Execution Of Goal-directed Movements Research Articles

Long-range monosynaptic inputs targeting apical and basal dendrites of primary motor cortex deep output neurons.

The primary motor cortex (M1) integrates various long-range signals from other brain regions for the learning and execution of goal-directed movements. How the different inputs target the distinct apical and basal dendrites of M1 pyramidal neurons is crucial in understanding the functions of M1, but the detailed connectivity pattern is still largely unknown. Here, by combining cre-dependent rabies virus tracing, layer-specific chemical retrograde tracing, optogenetic stimulation, and electrophysiological recording, we mapped all long-range monosynaptic inputs to M1 deep output neurons in layer 5 (L5) in mice. We revealed that most upstream areas innervate both dendritic compartments concurrently. These include the sensory cortices, higher motor cortices, sensory and motor thalamus, association cortices, as well as many subcortical nuclei. Furthermore, the dichotomous inputs arise mostly from spatially segregated neuronal subpopulations within an upstream nucleus, and even in the case of an individual cortical layer. Therefore, these input areas could serve as both feedforward and feedback sources albeit via different subpopulations. Taken together, our findings revealed a previously unknown and highly intricate synaptic input pattern of M1L5 neurons, which implicates that the dendritic computations carried out by these neurons during motor execution or learning are far more complicated than we currently understand.

Neural Code of Motor Planning and Execution during Goal-Directed Movements in Crows.

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.SIGNIFICANCE STATEMENT Corvid songbirds have become exciting new models for understanding complex cognitive behavior. As a key neural underpinning, the endbrain area nidopallium caudolaterale (NCL) represents sensory and memory-related task components. How such representations are converted into goal-directed motor output remained unknown. In crows, we report that NCL neurons are involved in the planning and execution of goal-directed movements. NCL neurons prospectively signaled motion directions in instructed trials, but also when the crows were free to choose a target. NCL neurons showed a target-specific sharpening of tuning with the transition from the planning to the execution period. Thus, the avian NCL not only represents high-level sensory and cognitive task components, but also transforms relevant information into action plans and motor execution.

Differential calcium channel-mediated dopaminergic modulation in the subthalamonigral synapse.

Dopamine (DA) modulates basal ganglia (BG) activity for initiation and execution of goal-directed movements and habits. While most studies are aimed to striatal function, the cellular and molecular mechanisms underlying dopaminergic regulation in other nuclei of the BG are not well understood. Therefore, we set to analyze the dopaminergic modulation occurring in subthalamo-nigral synapse, in both pars compacta (SNc) and pars reticulata (SNr) neurons, because these synapses are important for the integration of information previously processed in striatum and globus pallidus. In this study, electrophysiological and pharmacological evidence of dopaminergic modulation on glutamate release through calcium channels is presented. Using paired pulse ratio (PPR) measurements and selective blockers of these ionic channels, together with agonists and antagonists of DA D2 -like receptors, we found that blockade of the CaV 3 family occludes the presynaptic inhibition produced by the activation of DA receptors pharmacologically profiled as D3 -type in the STh-SNc synapses. On the contrast, the blockade of CaV 2 channels, but not CaV 3, occlude with the effect of the D3 agonist, PD 128907, in the STh-SNr synapse. The functional role of this differential distribution of calcium channels that modulate the release of glutamate in the SN implies a fine adjustment of firing for both classes of neurons. Dopaminergic neurons of the SNc establish a DA tone within the SN based on the excitatory/inhibitory inputs; such tone may contribute to processing information from subthalamic nucleus and could also be involved in pathological DA depletion that drives hyperexcitation of SNr neurons.

Effects of visuomotor delays on the control of movement and on perceptual localization in the presence and absence of visual targets.

The sensory system constantly deals with delayed feedback. Recent studies showed that playing a virtual game of pong with delayed feedback caused hypermetric reaching movements. We investigated whether this effect is associated with a perceptual bias. In addition, we examined the importance of the target in causing hypermetric movements. In a first experiment, participants played a delayed pong game and blindly reached to presented targets. Following each reaching movement, they assessed the position of the invisible cursor. We found that participants performed hypermetric movements but reported that the invisible cursor reached the target, suggesting that they were unaware of the hypermetria and that their perception was biased toward the target rather than toward their hand position. In a second experiment, we removed the visual target, and strikingly, the hypermetria vanished. Moreover, participants reported that the invisible cursor was located with their hand. Taking these results together, we conclude that the adaptation to the visuomotor delay during the pong game selectively affected the execution of goal directed movements, resulting in hypermetria and perceptual bias when movements are directed toward visual targets but not when such targets are absent.NEW & NOTEWORTHY Recent studies showed that adaptation to visuomotor delays causes hypermetric movements in the absence of visual feedback, suggesting that visuomotor delay is represented using current state information. We report that this adaptation also affects perception. Importantly, both the motor and perceptual effects are selective to the representations that are used in the execution of goal-directed movements toward visual targets.

Attention and suppression affect tactile perception in reach-to-grasp movements

Reaching with the hand is characterized by a decrease in sensitivity to tactile stimuli presented to the moving hand. Here, we investigated whether tactile suppression can be canceled by attentional orienting. In a first experiment, participants performed a dual-task involving a goal-directed movement paired with the speeded detection of a tactile pulse. The pulse was either delivered to the moving or stationary hand, during movement preparation, execution, or the post-movement phase. Furthermore, stimulation was delivered with equal probability to either hand, or with a higher probability to either the moving or resting hand. The results highlighted faster RTs under conditions of higher probability of stimulation delivery to both moving and resting hands, thus indicating an attentional effect. For the motor preparation period, RTs were faster only at the resting hand under conditions where tactile stimulation was more likely to be delivered there. In a second experiment, a non-speeded perceptual task was used as a secondary task and tactile discrimination thresholds were recorded. Tactile stimulation was delivered concomitantly at both index fingers either in the movement preparation period (both before and after the selection of the movement effector had taken place), in the motor execution period, or, in a control condition, in the time-window of motor execution, but the movement of the hand was restrained. In the preparation period, tactile thresholds were comparable for the two timings of stimulation delivery; i.e., before and after the selection of the movement effector had taken place. These results therefore suggest that shortly prior to, and during, the execution of goal-directed movements, a combined facilitatory and inhibitory influence acts on tactile perception.

Descending Corticospinal Control of Intersegmental Dynamics

To make an accurate movement, the CNS has to overcome the inherent complexities of the multijoint limb. For example, interaction torques arise when motion of individual arm segments propagates to adjacent segments causing their movement without any muscle contractions. Since these passive joint torques significantly add to the overall torques generated by active muscular contractions, they must be taken into account during planning or execution of goal-directed movements. We investigated the role of the corticospinal tract in compensating for the interaction torques during arm movements in humans. Twelve subjects reached to visual targets with their arm supported by a robotic exoskeleton. Reaching to one target was accompanied by interaction torques that assisted the movement, while reaching to the other target was accompanied by interaction torques that resisted the movement. Corticospinal excitability was assessed at different times during movement using single-pulse transcranial magnetic stimulation (TMS) over the upper-arm region of M1 (primary motor cortex). We found that TMS responses in shoulder monoarticular and elbow-shoulder biarticular muscles changed together with the interaction torques during movements in which the interaction torques were resistive. In contrast, TMS responses did not correlate with assistive interaction torques or with co-contraction. This suggests that the descending motor command includes compensation for passive limb dynamics. Furthermore, our results suggest that compensation for interaction torques involves the biarticular muscles, which span both shoulder and elbow joints and are in a biomechanically advantageous position to provide such compensation.

Inactivation of the rat dorsal striatum impairs performance in spatial tasks and alters hippocampal theta in the freely moving rat

We analysed the interaction between the dorsal striatum (motor coordination and planning) and the hippocampus (sensory information processing and integration) during performance of goal-directed tasks. The performance of rats that had been injected with different doses of the D 2-antagonist Sulpiride into the dorsal striatum was tested in an egocentric 4-arm maze task that tests striatal functions. Furthermore, hippocampal EEGs were recorded before, during and after inactivation of the dorsal striatum via injections of Sulpiride of rats that were performing a continuous alternation task. Injection of 5 μl of 100 mM Sulpiride increased the number of errors committed in the egocentric 4-arm maze ( p < 0.01), indicating that the dorsal striatum is involved in motor control and motor memory recall in such a task. In the recording study, the same dose of Sulpiride injected into the dorsal striatum had powerful effects on the hippocampal EEG. The main activity in the theta range (5–10 Hz) was shifted from higher frequencies in the 8–10 Hz range to lower frequencies in the 5–7 Hz range ( p < 0.005). The impairment in the behavioural egocentric task after Sulpiride injection, and the effects of Sulpiride on hippocampal theta shows that there is a functional interaction between the dorsal striatum and the hippocampus. While the dorsal striatum coordinates the execution of complex motor programs, the hippocampus integrates spatial and other sensory information required for the planning and execution of goal-directed movements.

The effects of response priming on the planning and execution of goal-directed movements in the presence of a distracting stimulus

Two models of selective reaching have been proposed to account for deviations in movement trajectories in cluttered environments. The response vector model predicts movement trajectories should deviate towards or away from the location a distractor of little or large salience, respectively. In contrast, the response activation model predicts that a distractor with large salience should cause movement deviations towards it whereas a distractor with little salience should not influence the movement. The precuing technique was combined with the distractor interference paradigm to test these predictions. Results indicate that when the target was presented at the precued (salient) location, movements were unaffected by a distractor. Conversely, when the distractor was presented at the precued location while the target was presented at an uncued (non-salient) location, participants demonstrated increased reaction times and trajectory deviations towards the location of the distractor. These findings are consistent with the model of response activation.

Recovery from directional hypokinesia and bradykinesia in unilateral neglect

Patients with acute right hemisphere (RH) damage and left unilateral neglect may exhibit slowness in both the initiation and execution of goal-directed movements toward the contralesional side (respectively, directional hypokinesia and directional bradykinesia). We retested 13 patients with RH damage, who on initial testing 1 year earlier had shown these impairments on a visually cued sequential movement task. Initiation and execution times were measured separately for leftward and rightward movement sequences, performed in either hemispace and across the body midline. Patients with anterior/subcortical lesions exhibited directional hypokinesia and bradykinesia on initial testing, but no longer showed either after 12 months. It is suggested that the recovery exhibited by these patients was determined conjointly by residual functioning of flexible anterior/subcortical structures involved in response production, in addition to the resolution of transient secondary dysfunction (i.e., diaschisis) of posterior (parietal) areas responsible for attentional orienting and target selection. In contrast, patients with posterior (parietal) lesions continued to exhibit directional hypokinesia after 12 months, probably as a result of permanent damage to a region whose dedicated or specialised functions cannot readily be compensated by other brain areas. These results support the notion that spatial attention and goal-directed movement are subserved by a distributed network involving separate but interconnected brain regions. Distinct functional losses may be predicted, in both the acute and chronic stages postinjury, on the basis of temporary or permanent dysfunction of discrete components of this network.

Diffusion and absorption of (−)sulpiride and raclopride after intracerebral administration in the rat

We analysed the interaction between the dorsal striatum (motor coordination and planning) and the hippocampus (sensory information processing and integration) during performance of goal-directed tasks. The performance of rats that had been injected with different doses of the D2-antagonist Sulpiride into the dorsal striatum was tested in an egocentric 4-arm maze task that tests striatal functions. Furthermore, hippocampal EEGs were recorded before, during and after inactivation of the dorsal striatum via injections of Sulpiride of rats that were performing a continuous alternation task. Injection of 5 μl of 100 mM Sulpiride increased the number of errors committed in the egocentric 4-arm maze (p < 0.01), indicating that the dorsal striatum is involved in motor control and motor memory recall in such a task. In the recording study, the same dose of Sulpiride injected into the dorsal striatum had powerful effects on the hippocampal EEG. The main activity in the theta range (5–10 Hz) was shifted from higher frequencies in the 8–10 Hz range to lower frequencies in the 5–7 Hz range (p < 0.005). The impairment in the behavioural egocentric task after Sulpiride injection, and the effects of Sulpiride on hippocampal theta shows that there is a functional interaction between the dorsal striatum and the hippocampus. While the dorsal striatum coordinates the execution of complex motor programs, the hippocampus integrates spatial and other sensory information required for the planning and execution of goal-directed movements.