To understand the cortical neuronal dynamics behind movement generation and control most studies focused on tasks where actions were planned and then executed, using different instances of visuomotor transformations. However, to fully understand the dynamics related to movement control one must also study how movements are actively inhibited. Inhibition, indeed, represents the first level of control both when different alternatives are available and only one solution could be adopted and when is necessary to maintain the current position. We recorded neuronal activity from a multielectrode array in the dorsal premotor (PMd) cortex of monkeys performing a countermanding reaching task that requires, in a subset of trials, to cancel a potentially planned movement before its onset. In the analysis of the neuronal state-spaces of PMd we found a subspace in which activities conveying temporal information were confined during active inhibition and position holding. Movement execution required activities to escape from the plane toward an orthogonal subspace and, furthermore, surpass a threshold associated to the maturation of the motor plan. These results revealed further details in the neuronal dynamics underlying movement control extending the hypothesis that neuronal computation confined in an output-null subspace does not produce movements.

https://biorxiv.org/content/biorxiv/early/2019/09/19/774307.full-text.pdf

Neuronal population dynamics during motor plan cancellation in non-human primates

Reward prospect weighs on motor decision processes, enhancing the selection of appropriate actions and the inhibition of others. While many studies have investigated the neuronal basis of reward representations and of cortical control of actions, the neuronal correlates of the influences of reward prospect on motor decisions are less clear. We recorded from the dorsal premotor cortex (PMd) of 2 male macaque monkeys performing a modified version of the Stop-signal (countermanding) task. This task challenges motor decisions by requiring responding to a frequent Go stimulus, but to suppress this response when a rare Stop signal is presented during the reaction time. We unbalanced the motivation to respond or to suppress the response by presenting a cue informing on three different rewards schedules: in one case, Go trials were rewarded more than Stop trials; in another case, Stop trials were rewarded more than Go trials; in the last case, both types of trials were rewarded equally. Monkeys adopted different strategies according to reward information provided by the cue: the higher the reward for Stop trials, the higher their ability to suppress the response and the slower their response to Go stimuli. PMd neuronal activity evolved in time and correlated with the behavior: PMd signaled first the cue salience, representing the chance to earn the highest reward at stake, then reflected the shaping of the motor choice by the motivation to move or to stop. These findings represent a neuronal correlate of the influence of reward information on motor decision.SIGNIFICANCE STATEMENT The motivation to obtain rewards drives how animals act over their environment. To explore the involvement of motor cortices in motivated behaviors, we recorded high-resolution neuronal activity in the premotor cortex of monkeys performing a task that manipulated the motivation to generate/withhold a movement through different cued reward probabilities. Our results show the presence of neuronal signals dynamically reflecting the salience of the cue, in the time immediately following its presentation, and a motivation-related activity in performing (or cancelling) a motor program, while the behavioral response approached. The encoding of multiple reward-related signals in this region leads to consider an important role of premotor areas in the reward circuitry supporting action.

Neuronal Activity in the Premotor Cortex of Monkeys Reflects Both Cue Salience and Motivation for Action Generation and Inhibition.

Sudden and surprising sensory events trigger neural processes that swiftly adjust behavior. To study the phylogenesis and the mechanism of this phenomenon, we trained two rhesus monkeys to keep a cursor inside a visual target by exerting force on an isometric joystick. We examined the effect of surprising auditory stimuli on exerted force, scalp electroencephalographic (EEG) activity, and local field potentials (LFP) recorded from the dorso-lateral prefrontal cortex. Auditory stimuli elicited (1) a biphasic modulation of isometric force: a transient decrease followed by a corrective tonic increase, and (2) EEG and LFP deflections dominated by two large negative-positive waves (N70 and P130). The EEG potential was maximal at the scalp vertex, in all respects similar to the human ‘vertex potential’. Electrocortical potentials and force were tightly coupled: the P130 amplitude predicted the magnitude of the corrective force increase, particularly in the EEG electrodes contralateral to the limb exerting force, and in the LFP recorded from deep rather than superficial cortical layers, suggesting a direct effect of the vertex potential on the motor output determining the behavior. These results disclose a phylogenetically-preserved cortico-motor mechanism supporting adaptive behavior in response to salient sensory events.

/pdf/a-cortical-mechanism-linking-saliency-detection-and-motor-1yik0j41.pdf

A cortical mechanism linking saliency detection and motor reactivity in rhesus monkeys

A general mathematical description of how the brain sequentially encodes knowledge remains elusive. We propose a linear solution for serial learning tasks, based on the concept of mixed selectivity in high-dimensional neural state spaces. In our framework, neural representations of items in a sequence are projected along a “geometric” mental line learned through classical conditioning. The model successfully solves serial position tasks and explains behaviors observed in humans and animals during transitive inference tasks amidst noisy sensory input and stochastic neural activity. This approach extends to recurrent neural networks performing motor decision tasks, where the same geometric mental line correlates with motor plans and modulates network activity according to the symbolic distance between items. Serial ordering is thus predicted to emerge as a monotonic mapping between sensory input and behavioral output, highlighting a possible pivotal role for motor-related associative cortices in transitive inference tasks. How the brain sequentially encodes knowledge is not fully understood. Here authors propose a geometric framework for the elusive neural principles of serial reasoning and sequence encoding. Neural representations are theorized to align along a learned mental line, solving serial position and transitive inference tasks.

A geometrical solution underlies general neural principle for serial ordering

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 using Transfer Entropy and graph theory methods on neural activities recorded from a multielectrode 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 the local network resulted organized in four classes of modules hierarchically arranged and differently partaking in information transfer. Interestingly, the hierarchical organization of modules changed during the task, being different for generated movements and cancelled ones. Our results suggest that motor decisions are based on a topological re-organization of the premotor functional network.

/pdf/hierarchical-organization-changes-of-local-information-r7brczmnor.pdf

Hierarchical organization changes of local information dynamics during motor decision in the premotor cortex of primates

Primates adopt various strategies to interact with the environment. Yet, no study has examined the effects of behavioral strategies with regard to how movement inhibition is implemented at the neuronal level. We modified a classical approach to study movement control (stop-task) by adding an extra signal – termed the Ignore signal – which influenced movement inhibition only under a specific strategy. We simultaneously recorded multisite neuronal activity from the dorsal premotor (PMd) cortex of macaque monkeys during a task and applied a state-space approach. As a result, we found that movement generation is characterized by neuronal dynamics that evolve between subspaces. When the movement is halted, this evolution is arrested and inverted. Conversely, when the Ignore signal is presented, inversion of the evolution is observed briefly and only when a specific behavioral strategy is adopted. Moreover, neuronal signatures during the inhibitory process were predictive of how PMd processes inhibitory signals, allowing the classification of the resulting behavioral strategy. Our data corroborate the PMd as a critical node in movement inhibition.

/pdf/neuronal-dynamics-of-signal-selective-motor-plan-4djrnmuvyb.pdf

Neuronal dynamics of signal selective motor plan cancellation in the macaque dorsal premotor cortex

Several studies reported similar neural modulations between brain areas of the frontal cortex, such as the dorsolateral prefrontal (DLPFC) and the premotor dorsal (PMd) cortex, in tasks requiring encoding of the abstract rules for selecting the proper action. Here, we compared the DLPFC and PMd neuronal activity of monkeys trained in choosing the highest ranking image of pair (target item), selected from an arbitrarily rank-ordered set (A>B>C>D>E>F) in the context of a transitive inference task. Once acquired by trial-and-error, the ordinal relationship between pairs of adjacent images (i.e. A>B; B>C; C>D; D>E; E>F), monkeys were tested in inferring the ordinal relation between items of the list not paired during learning. During inferential decisions, we observed that the choice accuracy increased and the reaction time decreased as the rank difference between the compared items enhanced. This result is in line with the hypothesis that after learning, the monkeys built an abstract mental representation of the ranked items, where rank comparisons correspond to the item position comparison on this representation. In both brain areas, we observed higher neuronal activity when the target item appeared in a specific location on the screen, with respect to the opposite position and that this difference was particularly enhanced at lower degrees of difficulty. By comparing the time evolution of the activity of the two areas, we revealed that the neural encoding of target item spatial position occurred earlier in DLPFC than in PMd, while in PMd the spatial encoding duration was longer.

/pdf/different-contribution-of-the-monkey-prefrontal-and-premotor-1b5e086eb2.pdf

Different contribution of the monkey prefrontal and premotor dorsal cortex in decision-making supported by inferential reasoning

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Neuronal dynamics of signal selective motor plan cancellation in the macaque dorsal premotor cortex

Different contribution of the monkey prefrontal and premotor dorsal cortex in decision-making supported by inferential reasoning