, the dependence of Nc on movement energy cost (slope SN) was steeper in patients than in control subjects. This difference in SN suggests that bradykinesia represents an implicit decision not to move fast because of a shift in the cost/benefit ratio of the energy expenditure needed to move at normal speed. SN was less steep, but statistically significant, in control subjects, which demonstrates a role for energetic cost in the normal control of movement speed. We propose that, analogous to the established role of dopamine in explicit reward-seeking behavior, the dopaminergic projection to the striatum provides a signal for implicit "motor motivation." [ABSTRACT FROM AUTHOR]

Basing higher-order decisions on expected value (reward probability X reward magnitude) maximizes an agent's accruement of reward over time. The goal of this study was to determine whether the advanced preparation of simple actions reflected the expected value of the potential outcomes. Human subjects were required to direct a saccadic eye movement to a visual target that was presented either to the left or right of a central fixation point on each trial. Expected value was manipulated by adjusting the probability of presenting each target and their associated magnitude of monetary reward across 15 blocks of trials. We found that saccadic reaction times (SRTs) were negatively correlated to the relative expected value of the targets. Occasionally, an irrelevant visual distractor was presented before the target to probe the spatial allocation of saccadic preparation. Distractor-directed errors (oculomotor captures) varied as a function of the relative expected value of, and the distance of distractors from, the potential valued targets. SRTs and oculomotor captures were better correlated to the relative expected value of actions than to reward probability, reward magnitude, or overall motivation. Together, our results suggest that the level and spatial distribution of competitive dynamic neural fields representing saccadic preparation reflect the relative expected value of the potential actions. [ABSTRACT FROM AUTHOR]

Perceptual attention and target choice for movement have many features in common. In particular, both generally are based on selection of a particular location in space. To ask whether motor control, like attention, also can exhibit target choice based on nonspatial features of the stimulus, we assessed the initiation of smooth pursuit eye movements when two targets move in different directions after human subjects have been cued which direction or color to track. The direction cue consisted of a patch of dots undergoing either 0% coherent motion or 50% coherent motion in the direction of motion of one of the subsequent targets. After a delay, the fixation spot was extinguished and two spots moved across the same small region of the visual field, one in the cued direction ("target") and one in an orthogonal direction ("distracter"). After the 0% coherent cue, pursuit was approximately the vector average of responses to the two motions presented singly. After the 50% coherent cue, the initial pursuit response was biased strongly toward the target that moved in the cued direction. The impact of the cued direction persisted over delays of up to 1000 ms. Other cues about the direction of upcoming target motion biased the response similarly. Cues about target color also biased pursuit in the direction of motion of the cued target but were considerably less effective than cues indicating the direction of target motion. We conclude that target choice for movement, like perceptual attention, can be based on the features of the chosen target and not only its location in space. [ABSTRACT FROM AUTHOR]

We present experiments and analyses designed to test the idea that firing rates in premotor cortex become optimized during motor preparation, approaching their ideal values over time. We measured the across-trial variability of neural responses in dorsal premotor cortex of three monkeys performing a delayed-reach task. Such variability was initially high, but declined after target onset, and was maintained at a rough plateau during the delay. An additional decline was observed after the go cue. Between target onset and movement onset, variability declined by an average of 34%. This decline in variability was observed even when mean firing rate changed little. We hypothesize that this effect is related to the progress of motor preparation. In this interpretation, firing rates are initially variable across trials but are brought, over time, to their "appropriate" values, becoming consistent in the process. Consistent with this hypothesis, reaction times were longer if the go cue was presented shortly after target onset, when variability was still high, and were shorter if the go cue was presented well after target onset, when variability had fallen to its plateau. A similar effect was observed for the natural variability in reaction time: longer (shorter) reaction times tended to occur on trials in which firing rates were more (less) variable. These results reveal a remarkable degree of temporal structure in the variability of cortical neurons. The relationship with reaction time argues that the changes in variability approximately track the progress of motor preparation. [ABSTRACT FROM AUTHOR]