Changing in the hierarchical organization of local information dynamics during motor decision in the premotor cortex of primates

Despite recent works have investigated functional and effective cortical networks in animal models, the dynamical information transfer among functional modules underneath cognitive control is still largely unknown. Here we addressed the issue by using transfer entropy and graph theory methods on neural activities recorded from a multielectrode (96 recording sites) array in the dorsal premotor cortex of rhesus monkeys. We focused our analysis on the decision time of a stop-signal (countermanding) task. When comparing trials with successful inhibition to those with generated movement we found evidence of heterogeneous interacting modules described by 4 main classes, hierarchically organized. Interestingly, the hierarchical organization resulted different in the two type of trials. Our results suggest that motor decisions are based on the local re-organization of the premotor cortical network

Dissociation of Medial Frontal β-Bursts and Executive Control

ABSTRACTThe neural mechanisms of executive and motor control concern both basic researchers and clinicians. In human studies, preparation and cancellation of movements are accompanied by changes in the β-frequency band (15–29 Hz) of EEG. Previous studies with human participants performing stop signal (countermanding) tasks have described reduced frequency of transient β-bursts over sensorimotor cortical areas before movement initiation and increased β-bursting over medial frontal areas with movement cancellation. This modulation has been interpreted as contributing to the trial-by-trial control of behavior. We performed identical analyses of EEG recorded over the frontal lobe of macaque monkeys performing a saccade countermanding task. Whilst, we replicate the occurrence and modulation of β-bursts associated with initiation and cancellation of saccades, we found that β-bursts occur too infrequently to account for the observed stopping behavior. We also found β-bursts were more common after errors, but their incidence was unrelated to response time adaptation. These results demonstrate the homology of this EEG signature between humans and macaques but raise questions about the current interpretation of β-band functional significance.SIGNIFICANCE STATEMENTThe finding of increased β-bursting over medial frontal cortex with movement cancellation in humans is difficult to reconcile with the finding of modulation too late to contribute to movement cancellation in medial frontal cortex of macaque monkeys. To obtain comparable measurement scales, we recorded EEG over medial frontal cortex of macaques performing a stop signal (countermanding) task. We replicated the occurrence and modulation of β-bursts associated with the cancellation of movements, but we found that β-bursts occur too infrequently to account for observed stopping behavior. Unfortunately, this finding raises doubts whether β-bursts can be a causal mechanism of response inhibition, which impacts future applications in devices such as brain-machine interfaces.

Express saccades during a countermanding task

A serendipitous discovery that macaque monkeys produce express saccades under conditions that should discourage them reveals how cognitive control can adapt behavior to maximize reward.

Express saccades during a countermanding task

ABSTRACTExpress saccades are unusually short latency, visually guided saccadic eye movements. They are most commonly observed when the fixation spot disappears at a consistent, short interval before a target spot appears at a repeated location. The saccade countermanding task includes no fixation-target gap, variable target presentation times, and the requirement to withhold saccades on some trials. These testing conditions should discourage production of express saccades. However, two macaque monkeys performing the saccade countermanding task produced consistent, multimodal distributions of saccadic latencies. These distributions consisted of a longer mode extending from 200 ms to as much as 600 ms after target presentation and another consistently less than 100 ms after target presentation. Simulations revealed that by varying express saccade production, monkeys could earn more reward. If express saccades were not rewarded, they were rarely produced. The distinct mechanisms producing express and longer saccade latencies were revealed further by the influence of regularities in the duration of the fixation interval preceding target presentation on saccade latency. Temporal expectancy systematically affected the latencies of regular but not of express saccades. This study highlights that cognitive control can integrate information across trials and strategically elicit intermittent very short latency saccades to acquire more reward.

Corrective response times in a coordinated eye-head-arm countermanding task

Inhibition of motor responses has been described as a race between two competing decision processes of motor initiation and inhibition, which manifest as the reaction time (RT) and the stop signal reaction time (SSRT); in the case where motor initiation wins out over inhibition, an erroneous movement occurs that usually needs to be corrected, leading to corrective response times (CRTs). Here we used a combined eye-head-arm movement countermanding task to investigate the mechanisms governing multiple effector coordination and the timing of corrective responses. We found a high degree of correlation between effector response times for RT, SSRT, and CRT, suggesting that decision processes are strongly dependent across effectors. To gain further insight into the mechanisms underlying CRTs, we tested multiple models to describe the distribution of RTs, SSRTs, and CRTs. The best-ranked model (according to 3 information criteria) extends the LATER race model governing RTs and SSRTs, whereby a second motor initiation process triggers the corrective response (CRT) only after the inhibition process completes in an expedited fashion. Our model suggests that the neural processing underpinning a failed decision has a residual effect on subsequent actions. NEW & NOTEWORTHY Failure to inhibit erroneous movements typically results in corrective movements. For coordinated eye-head-hand movements we show that corrective movements are only initiated after the erroneous movement cancellation signal has reached a decision threshold in an accelerated fashion.

Visual salience of the stop-signal affects neural dynamics of controlled inhibition

The countermanding or stop-signal task is broadly used to evaluate response inhibition: it sporadically requires to inhibit a movement upon an incoming salient stop-signal.To study the neural basis of arm movements inhibition we combined the approach typically employed for the study of perceptual-decision making with the countermanding task, that is broadly used to evaluate response inhibitionTo this aim we modified the salience of the stop-signal and we found that this modulation affected the ability to inhibit in macaque monkeys: coherently to what already observed in humans, we found that less salient stimuli deteriorate inhibitory performance. These behavioural results were subtended by neural modulations representing an inhibitory process that started later in time and showed a less steeper dynamic for stimuli difficult to be processed.This study shows that the neural patterns observed when deciding to stop are broadly similar to the neural patterns observed when deciding to act in the literature; thus it is a first step in investigating the perceptual decision making process involved in movement inhibition.

Microcircuitry of Performance Monitoring

Cortical circuit mechanisms in medial frontal cortex enabling executive control are unknown. Hence, in monkeys performing a saccade countermanding task to earn larger or smaller fluid rewards, we sampled spiking and synaptic activity simultaneously across all layers of the supplementary eye field (SEF), an agranular cortical area contributing to performance monitoring in nonhuman primate and human studies. Laminar-specific synaptic currents with associated spike rate facilitation and suppression represented error production, reward gain or loss feedback, and reward delivery. The latency, polarity and magnitude of current and spike rate modulation were not predicted by the canonical cortical microcircuit. Pronounced synaptic currents in layer 2/3, which are modulated by loss magnitude, will contribute to the error-related negativity (ERN) and feedback-related negativity (FRN). These unprecedented findings reveal critical features of the cortical microcircuitry supporting performance monitoring and demonstrate that SEF can contribute to the error- and feedback-related negativity.

Models of inhibitory control

We survey models of response inhibition having different degrees of mathematical, computational and neurobiological specificity and generality. The independent race model accounts for performance of the stop-signal or countermanding task in terms of a race between GO and STOP processes with stochastic finishing times. This model affords insights into neurophysiological mechanisms that are reviewed by other authors in this volume. The formal link between the abstract GO and STOP processes and instantiating neural processes is articulated through interactive race models consisting of stochastic accumulator GO and STOP units. This class of model provides quantitative accounts of countermanding performance and replicates the dynamics of neural activity producing that performance. The interactive race can be instantiated in a network of biophysically plausible spiking excitatory and inhibitory units. Other models seek to account for interactions between units in frontal cortex, basal ganglia and superior colliculus. The strengths, weaknesses and relationships of the different models will be considered. We will conclude with a brief survey of alternative modelling approaches and a summary of problems to be addressed including accounting for differences across effectors, species, individuals, task conditions and clinical deficits. This article is part of the themed issue ‘Movement suppression: brain mechanisms for stopping and stillness’.