Thomas Michelet

Response Competition in the Primary Motor Cortex: Corticospinal Excitability Reflects Response Replacement During Simple Decisions

It has been suggested that, during decisions about actions, multiple options are initially specified in parallel and then gradually eliminated in a competition for overt execution. To further test this hypothesis, we studied the modulation of human corticospinal excitability during the reaction time of the Eriksen flanker task. In the task, subjects responded with finger flexion or extension to a central arrow while ignoring congruent or incongruent flanker arrows. Single-pulse transcranial magnetic stimulation (TMS) was applied over primary motor cortex (M1) at one of five different latencies after stimulus onset, and motor-evoked potentials (MEPs) were measured in the contralateral index finger. During the control (no flankers) and congruent conditions, MEP size in the agonist increased gradually over the course of reaction time, indicating an increase in corticospinal excitability. Conversely, when the same muscle acted as an antagonist, MEP size decreased, suggesting inhibition. Critically, in the incongruent condition, MEPs briefly increased in the muscle corresponding to an initial default response to the flanker arrows and were later replaced by MEPs corresponding to the correct response to the central arrow. Finally, we found that the gradually growing MEPs for the three conditions reached a constant maximum level just before movement initiation. We propose that this dynamic modulation in corticospinal excitability reflects the competition process, leading to the selection of one response and the rejection of the other. Our results suggest that response competition influences activity in primary motor cortex and that its timing directly influences motor output latency.

Disruption of the proprioceptive mapping in the medial wall of parkinsonian monkeys

Parkinsonian patients present an impairment of proprioceptor‐guided movement that could imply abnormal processing in the frontal mesial cortex. To test this hypothesis, we compared neuronal response to joint displacement in the supplementary and presupplementary motor areas of two monkeys, before and after the progressive establishment of an 1‐methyl‐4‐phenyl‐1,2,3,6‐tetrahydropyridine (MPTP)–induced parkinsonian syndrome. After MPTP administration, neurons were activated by the passive movement of numerous joints in various directions and no longer simply by one or two joints in one direction. This impairment of the focused selection of proprioceptive inputs, imputable to dopamine depletion, could impede motor planning and thus contribute to akinesia.

Impact of Commitment on Performance Evaluation in the Rostral Cingulate Motor Area

Performance evaluation is a prerequisite for behavioral adaptation. Although the anterior cingulate cortex (ACC) is thought to play a central role in error detection, little is known about the electrophysiological activity of this structure during the performance-monitoring process. We directly addressed this issue by training monkeys to perform a Stroop-like task and then recorded neuronal activity in the rostral cingulate motor area (CMAr), a relatively unexplored region of the ACC known to be involved in motor processing. We found that most CMAr neurons responded during the evaluation period to both positive and negative feedback, but neuronal changes were more important after an error than after a successful trial. Interestingly, this performance-monitoring activity was not directly modulated by the degree of difficulty of the cognitive situation because changes in discharge frequency were similar whatever the level of attentional control imposed on the monkey. Firing activity during the evaluation period increased more, however, in erroneously completed than in incompleted trials and when the reward was delivered in an active rather than passive context, indicating that performance evaluation was conditioned by the degree of commitment of the animal to the task. It would thus seem that CMAr neurons could constitute a system for the evaluation of behavioral performance contingent on the subjects commitment to the task.

Electrophysiological Correlates of a Versatile Executive Control System in the Monkey Anterior Cingulate Cortex

When a subject faces conflicting situations, decision-making becomes uncertain. The human dorsal anterior cingulate cortex (dACC) has been repeatedly implicated in the monitoring of such situations, and its neural activity is thought to be involved in behavioral adjustment. However, this hypothesis is mainly based on neuroimaging results and is challenged by animal studies that failed to report any neuronal correlates of conflict monitoring. This discrepancy is thought be due either to methodological or more fundamental cross-species differences. In this study, we eliminated methodological biases and recorded single-neuron activity in monkeys performing a Stroop-like task. We found specific changes in dACC activity during incongruent trials but only in a small subpopulation of cells. Critically, these changes were not related to reaction time and were absent before any incorrect action was taken. A larger fraction of neurons exhibited sustained activity during the whole decision period, whereas another subpopulation of neurons was modulated by reaction time, with a gradual increase in their firing rate that peaked at movement onset. Most of the neurons found in these subpopulations exhibited activity after the delivery of an external negative feedback stimulus that indicated an error had been made. These findings, which are consistent with an executive control role, reconcile various theories of prefrontal cortex function and support the homology between human and monkey cognitive architectures.

Dorsal premotor cortex: neural correlates of reach target decisions based on a color-location matching rule and conflicting sensory evidence

We recorded single-neuron activity in dorsal premotor (PMd) and primary motor cortex (M1) of two monkeys in a reach-target selection task. The monkeys chose between two color-coded potential targets by determining which targets color matched the predominant color of a multicolored checkerboard-like Decision Cue (DC). Different DCs contained differing numbers of colored squares matching each target. The DCs provided evidence about the correct target ranging from unambiguous (one color only) to very ambiguous and conflicting (nearly equal number of squares of each color). Differences in choice behavior (reach response times and success rates as a function of DC ambiguity) of the monkeys suggested that each applied a different strategy for using the target-choice evidence in the DCs. Nevertheless, the appearance of the DCs evoked a transient coactivation of PMd neurons preferring both potential targets in both monkeys. Reach response time depended both on how long it took activity to increase in neurons that preferred the chosen target and on how long it took to suppress the activity of neurons that preferred the rejected target, in both correct-choice and error-choice trials. These results indicate that PMd neurons in this task are not activated exclusively by a signal proportional to the net color bias of the DCs. They are instead initially modulated by the conflicting evidence supporting both response choices; final target selection may result from a competition between representations of the alternative choices. The results also indicate a temporal overlap between action selection and action initiation processes in PMd and M1.

A safety mechanism for observational learning

This empirical article presents the first evidence of a “safety mechanism” based on an observational-learning paradigm. It is accepted that during observational learning, a person can use different strategies to learn a motor skill, but it is unknown whether the learner is able to circumvent the encoding of an uncompleted observed skill. In this study, participants were tested in a dyadic protocol in which an observer watched a participant practicing two different motor sequences during a learning phase. During this phase, one of the two motor sequences was interrupted by a stop signal that precluded motor learning. The results of the subsequent retention test revealed that both groups learned the two motor sequences, but only the physical practice group showed worse performance for the interrupted sequence. The observers were consequently able to use a safety strategy to learn both sequences equally. Our findings are discussed in light of the implications of the action observation network for sequence learning and the cognitive mechanisms of error-based observation.

Checking behavior in rhesus monkeys is related to anxiety and frontal activity

When facing doubt, humans can go back over a performed action in order to optimize subsequent performance. The present study aimed to establish and characterize physiological doubt and checking behavior in non-human primates (NHP). We trained two rhesus monkeys (Macaca mulatta) in a newly designed “Check-or-Go” task that allows the animal to repeatedly check and change the availability of a reward before making the final decision towards obtaining that reward. By manipulating the ambiguity of a visual cue in which the reward status is embedded, we successfully modulated animal certainty and created doubt that led the animals to check. This voluntary checking behavior was further characterized by making EEG recordings and measuring correlated changes in salivary cortisol. Our data show that monkeys have the metacognitive ability to express voluntary checking behavior similar to that observed in humans, which depends on uncertainty monitoring, relates to anxiety and involves brain frontal areas.

Creating semantics in tool use

This article presents the first evidence for a functional link between tool use and the processing of abstract symbols like Arabic numbers. Participants were required to perform a tool-use task after the processing of an Arabic number. These numbers represented either a small (2 or 3) or a large magnitude (8 or 9). The tool-use task consisted in using inverse pliers for gripping either a small or a large object. The inverse pliers enable to dissociate the hand action from the tool action in relation to the object (i.e., closing the hand led to an opening of the tool and vice versa). The number/tool hypothesis predicts that the quantity representation associated with Arabic numbers will interact with the action of the tool toward the object. Conversely, the number/hand hypothesis predicts that the quantity associated with numbers will interact with the action of the hand toward the tool. Results confirmed the first hypothesis and rejected the second. Indeed, large numbers interacted with the action of the tool, such that participants were longer to perform an “opening-hand/closing-tool” action after the processing of large numbers. Moreover, no effect was detected for small numbers, confirming previous studies which used only finger movements. Altogether, our finding suggests that the well-known finger/number interaction can be reversed with tool use.