Chapter 17 - Brain mechanisms controlling decision making and motor planning

Many studies have associated mental imagery with motor control mechanisms by showing mutually active brain areas and functions, as well as similar temporal patterns of imagining and executing the same motor actions. One of the main conjectured mutual mechanisms is the Cerebellar forward-model, commonly believed to generate sensory predictions as part of both motor control and mental imagery processes. Nevertheless, trials to associate one’s overall individual mental and motor capacities have shown only mild and inconsistent correlations, hence challenging the mutual mechanism assumption. We hypothesized that one cause to this inconsistency is the forward-model’s dominance in the motor-planning stage only when adapting to novel sensorimotor environments, while the inverse-model is gradually taking the lead along the adaptation, and therefore biasing most attempts to measure motor-mental overlapping functions and correlate these measurements under regular circumstances. Our current study aimed to tackle and explore this gap using immersive virtual embodiment, by applying an experience of a fundamental sensorimotor conflict, thereby manipulating the sensory prediction mechanism, and presumably forcing an increased involvement of the forward-model in the motor planning stage throughout the experiment. In the study, two groups of subjects (n = 48) performed mental and manual rotation within an immersive, motion-captured, virtual reality environment, while the sensorimotor dynamics of only the test group were altered by physical-virtual speed re-mapping making the virtual hand move twice as fast as the physical hand controlling it. Individual mental imagery capacities were assessed before and after three blocks of manual-rotation, where motor planning durations were measured as the time until motion onset. The results show that virtual sensorimotor alteration extremely increases the correlation of mental imagery and motor planning (r = 0.9, p < .0001) and leads to higher mental imagery performance improvement following the physical blocks. We particularly show that virtual embodiment manipulation affects the motor planning stage to change and functionally overlap with imagery mechanisms, rather than the other way around, which supports our conjecture of an increased sensory-prediction forward-model involvement. Our results shed new light on the embodied nature of mental imagery, support the view of the predictive forward-model as a key mechanism mutually underlying motor control and imagery, and suggest virtual sensorimotor alteration as a novel methodology to increase physical-mental convergence. These findings also suggest the applicability of using existing motion-tracked virtual environments for continuous cognitive evaluation and treatment, through kinematic analysis of ongoing natural motor behaviors.

In the planning of a movement, the brain has the opportunity to delay the incorporation of accuracy requirements of the motor plan in order to reduce the reaction time by up to 100 ms (average: 32 ms). Such shortening of reaction time is observed here when the first phase of the movement consists of a transport phase. This forces us to reconsider the hypothesis that motor plans are fully defined before movement onset.

We examined whether the frontal eye fields (FEF) are involved in the suppression of reflexive saccades. Simultaneous recording of horizontal eye movements and functional magnetic resonance imaging enabled us to perform a randomized pro- and antisaccade task and to sort blood oxygenation level dependent (BOLD) time series on the basis of task performance. Saccadic reaction time distributions were comparable across tasks indicating a similar effort in preprocessing of the saccades. Furthermore, we found similar BOLD activation in FEF during both correctly performed pro- and antisaccades. Frontal eye field activation started prior to target presentation and saccade generation. While we observed only few erroneous antisaccades, these were associated with a decrease in BOLD activity prior to target presentation, and increased BOLD activity after target presentation relative to correctly performed antisaccades. These findings are consistent with a role of the FEF in the suppression of reflexive saccades. The increase in activity after target presentation for antisaccade errors can only be indirectly linked to such a role but may also reflect activity related to the generation of a correction saccade. Frontal eye field BOLD activity may further represent general arousal, preparatory set, short-term memory, or salience-map related activity.

Decision Making in Recurrent Neuronal Circuits

Even in the presence of significant motor limitations, how does physical action continue to be intensely elaborated by the brain? Cerebral palsy (CP) requires motor control to be understood not only as peripheral execution but as an internal construction of action. Between the intention to move and the possible action lies a representational domain in which movement is anticipated, organized, and mentally rehearsed, and it is at this conceptual level that motor imagery becomes central.1 Disregarding this dimension implies restricting rehabilitation to the observable body while neglecting neural processes responsible for intention and motor planning. Thus, shifting the focus to motor imagery means investigating not only whether the child moves, but how actions are planned and simulated before execution. This perspective poses a methodological challenge: how to empirically operationalize internal motor simulation processes. The Hand Laterality Test is widely used as an indirect measure of motor imagery because it requires mental rotation of one's own limb for spatial judgment. However, results based only on mean reaction time or accuracy have been inconsistent. In this context, the study by Breuer Asher et al.2 is particularly relevant for proposing performance variability as a primary indicator of imagery stability. This proposal aligns with contemporary models of motor control and cognition in CP, in which variability is interpreted as a marker of system instability. Accordingly, performance fluctuations should not be regarded as statistical noise but as manifestations of alterations in internal mechanisms of action simulation, supporting the hypothesis of Steenbergen et al.3 that imagery and planning deficits are qualitative and compromise representational consistency. The study by Breuer Asher et al.2 advances the field by showing that motor imagery in children with CP is characterized less by reduced accuracy and more by increased intraindividual variability, particularly in reaction time. By adopting variability as a core variable, the authors provide an integrative explanation for previously discrepant findings, suggesting that the main difficulty lies in performance instability rather than slowness.3, 4 This interpretation is consistent with a recent systematic review demonstrating substantial methodological and outcome heterogeneity, indicating that imagery deficits vary according to task demands, clinical subtype, and functional level.5 Moreover, the proposed composite score integrating accuracy and variability advances the clinical operationalization of motor imagery by offering a quantitative criterion capable of discriminating children with CP from typically developing peers and monitoring this ability over time. Despite these advances, controversies remain regarding the nature of the motor imagery deficit in CP. It is unclear whether increased variability reflects alterations in specific motor simulation mechanisms or broader limitations related to attention, executive functions, or working memory. Steenbergen et al.3 suggested that imagery impairments may be linked to general difficulties in action planning and representation rather than exclusively to simulation capacity. The high prevalence of attention-deficit/hyperactivity disorder in the sample studied by Breuer Asher et al.2 reinforces this complexity, as reaction time instability may reflect attentional fluctuations rather than failures of body representation alone. Thus, it remains unresolved whether variability constitutes a specific marker of imagery or a general index of cognitive instability. Clinically, these findings indicate that motor imagery should not be applied uniformly to children with CP, given distinct imagery performance profiles. Prior assessment is therefore necessary to guide eligibility and intervention design, as children with greater variability tend to respond less consistently to imagery-based protocols and may benefit from combined strategies incorporating attentional support and perceptual feedback, consistent with evidence of partial imagery preservation in unilateral CP.4 For future research, it will be important to determine whether performance variability is sensitive to training and whether it represents a stable trait or a modifiable state. The Article Processing Charge for the publication of this research was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) (ROR identifier: 00x0ma614). Not required.

Planning and coordination of a reach–grasp–eat task in children with hemiplegia

To aid in the successful execution of goal-directed walking (discrete movement from a start location to an end target) the central nervous system forms a predictive motor plan. For the motor plan to be effective, it must be adapted in response to environmental changes. Despite motor planning being inherent to goal-directed walking, it is not understood how the nervous system adapts these plans to interact with changing environments. Our objective was to understand how people adapt motor plans of center of mass (COM) trajectory during goal-directed walking in response to a consistent change in environmental dynamics. Participants preformed a series of goal-directed walking trials in a novel environment created by a cable robot that applied a lateral force field to their COM. We hypothesized that participants would adapt to the environment by forming an internal model of their COM trajectory within the force field. Our findings support this hypothesis. Initially, we found COM trajectory significantly deviated in the same direction as the applied field, relative to baseline (no field) (p = 0.002). However, with practice in the field, COM trajectory adapted back to the baseline (p = 0.6). When we unexpectedly removed the field, participants demonstrated after-effects, COM trajectory deviated in the direction opposite of the field relative to baseline (p < 0.001). Our findings suggest that when performing a goal-directed walking task, people adapt a motor plan that predicts the COM trajectory that will emerge from the interaction between a specific set of motor commands and the external environment.

Event-related desynchronization (ERD) is a relative attenuation in the spectral power of an electroencephalogram (EEG) observed over the sensorimotor area during motor execution and motor imagery. It is a well-known EEG feature and is commonly employed in brain-computer interfaces. However, its underlying neural mechanisms are not fully understood, as ERD is a single variable correlated with external events involving numerous pathways, such as motor intention, planning, and execution. In this study, we aimed to identify a dominant factor for inducing ERD. Participants were instructed to grasp their right hand with three different (10, 25, or 40%MVF: maximum voluntary force) levels under two distinct experimental conditions: a closed-loop condition involving real-time visual force feedback (VF) or an open-loop condition in a feedforward (FF) manner. In each condition, participants were instructed to repeat the grasping task a certain number of times with a timeline of Rest (10.0 s), Preparation (1.0 s), and Motor Execution (4.0 s) periods, respectively. EEG signals were recorded simultaneously with the motor task to evaluate the time-course of the event-related spectrum perturbation for each condition and dissect the modulation of EEG power. We performed statistical analysis of mu and beta-ERD under the instructed grasping force levels and the feedback conditions. In the FF condition (i.e., no force feedback), mu and beta-ERD were significantly attenuated in the contralateral motor cortex during the middle of the motor execution period, while ERD in the VF condition was maintained even during keep grasping. Only mu-ERD at the somatosensory cortex tended to be slightly stronger in high load conditions. The results suggest that the extent of ERD reflects neural activity involved in the motor planning process for changing virtual equilibrium point rather than the motor control process for recruiting motor neurons to regulate grasping force.

Actions often require the selection of a specific goal amongst a range of possibilities, like when a softball player must precisely position her glove to field a fast-approaching ground ball. Previous studies have suggested that during goal uncertainty the brain prepares for all potential goals in parallel and averages the corresponding motor plans to command an intermediate movement that is progressively refined as additional information becomes available. Although intermediate movements are widely observed, they could instead reflect a neural decision about the single best action choice given the uncertainty present. Here we systematically dissociate these possibilities using novel experimental manipulations and find that when confronted with uncertainty, humans generate a motor plan that optimizes task performance rather than averaging potential motor plans. In addition to accurate predictions of population-averaged changes in motor output, a novel computational model based on this performance-optimization theory accounted for a majority of the variance in individual differences between participants. Our findings resolve a long-standing question about how the brain selects an action to execute during goal uncertainty, providing fundamental insight into motor planning in the nervous system.

Application of the "gap paradigm" reduces mean saccadic reaction time (SRT). It enhances oculomotor response, sometimes showing express-like reactions within about 100-140 ms from target onset, which are called "express saccades." Despite some controversy, there is evidence that express and regular saccades may be controlled by different pathways, but it is still not clear which pathways are involved in the generation of express saccades. It was suggested that the substantia nigra (SN) could take part in the control of these saccades. We compared saccadic reaction times of 14 patients with mild to moderate Parkinson's disease (PD), which commonly affects the SN, with those of nine elderly normal subjects. The results show a clear gap effect and no significant difference between mean saccadic reaction times and reaction time distributions of the PD and the control group. In the gap condition, express saccades are present in several subjects of both groups. Therefore, it is concluded that the deficits in the SN pars compacta due to PD, which affect directly and indirectly the activity of the SN pars reticulata that projects to SC, do not dominantly influence the process of preparing and executing express and regular saccades in patients with mild to moderate PD.

Motor learning and COMT Val158met polymorphism: Analyses of oculomotor behavior and corticocortical communication.

Neuronal activity in the frontal eye field (FEF) ranges from purely motor (related to saccade production) to purely visual (related to stimulus presence). According to numerous studies, visual responses correlate strongly with early perceptual analysis of the visual scene, including the deployment of spatial attention, whereas motor responses do not. Thus, functionally, the consensus is that visually responsive FEF neurons select a target among visible objects, whereas motor-related neurons plan specific eye movements based on such earlier target selection. However, these conclusions are based on behavioral tasks that themselves promote a serial arrangement of perceptual analysis followed by motor planning. So, is the presumed functional hierarchy in FEF an intrinsic property of its circuitry or does it reflect just one possible mode of operation? We investigate this in monkeys performing a rapid-choice task in which, crucially, motor planning always starts ahead of task-critical perceptual analysis, and the two relevant spatial locations are equally informative and equally likely to be target or distracter. We find that the choice is instantiated in FEF as a competition between oculomotor plans, in agreement with model predictions. Notably, although perception strongly influences the motor neurons, it has little if any measurable impact on the visual cells; more generally, the more dominant the visual response, the weaker the perceptual modulation. The results indicate that, contrary to expectations, during rapid saccadic choices perceptual information may directly modulate ongoing saccadic plans, and this process is not contingent on prior selection of the saccadic goal by visually driven FEF responses.

The developmental nature of reaction time (RT) and anticipation timing (AT) performance, as well as the relationship between them, was investigated using 15 male and 15 female subjects at each of five age levels—7, 9, 11, 13, and 20 yrs. Each subject was given 40 trials for both RT and AT performance with task order counterbalanced. Results indicated that as age increased RT decreased, with males having more rapid RT than females. The two younger age groups differed from the three older groups on AT performance. RT was significantly correlated with AT (|CE| measure) for the 7, 9, and 11 yr old males but not in any other age by gender condition. Apparently neither young males nor young females have a good motor plan in memory to control AT performance. However, the more rapid RT (and thus better response initiation) of the males allows better AT performance at the younger ages. Beginning about 10–11 yrs of age, better motor plans are developed in children's memory system, leading to less reliance on rapid RT for good AT performance, and thus the correlation between RT and AT performance is not present.

The reaction times of saccadic eye movements have been studied extensively as a probe for cognitive behavior controlled by large-scale cortical and subcortical neural networks. Recent studies have shown that the reaction times of targeting saccades toward peripheral visual stimuli are prolonged by fixational saccades, the largest miniature eye movements including microsaccades. We have shown previously that the frequency of fixational saccades is decreased by volitional action preparation controlled internally during the antisaccade paradigm (look away from a stimulus). Instead, here we examined whether fixational saccade modulation induced externally by sensory events could also account for targeting saccade facilitation by the same sensory events. When targeting saccades were facilitated by prior fixation stimulus disappearance (gap effect), fixational saccade occurrence was reduced, which could theoretically facilitate targeting saccades. However, such reduction was followed immediately by the rebound of fixational saccade occurrence in some subjects, which could eliminate potential benefits from the previous fixational saccade reduction. These results do not mean that fixational saccades were unrelated to the gap effect because they indeed altered that effect by delaying targeting saccade initiation on trials without the fixation gap more strongly than trials with it. Such changes might be attributed to the disruption of volitional saccade preparation because the frequency of fixational saccades observed in this study was associated with the ability of volitional control over antisaccade behavior. These results suggest that fixational saccades alter the gap effect on targeting saccade reaction times, presumably by disrupting volitional saccade commands.

Recent data and motor control theory argues that movement planning involves preparing the neural state of primary motor cortex (M1) for forthcoming action execution. Theories related to internal models, feedback control, and predictive coding also emphasize the importance of sensory prediction (and processing) before (and during) the movement itself, explaining why motor-related deficits can arise from damage to primary somatosensory cortex (S1). Motivated by this work, here we examined whether motor planning, in addition to changing the neural state of M1, changes the neural state of S1, preparing it for the sensory feedback that arises during action. We tested this idea in two human functional MRI studies (N = 31, 16 females) involving delayed object manipulation tasks, focusing our analysis on premovement activity patterns in M1 and S1. We found that the motor effector to be used in the upcoming action could be decoded, well before movement, from neural activity in M1 in both studies. Critically, we found that this effector information was also present, well before movement, in S1. In particular, we found that the encoding of effector information in area 3b (S1 proper) was linked to the contralateral hand, similarly to that found in M1, whereas in areas 1 and 2 this encoding was present in both the contralateral and ipsilateral hemispheres. Together, these findings suggest that motor planning not only prepares the motor system for movement but also changes the neural state of the somatosensory system, presumably allowing it to anticipate the sensory information received during movement.SIGNIFICANCE STATEMENT Whereas recent work on motor cortex has emphasized the critical role of movement planning in preparing neural activity for movement generation, it has not investigated the extent to which planning also modulates the activity in the adjacent primary somatosensory cortex. This reflects a key gap in knowledge, given that recent motor control theories emphasize the importance of sensory feedback processing in effective movement generation. Here, we find through a convergence of experiments and analyses, that the planning of object manipulation tasks, in addition to modulating the activity in the motor cortex, changes the state of neural activity in different subfields of the human S1. We suggest that this modulation prepares the S1 for the sensory information it will receive during action execution.