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Giarrocco, F.

Publications and source records attributed to Giarrocco, F..

6 recordsLinked to original sources

Embodied reinforcement learning in the primate cortico-basal ganglia system

Learning the value of environmental stimuli from reward experience allows animals to make advantageous choices. Existing biological accounts of reinforcement learning (RL) often assume that this value is represented as a single, motor-system-invariant neural signal. Here we recorded neuronal activity across eight nodes of the macaque cortico-basal ganglia system -- from limbic to neocortical regions -- while monkeys learned stimulus-reward associations using either saccades or reaches as the required motor response. The geometry of population activity revealed largely distinct value-coding dimensions for saccades and reaches, including in limbic regions typically associated with motor-system-invariant value coding. Consequently, value information was substantially reduced when read out across motor systems. These results provide circuit-wide evidence that challenges existing neural implementations of RL. They link biological accounts of value learning to embodied frameworks in cognitive science and artificial intelligence, in which behavior is grounded in an agents physical structure rather than abstracted from it.

neuroscience↗

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

Recent studies have explored functional and effective neural networks in animal models; however, the dynamics of information propagation among functional modules under cognitive control remain largely unknown. Here, we addressed the issue using Transfer Entropy and graph theory methods on mesoscopic neural activities recorded in the dorsal premotor cortex of rhesus monkeys. We focused our study on the decision time of a Stop-signal task, looking for patterns in the network configuration that could influence motor plan maturation when the Stop signal is provided. When comparing trials with successful inhibition to those with generated movement, the nodes of the network resulted organized into four clusters, hierarchically arranged, and distinctly involved in information transfer. Interestingly, the hierarchies and the strength of information transmission between clusters varied throughout the task, distinguishing between generated movements and canceled ones and corresponding to measurable levels of network complexity. Our results suggest a putative mechanism for motor inhibition in premotor cortex: a topological reshuffle of the information exchanged among ensembles of neurons. AUTHOR SUMMARYIn this study, we investigated the dynamics of information transfer among functionally identified neural modules during cognitive motor control. Our focus was on mesoscopic neural activities in the dorsal premotor cortex of rhesus monkeys engaged in a Stop-signal task. Leveraging multivariate Transfer Entropy and graph theory, we uncovered insights on how behavioral control shapes the topology of information transmission in a local brain network. Task phases modulated the strength and hierarchy of information exchange between modules, revealing the nuanced interplay between neural populations during generated and canceled movements. Notably, during successful inhibition, the network displayed a distinctive configuration, unveiling a novel mechanism for motor inhibition in the premotor cortex: a topological reshuffle of information among neuronal ensembles.

neuroscience↗

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

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.

neuroscience↗

Neuronal activity in the premotor cortex of monkeys reflects both cue salience and motivation for action generation and inhibition

Animals adopt different strategies, promoting certain actions and withholding inconvenient ones, to achieve their goals. The motivation to obtain them is the main drive that determines the behavioural performance. While much work has focused on understanding how motor cortices control actions, their role on motivated behaviours remains unclear. We recorded from dorsal premotor cortex (PMd) of monkeys performing a modified version of the stop-signal task, in which the motivation to perform/withhold an action was manipulated by presenting cues that informed on the probability to obtain different amounts of reward in relation to the motor outcome. According to the motivational context, animals performance adapted to maximize reward. Neuronal activity displayed a cue salience related modulation at trial start and, while the behavioural response approached, reflected more the motivation to start/cancel the action. These findings reveal multiple representations of motivation-related signals in PMd, highlighting its involvement in the control of finalized actions.\n\nSIGNIFICATIVE STATEMENTThe motivation to obtain rewards drives how animals act over their environment. To explore the involvement of motor cortices in motivated behaviours, 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 a cue related activity, in the time immediately following its presentation, and a motivation related activity in performing (or cancelling) a motor program, while the behavioural response approached. The encoding of multiple reward-related signals in motor regions, leads to consider an important role of premotor areas in the reward circuitry.

neuroscience↗

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

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 it 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 planned movement before its onset. In the analysis of the neuronal state-space 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 this subspace toward an orthogonal subspace and, furthermore, surpass a threshold associated with 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. Significance StatementA core question in neuroscience is how the brain generates arm movements. Most studies have approached this issue by investigating the neuronal dynamics that accompany movement production, leaving unanswered the question of which aspects of this dynamics are logically necessary to make the movement. Here we explored this topic by characterizing the neuronal correlates of movement decisions between active inhibition and release of movements. We found that active inhibition and stillness require neuronal signals to be confined in a functional sub-space while actions depend on the transit of activities in an orthogonal space. This dynamics is characterized by a threshold mechanism finally allowing the translation of the motor plan into overt action.

neuroscience↗

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.\n\nTo 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 inhibition\n\nTo 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.\n\nThis 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.

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