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.

Comparison of Motor Inhibition in Variants of the Instructed-Delay Choice Reaction Time Task.

Using instructed-delay choice reaction time (RT) paradigms, many previous studies have shown that the motor system is transiently inhibited during response preparation: motor-evoked potentials (MEPs) elicited by transcranial magnetic stimulation (TMS) over the primary motor cortex are typically suppressed during the delay period. This effect has been observed in both selected and non-selected effectors, although MEP changes in selected effectors have been more inconsistent across task versions. Here, we compared changes in MEP amplitudes in three different variants of an instructed-delay choice RT task. All variants required participants to choose between left and right index finger movements but the responses were either provided "in the air" (Variant 1), on a regular keyboard (Variant 2), or on a response device designed to control from premature responses (Variant 3). The task variants also differed according to the visual layout (more concrete in Variant 3) and depending on whether participants received a feedback of their performance (absent in Variant 1). Behavior was globally comparable between the three variants of the task although the propensity to respond prematurely was highest in Variant 2 and lowest in Variant 3. MEPs elicited in a non-selected hand were similarly suppressed in the three variants of the task. However, significant differences emerged when considering MEPs elicited in the selected hand: these MEPs were suppressed in Variants 1 and 3 whereas they were often facilitated in Variant 2, especially in the right dominant hand. In conclusion, MEPs elicited in selected muscles seem to be more sensitive to small variations to the task design than those recorded in non-selected effectors, probably because they reflect a complex combination of inhibitory and facilitatory influences on the motor output system. Finally, the use of a standard keyboard seems to be particularly inappropriate because it encourages participants to respond promptly with no means to control for premature responses, probably increasing the relative amount of facilitatory influences at the time motor inhibition is probed.

Comparison of the two cerebral hemispheres in inhibitory processes operative during movement preparation.

Neuroimaging and neuropsychological studies suggest that in right-handed individuals, the left hemisphere plays a dominant role in praxis, relative to the right hemisphere. However hemispheric asymmetries assessed with transcranial magnetic stimulation (TMS) has not shown consistent differences in corticospinal (CS) excitability of the two hemispheres during movements. In the current study, we systematically explored hemispheric asymmetries in inhibitory processes that are manifest during movement preparation and initiation. Single-pulse TMS was applied over the left or right primary motor cortex (M1LEFT and M1RIGHT, respectively) to elicit motor-evoked potentials (MEPs) in the contralateral hand while participants performed a two-choice reaction time task requiring a cued movement of the left or right index finger. In Experiments 1 and 2, TMS probes were obtained during a delay period following the presentation of the preparatory cue that provided partial or full information about the required response. MEPs were suppressed relative to baseline regardless of whether they were elicited in a cued or uncued hand. Importantly, the magnitude of these inhibitory changes in CS excitability was similar when TMS was applied over M1LEFT or M1RIGHT, irrespective of the amount of information carried by the preparatory cue. In Experiment 3, there was no preparatory cue and TMS was applied at various time points after the imperative signal. When CS excitability was probed in the cued effector, MEPs were initially inhibited and then rose across the reaction time interval. This function was similar for M1LEFT and M1RIGHT TMS. When CS excitability was probed in the uncued effector, MEPs remained inhibited throughout the RT interval. However, MEPs in right FDI became more inhibited during selection and initiation of a left hand movement, whereas MEPs in left FDI remained relatively invariant across RT interval for the right hand. In addition to these task-specific effects, there was a global difference in CS excitability across experiments between the two hemispheres. When the intensity of stimulation was set to 115% of the resting threshold, MEPs were larger when the TMS probe was applied over the M1LEFT than over M1RIGHT. In summary, while the latter result suggests that M1LEFT is more excitable than M1RIGHT, the recruitment of preparatory inhibitory mechanisms is similar within the two cerebral hemispheres.

Increased Reliance on Value-based Decision Processes Following Motor Cortex Disruption.

BACKGROUND: During motor decision making, the neural activity in primary motor cortex (M1) encodes dynamically the competition occurring between potential action plans. A common view is that M1 represents the unfolding of the outcome of a decision process taking place upstream. Yet, M1 could also be directly involved in the decision process. OBJECTIVE: Here we tested this hypothesis by assessing the effect of M1 disruption on a motor decision-making task. METHODS: We applied continuous theta burst stimulation (cTBS) to inhibit either left or right M1 in different groups of subjects and included a third control group with no stimulation. Following cTBS, participants performed a task that required them to choose between two finger key-presses with the right hand according to both perceptual and value-based information. Effects were assessed by means of generalized linear mixed models and computational simulations. RESULTS: In all three groups, subjects relied both on perceptual (P < 0.0001) and value-based information (P = 0.003) to reach a decision. Yet, left M1 disruption led to an increased reliance on value-based information (P = 0.03). This result was confirmed by a computational model showing an increased weight of the valued-based process on the right hand finger choices following left M1 cTBS (P < 0.01). CONCLUSION: These results indicate that M1 is involved in motor decision making, possibly by weighting the final integration of multiple sources of evidence driving motor behaviors.

Generic inhibition of the selected movement and constrained inhibition of nonselected movements during response preparation.

Previous studies have identified two inhibitory mechanisms that operate during action selection and preparation. One mechanism, competition resolution, is manifest in the inhibition of the nonselected response and attributed to competition between candidate actions. The second mechanism, impulse control, is manifest in the inhibition of the selected response and is presumably invoked to prevent premature response. To identify constraints on the operation of these two inhibitory mechanisms, we manipulated the effectors used for the response alternatives, measuring changes in corticospinal excitability with motor-evoked potentials to TMS. Inhibition of the selected response (impulse control) was independent of the task context, consistent with a model in which this form of inhibition is automatically triggered as part of response preparation. In contrast, inhibition of the nonselected response (competition resolution) was context-dependent. Inhibition of the nonselected response was observed when the response alternatives involved movements of the upper limbs but was absent when one response alternative involved an upper limb and the other involved a lower limb. Interestingly, competition resolution for pairs of upper limbs did not require homologous effectors, observed when a left index finger response was pitted with either a nonhomologous right index finger movement or a right arm movement. These results argue against models in which competition resolution is viewed as a generic or fully flexible process, as well as models based on strong anatomical constraints. Rather, they are consistent with models in which inhibition for action selection is constrained by the similarity between the potential responses, perhaps reflecting an experience-dependent mechanism sensitive to the past history of competitive interactions.

Top-down suppression of incompatible motor activations during response selection under conflict.

Top-down control is critical to select goal-directed actions in changeable environments, particularly when several options compete for selection. This control system is thought to involve a mechanism that suppresses activation of unwanted response representations. We tested this hypothesis, in humans, by measuring motor-evoked potentials (MEPs) elicited by transcranial magnetic stimulation (TMS) in a left finger muscle during motor preparation in an adapted Eriksen flanker task. Subjects reported, by a left or right button-press, the orientation of a left- or right-facing central arrow, flanked by two distractor arrows on each side. Central and peripheral arrows either pointed in the same (congruent trial) or in the opposite direction (incongruent trial). Top-down control was manipulated by changing the probability of congruent and incongruent trials in a given block. In the "mostly incongruent" (MI) blocks, 80% of trials were incongruent, producing a context in which subjects strongly anticipated that they would have to face conflict. In the "mostly congruent" (MC) blocks, 80% of trials were congruent and thus subjects barely anticipated conflict in that context. Thus, we assume that top-down control was stronger in the MI than in the MC condition. Accordingly, subjects displayed a lower error rate and shorter reaction times for the incongruent trials in the MI context than for similar trials in the MC context. More interestingly, we found that top-down control specifically reduced activation of the incompatible motor representation during response selection under high conflict. That is, when the central arrow specified a right hand response, left (non-selected) MEPs became smaller in the MI than in the MC condition, but only for incongruent trials, and this measure was positively correlated with performance. In contrast, MEPs elicited in the non-selected hand during congruent trials, or during all trials in which the left hand was selected, tended to increase more after the imperative signal in the MI than the MC condition. Another important observation was that, overall, MEPs were already strongly suppressed at the onset of the imperative signal and that this effect was particularly pronounced in the MI context. Hence, suppression of motor excitability seems to be a key component of conflict resolution.

Influence of reward on corticospinal excitability during movement preparation.

Current models of decision making postulate that action selection entails a competition within motor-related areas. According to this view, during action selection, motor activity should integrate cognitive information (e.g., reward) that drives our decisions. We tested this hypothesis in humans by measuring motor-evoked potentials (MEPs) in a left finger muscle during motor preparation in a hand selection task, in which subjects performed left or right key presses according to an imperative signal. This signal was either obvious or ambiguous, but subjects were always asked to react as fast as possible. When the signal was really indistinct, any key press was regarded as correct, so subjects could respond "at random" in those trials. A score based on reaction times was provided after each correct response, and subjects were told they would receive a monetary reward proportional to their final score. Importantly, the scores were either equitable for both hands or favored implicitly left responses (reward(neutral) and reward(biased) blocks, respectively). We found that subjects selected their left hand more often in the reward(biased) than in the reward(neutral) condition, particularly after ambiguous signals. Moreover, left MEPs were larger, as soon as the signal appeared, in the reward(biased) than in the reward(neutral) conditions. During the course of motor preparation, this effect became strongest following ambiguous signals, a condition in which subjects' choices relied strongly on the reward. These results indicate that motor activity is shaped by a cognitive variable that drives our choices, possibly in the context of a competition taking place within motor-related areas.