Hasty sensorimotor decisions rely on an overlap of broad and selective changes in motor activity.

Humans and other animals are able to adjust their speed-accuracy trade-off (SAT) at will depending on the urge to act, favoring either cautious or hasty decision policies in different contexts. An emerging view is that SAT regulation relies on influences exerting broad changes on the motor system, tuning its activity up globally when hastiness is at premium. The present study aimed to test this hypothesis. A total of 50 participants performed a task involving choices between left and right index fingers, in which incorrect choices led either to a high or to a low penalty in 2 contexts, inciting them to emphasize either cautious or hasty policies. We applied transcranial magnetic stimulation (TMS) on multiple motor representations, eliciting motor-evoked potentials (MEPs) in 9 finger and leg muscles. MEP amplitudes allowed us to probe activity changes in the corresponding finger and leg representations, while participants were deliberating about which index to choose. Our data indicate that hastiness entails a broad amplification of motor activity, although this amplification was limited to the chosen side. On top of this effect, we identified a local suppression of motor activity, surrounding the chosen index representation. Hence, a decision policy favoring speed over accuracy appears to rely on overlapping processes producing a broad (but not global) amplification and a surround suppression of motor activity. The latter effect may help to increase the signal-to-noise ratio of the chosen representation, as supported by single-trial correlation analyses indicating a stronger differentiation of activity changes in finger representations in the hasty context.

Connecting the dots: harnessing dual-site transcranial magnetic stimulation to quantify the causal influence of medial frontal areas on the motor cortex.

Dual-site transcranial magnetic stimulation has been widely employed to investigate the influence of cortical structures on the primary motor cortex. Here, we leveraged this technique to probe the causal influence of two key areas of the medial frontal cortex, namely the supplementary motor area and the medial orbitofrontal cortex, on primary motor cortex. We show that supplementary motor area stimulation facilitates primary motor cortex activity across short (6 and 8 ms) and long (12 ms) inter-stimulation intervals, putatively recruiting cortico-cortical and cortico-subcortico-cortical circuits, respectively. Crucially, magnetic resonance imaging revealed that this facilitatory effect depended on a key morphometric feature of supplementary motor area: individuals with larger supplementary motor area volumes exhibited more facilitation from supplementary motor area to primary motor cortex for both short and long inter-stimulation intervals. Notably, we also provide evidence that the facilitatory effect of supplementary motor area stimulation at short intervals is unlikely to arise from spinal interactions of volleys descending simultaneously from supplementary motor area and primary motor cortex. On the other hand, medial orbitofrontal cortex stimulation moderately suppressed primary motor cortex activity at both short and long intervals, irrespective of medial orbitofrontal cortex volume. These results suggest that dual-site transcranial magnetic stimulation is a fruitful approach to investigate the differential influence of supplementary motor area and medial orbitofrontal cortex on primary motor cortex activity, paving the way for the multimodal assessment of these fronto-motor circuits in health and disease.

Inhalation boosts perceptual awareness and decision speed.

The emergence of consciousness is one of biology's biggest mysteries. During the past two decades, a major effort has been made to identify the neural correlates of consciousness, but in comparison, little is known about the physiological mechanisms underlying first-person subjective experience. Attention is considered the gateway of information to consciousness. Recent work suggests that the breathing phase (i.e., inhalation vs. exhalation) modulates attention, in such a way that attention directed toward exteroceptive information would increase during inhalation. One key hypothesis emerging from this work is that inhalation would improve perceptual awareness and near-threshold decision-making. The present study directly tested this hypothesis. We recorded the breathing rhythms of 30 humans performing a near-threshold decision-making task, in which they had to decide whether a liminal Gabor was tilted to the right or the left (objective decision task) and then to rate their perceptual awareness of the Gabor orientation (subjective decision task). In line with our hypothesis, the data revealed that, relative to exhalation, inhalation improves perceptual awareness and speeds up objective decision-making, without impairing accuracy. Overall, the present study builds on timely questions regarding the physiological mechanisms underlying consciousness and shows that breathing shapes the emergence of subjective experience and decision-making.NEW & NOTEWORTHY Breathing is a ubiquitous biological rhythm in animal life. However, little is known about its effect on consciousness and decision-making. Here, we measured the respiratory rhythm of humans performing a near-threshold discrimination experiment. We show that inhalation, compared with exhalation, improves perceptual awareness and accelerates decision-making while leaving accuracy unaffected.

Corticospinal Suppression Underlying Intact Movement Preparation Fades in Parkinson's Disease.

BACKGROUND: In Parkinson's disease (PD), neurophysiological abnormalities within the primary motor cortex (M1) have been shown to contribute to bradykinesia, but exact modalities are still uncertain. We propose that such motor slowness could involve alterations in mechanisms underlying movement preparation, especially the suppression of corticospinal excitability-called "preparatory suppression"-which is considered to propel movement execution by increasing motor neural gain in healthy individuals. METHODS: On two consecutive days, 29 PD patients (on and off medication) and 29 matched healthy controls (HCs) underwent transcranial magnetic stimulation over M1, eliciting motor-evoked potentials (MEPs) in targeted hand muscles, while they were either at rest or preparing a left- or right-hand response in an instructed-delay choice reaction time task. Preparatory suppression was assessed by expressing MEP amplitudes during movement preparation relative to rest. RESULTS: Contrary to HCs, PD patients showed a lack of preparatory suppression when the side of the responding hand was analyzed, especially when the latter was the most affected one. This deficit, which did not depend on dopamine medication, increased with disease duration and also tended to correlate with motor impairment, as measured by the Movement Disorder Society Unified Parkinson's Disease Rating Scale, Part III (both total and bradykinesia scores). CONCLUSIONS: Our novel findings indicate that preparatory suppression fades in PD, in parallel with worsening motor symptoms, including bradykinesia. Such results suggest that an alteration in this marker of intact movement preparation could indeed cause motor slowness and support its use in future studies on the relation between M1 alterations and motor impairment in PD. © 2022 International Parkinson and Movement Disorder Society.

Trading accuracy for speed over the course of a decision.

Humans and other animals often need to balance the desire to gather sensory information (to make the best choice) with the urgency to act, facing a speed-accuracy tradeoff (SAT). Given the ubiquity of SAT across species, extensive research has been devoted to understanding the computational mechanisms allowing its regulation at different timescales, including from one context to another, and from one decision to another. However, animals must frequently change their SAT on even shorter timescales-that is, over the course of an ongoing decision-and little is known about the mechanisms that allow such rapid adaptations. The present study aimed at addressing this issue. Human subjects performed a decision task with changing evidence. In this task, subjects received rewards for correct answers but incurred penalties for mistakes. An increase or a decrease in penalty occurring halfway through the trial promoted rapid SAT shifts, favoring speeded decisions either in the early or in the late stage of the trial. Importantly, these shifts were associated with stage-specific adjustments in the accuracy criterion exploited for committing to a choice. Those subjects who decreased the most their accuracy criterion at a given decision stage exhibited the highest gain in speed, but also the highest cost in terms of performance accuracy at that time. Altogether, the current findings offer a unique extension of previous work, by suggesting that dynamic cha*nges in accuracy criterion allow the regulation of the SAT within the timescale of a single decision.NEW & NOTEWORTHY Extensive research has been devoted to understanding the mechanisms allowing the regulation of the speed-accuracy tradeoff (SAT) from one context to another and from one decision to another. Here, we show that humans can voluntarily change their SAT on even shorter timescales-that is, over the course of a decision. These rapid SAT shifts are associated with dynamic adjustments in the accuracy criterion exploited for committing to a choice.

Advanced TMS approaches to probe corticospinal excitability during action preparation.

The motor system displays strong changes in neural activity during action preparation. In the past decades, several techniques, including transcranial magnetic stimulation (TMS), electroencephalography (EEG) and functional magnetic resonance imaging (fMRI), have allowed us to gain insights into the functional role of such preparatory activity in humans. More recently, new TMS tools have been proposed to study the mechanistic principles underlying the changes in corticospinal excitability during action preparation. The aim of the present review is to provide a comprehensive description of these advanced methods and to discuss the new knowledge they give access to, relative to other existing approaches. We start with a brief synthesis of the work that has been achieved so far using classic TMS protocols during action preparation, such as the so-called single-pulse and paired-pulse techniques. We then highlight three new approaches that recently arose in the field of action preparation, including (1) the exploitation of TMS current direction, known as directional TMS, which enables investigating different subsets of neurons in the primary motor cortex, (2) the use of paired-pulse TMS to study the suppressive influence of the cerebellum on corticospinal excitability and (3) the development of a double-coil TMS approach, which facilitates the study of bilateral changes in corticospinal excitability. The aim of the present article is twofold: we seek to provide a comprehensive description of these advanced TMS tools and to discuss their bearings for the field of action preparation with respect to more traditional TMS approaches, as well as to neuroimaging techniques such as EEG or fMRI. Finally, we point out perspectives for fundamental and clinical research that arise from the combination of these methods, widening the horizon of possibilities for the investigation of the human motor system, both in health and disease.

Motor training strengthens corticospinal suppression during movement preparation.

Training can improve motor skills and modify neural activity at rest and during movement execution. Learning-related modulations may also concern motor preparation but the neural correlates and the potential behavioral relevance of such adjustments remain unclear. In humans, preparatory processes have been largely investigated using transcranial magnetic stimulation (TMS) with several studies reporting decreased corticospinal excitability (CSE) relative to a baseline measure at rest; a phenomenon called preparatory suppression. Here, we investigated the effect of motor training on such preparatory suppression, in relation to resting CSE, in humans. We trained participants to initiate quick movements in an instructed-delay reaction time (RT) task and used TMS to investigate changes in CSE over the practice blocks. Training on the task speeded up RTs, with no repercussion on error rates. Training also increased resting CSE. Most interestingly, we found that CSE during action preparation did not mirror the training-related increase observed at rest. Rather, compared with the rising baseline, the degree of preparatory suppression strengthened with practice. This training-related change in preparatory suppression (but not the changes in baseline CSE) predicted RT gains: the subjects showing a greater strengthening of preparatory suppression were also those exhibiting larger gains in RTs. Finally, such a relationship between RTs and preparatory suppression was also evident at the single-trial level, though only in the nonselected effector: RTs were generally faster in trials where preparatory suppression was deeper. These findings suggest that training induces changes in motor preparatory processes that are linked to an enhanced ability to initiate fast movements.NEW & NOTEWORTHY Movement preparation involves a broad suppression in the excitability of the corticospinal pathway, a phenomenon called preparatory suppression. Here, we show that motor training strengthens preparatory suppression and that this strengthening is associated with faster reaction times. Our findings highlight a key role of preparatory suppression in training-driven behavioral improvements.

Visuomotor Correlates of Conflict Expectation in the Context of Motor Decisions.

Many behaviors require choosing between conflicting options competing against each other in visuomotor areas. Such choices can benefit from top-down control processes engaging frontal areas in advance of conflict when it is anticipated. Yet, very little is known about how this proactive control system shapes the visuomotor competition. Here, we used electroencephalography in human subjects (male and female) to identify the visual and motor correlates of conflict expectation in a version of the Eriksen Flanker task that required left or right responses according to the direction of a central target arrow surrounded by congruent or incongruent (conflicting) flankers. Visual conflict was either highly expected (it occurred in 80% of trials; mostly incongruent blocks) or very unlikely (20% of trials; mostly congruent blocks). We evaluated selective attention in the visual cortex by recording target- and flanker-related steady-state visual-evoked potentials (SSVEPs) and probed action selection by measuring response-locked potentials (RLPs) in the motor cortex. Conflict expectation enhanced accuracy in incongruent trials, but this improvement occurred at the cost of speed in congruent trials. Intriguingly, this behavioral adjustment occurred while visuomotor activity was less finely tuned: target-related SSVEPs were smaller while flanker-related SSVEPs were higher in mostly incongruent blocks than in mostly congruent blocks, and incongruent trials were associated with larger RLPs in the ipsilateral (nonselected) motor cortex. Hence, our data suggest that conflict expectation recruits control processes that augment the tolerance for inappropriate visuomotor activations (rather than processes that downregulate their amplitude), allowing for overflow activity to occur without having it turn into the selection of an incorrect response.SIGNIFICANCE STATEMENT Motor choices made in front of discordant visual information are more accurate when conflict can be anticipated, probably due to the engagement of top-down control from frontal areas. How this control system modulates activity within visual and motor areas is unknown. Here, we show that, when control processes are recruited in anticipation of conflict, as evidenced by higher midfrontal theta activity, visuomotor activity is less finely tuned: visual processing of the goal-relevant location was reduced and the motor cortex displayed more inappropriate activations, compared with when conflict was unlikely. We argue that conflict expectation is associated with an expansion of the distance-to-selection threshold, improving accuracy while the need for online control of visuomotor activity is reduced.

Implicit visual cues tune oscillatory motor activity during decision-making.

Motor decisions entails a buildup of choice-selective activity in the motor cortex. The rate of this buildup crucially depends on the amount of evidence favoring the selection of each action choice in the visual environment. Though numerous studies have characterized how sensory evidence drives motor activity when processed consciously, very little is known about the neural mechanisms that underlie the integration of implicit sources of information. Here, we used electroencephalography to investigate the impact of implicit visual cues on response-locked potentials and oscillatory activity in the motor cortex during decision-making. Subjects were required to select between left and right index finger responses according to the motion direction of a cloud of dots presented in one of three possible colors. Unbeknown to the participants, the color cue could bring evidence either in favor of or against the selection of the correct response. Implicit color cues tuned choice-selective oscillatory activity in the low beta range (16-25 Hz), boosting the buildup of contralateral activity when evidence favored the selection of the correct action, while weakening it when evidence biased against the correct response. This modulation of oscillatory activity influenced the speed at which the correct action was eventually chosen. Implicit cues also altered oscillatory activity in a non-selective way in the low frequency oscillation (1-7 Hz) and high beta ranges (25-35 Hz), impacting both contralateral and ipsilateral activity. The current findings yield a critical extension of prior observations by indicating that the integration of both explicit and implicit sources of evidence tunes oscillatory motor activity during decision-making.

Motor cortex disruption delays motor processes but not deliberation about action choices.

Decisions about actions typically involve a period of deliberation that ends with the commitment to a choice and the motor processes overtly expressing that choice. Previous studies have shown that neural activity in sensorimotor areas, including the primary motor cortex (M1), correlates with deliberation features during action selection. However, the causal contribution of these areas to the decision process remains unclear. Here, we investigated whether M1 determines choice commitment or whether it simply reflects decision signals coming from upstream structures and instead mainly contributes to the motor processes that follow commitment. To do so, we tested the impact of a disruption of M1 activity, induced by continuous theta burst stimulation (cTBS), on the behavior of human subjects in 1) a simple reaction time (SRT) task allowing us to estimate the duration of the motor processes and 2) a modified version of the tokens task (Cisek P, Puskas GA, El-Murr S. J Neurosci 29: 11560-11571, 2009), which allowed us to estimate subjects' time of commitment as well as accuracy criterion. The efficiency of cTBS was attested by a reduction in motor evoked potential amplitudes following M1 disruption compared with those following a sham stimulation. Furthermore, M1 cTBS lengthened SRTs, indicating that motor processes were perturbed by the intervention. Importantly, all of the behavioral results in the tokens task were similar following M1 disruption and sham stimulation, suggesting that the contribution of M1 to the deliberation process is potentially negligible. Taken together, these findings favor the view that M1 contribution is downstream of the decision process.NEW & NOTEWORTHY Decisions between actions are ubiquitous in the animal realm. Deliberation during action choices entails changes in the activity of the sensorimotor areas controlling those actions, but the causal role of these areas is still often debated. With the use of continuous theta burst stimulation, we show that disrupting the primary motor cortex (M1) delays the motor processes that follow instructed commitment but does not alter volitional deliberation, suggesting that M1 contribution may be downstream of the decision process.

Learning stage-dependent effect of M1 disruption on value-based motor decisions.

The present study aimed at characterizing the impact of M1 disruption on the implementation of implicit value information in motor decisions, at both early stages (during reinforcement learning) and late stages (after consolidation) of action value encoding. Fifty subjects performed, over three consecutive days, a task that required them to select between two finger responses according to the color (instruction) and to the shape (implicit, undisclosed rule) of an imperative signal: considering the implicit rule in addition to the instruction allowed subjects to earn more money. We investigated the functional contribution of M1 to the implementation of the implicit rule in subjects' motor decisions. Continuous theta burst stimulation (cTBS) was applied over M1 either on Day 1 or on Day 3, producing a temporary lesion either during reinforcement learning (cTBSLearning group) or after consolidation of the implicit rule, during decision-making (cTBSDecision group), respectively. Interestingly, disrupting M1 activity on Day 1 improved the reliance on the implicit rule, plausibly because M1 cTBS increased dopamine release in the putamen in an indirect way. This finding corroborates the view that cTBS may affect activity in unstimulated areas, such as the basal ganglia. Notably, this effect was short-lasting; it did not persist overnight, suggesting that the functional integrity of M1 during learning is a prerequisite for the consolidation of implicit value information to occur. Besides, cTBS over M1 did not impact the use of the implicit rule when applied on Day 3, although it did so when applied on Day 2 in a recent study where the reliance on the implicit rule declined following cTBS (Derosiere et al., 2017). Overall, these findings indicate that the human M1 is functionally involved in the consolidation and implementation of implicit value information underlying motor decisions. However, M1 contribution seems to vanish as subjects become more experienced in using the implicit value information to make their motor decisions.

Primary motor cortex contributes to the implementation of implicit value-based rules during motor decisions.

In the present study, we investigated the functional contribution of the human primary motor cortex (M1) to motor decisions. Continuous theta burst stimulation (cTBS) was used to alter M1 activity while participants performed a decision-making task in which the reward associated with the subjects' responses (right hand finger movements) depended on explicit and implicit value-based rules. Subjects performed the task over two consecutive days and cTBS occurred in the middle of Day 2, once the subjects were just about to implement implicit rules, in addition to the explicit instructions, to choose their responses, as evident in the control group (cTBS over the right somatosensory cortex). Interestingly, cTBS over the left M1 prevented subjects from implementing the implicit value-based rule while its implementation was enhanced in the group receiving cTBS over the right M1. Hence, cTBS had opposite effects depending on whether it was applied on the contralateral or ipsilateral M1. The use of the explicit value-based rule was unaffected by cTBS in the three groups of subject. Overall, the present study provides evidence for a functional contribution of M1 to the implementation of freshly acquired implicit rules, possibly through its involvement in a cortico-subcortical network controlling value-based motor decisions.

Adaptations of motor neural structures' activity to lapses in attention.

Sustained attention is fundamental for cognition and when impaired, impacts negatively on important contemporary living skills. Degradation in sustained attention is characterized by the time-on-task (TOT) effect, which manifests as a gradual increase in reaction time (RT). The TOT effect is accompanied by changes in relative brain activity patterns in attention-related areas, most noticeably in the prefrontal cortex (PFC) and the right parietal areas. However, activity changes in task-relevant motor structures have not been confirmed to date. This article describes an investigation of such motor-related activity changes as measured with 1) the time course of corticospinal excitability (CSE) through single-pulse transcranial magnetic stimulation; and 2) the changes in activity of premotor (PMC), primary motor (M1), PFC, and right parietal areas by means of near-infrared spectroscopy, during a sustained attention RT task exhibiting the TOT effect. Our results corroborate established findings such as a significant increase (P < 0.05) in lateral prefrontal and right parietal areas activity after the emergence of the TOT effect but also reveal adaptations in the form of motor activity changes--in particular, a significant increase in CSE (P < 0.01) and in primary motor area (M1) activity (P < 0.05).

Expectations induced by natural-like temporal fluctuations are independent of attention decrement: evidence from behavior and early visual evoked potentials.

Temporal expectations and attention decrement affect human behavior in opposing ways: the former positively, the latter negatively yet both exhibit similar neural signatures - i.e., reduction in the early event-related potential components' amplitude - despite different underlying mechanisms. Furthermore, there is a significant and growing debate in the literature regarding the putative role of attention in the encoding of expectations in perception. The question then arises as to what are the behavioral and neural consequences, if any, of attention decrement on temporal expectations and related enhancement of sensory information processing. Here, we investigated behavioral performance and visual N1a, N1p and P1 components during a sustained attention reaction time task inducing attention decrement under two conditions. In one condition, the inter-stimulus intervals (ISIs) were randomly distributed to impede expectation effects while for the other, the ISI exhibited natural-like long-term correlations supposed to induce temporal expectations. Behavioral results show that natural-like fluctuations in ISI indeed induced faster RT due to temporal expectations. These temporal expectations were beneficial even under attention decrement circumstances. Further, temporal expectations were associated with reduced N1a amplitude while attention decrement was associated with reduced N1p amplitude. Our findings provide evidence that the effects of temporal expectations and attention decrement induced in a single task can be independent at the behavioral level, and are supported at separate information processing stages at the neural level in vision.

Accelerometry as a tool for measuring the effects of transcranial magnetic stimulation.

OBJECTIVE: We predicted that accelerometry would be a viable alternative to electromyography (EMG) for assessing fundamental Transcranial Magnetic Stimulation (TMS) measurements (e.g. Resting Motor Threshold (RMT), recruitment curves, latencies). NEW METHOD: 21 participants were tested. TMS evoked responses were recorded with EMG on the First Dorsal Interosseus muscle and an accelerometer on the index fingertip. TMS was used to determine the (EMG-defined) RMT, then delivered at a range of intensities allowing determination of both the accelerometry-defined RMT and measurement of recruitment curves. RESULTS: RMT assessed by EMG was significantly lower than for accelerometry (t(19)=-3.84, p<.001, mean±SD EMG = 41.1±5.28% MSO (maximum stimulator output), Jerk = 44.55±5.82% MSO), though RMTs calculated for each technique were highly correlated (r(18)=.72, p<.001). EMG/Accelerometery recruitment curves were strongly correlated (r(14)=.98, p<.001), and Bayesian model comparison indicated they were equivalent (BF01>9). Latencies measured with EMG were lower and more consistent than those identified using accelerometry (χ2(1)=80.38, p<.001, mean±SD EMG=27.01±4.58 ms, Jerk=48.4±15.33 ms). COMPARISON WITH EXISTING METHODS: EMG is used as standard by research groups that study motor control and neurophysiology, but accelerometry has not yet been considered as a potential tool to assess measurements such as the overall magnitude and latency of the evoked response. CONCLUSIONS: While EMG provides more sensitive and reliable measurements of RMT and latency, accelerometry provides a reliable alternative to measure of the overall magnitude of TMS evoked responses.

Non-invasive stimulation of the human striatum disrupts reinforcement learning of motor skills.

Reinforcement feedback can improve motor learning, but the underlying brain mechanisms remain underexplored. In particular, the causal contribution of specific patterns of oscillatory activity within the human striatum is unknown. To address this question, we exploited a recently developed non-invasive deep brain stimulation technique called transcranial temporal interference stimulation (tTIS) during reinforcement motor learning with concurrent neuroimaging, in a randomized, sham-controlled, double-blind study. Striatal tTIS applied at 80 Hz, but not at 20 Hz, abolished the benefits of reinforcement on motor learning. This effect was related to a selective modulation of neural activity within the striatum. Moreover, 80 Hz, but not 20 Hz, tTIS increased the neuromodulatory influence of the striatum on frontal areas involved in reinforcement motor learning. These results show that tTIS can non-invasively and selectively modulate a striatal mechanism involved in reinforcement learning, expanding our tools for the study of causal relationships between deep brain structures and human behaviour.

Post-error Slowing Reflects the Joint Impact of Adaptive and Maladaptive Processes During Decision Making.

Errors and their consequences are typically studied by investigating changes in decision speed and accuracy in trials that follow an error, commonly referred to as "post-error adjustments". Many studies have reported that subjects slow down following an error, a phenomenon called "post-error slowing" (PES). However, the functional significance of PES is still a matter of debate as it is not always adaptive. That is, it is not always associated with a gain in performance and can even occur with a decline in accuracy. Here, we hypothesized that the nature of PES is influenced by one's speed-accuracy tradeoff policy, which determines the overall level of choice accuracy in the task at hand. To test this hypothesis, we had subjects performing a task in two distinct contexts (separate days), which either promoted speed (hasty context) or cautiousness (cautious context), allowing us to consider post-error adjustments according to whether subjects performed choices with a low or high accuracy level, respectively. Accordingly, our data indicate that post-error adjustments varied according to the context in which subjects performed the task, with PES being solely significant in the hasty context (low accuracy). In addition, we only observed a gain in performance after errors in a specific trial type, suggesting that post-error adjustments depend on a complex combination of processes that affect the speed of ensuing actions as well as the degree to which such PES comes with a gain in performance.