Publications by authors named "Stefano Ferraina"

42 Publications

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

J Neurosci 2021 09 30;41(36):7591-7606. Epub 2021 Jul 30.

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, 00185, Italy

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. 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.
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http://dx.doi.org/10.1523/JNEUROSCI.0641-20.2021DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8425983PMC
September 2021

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

Cortex 2021 02 19;135:326-340. Epub 2020 Nov 19.

Department of Physiology and Pharmacology, CU027, Sapienza University, Rome, Italy. Electronic address:

Primates adopt various strategies to interact with the environment. Yet, no study has examined the effects of behavioural strategies with regard to how movement inhibition is implemented at the neuronal level. We used a modified version of the stop-task by adding an extra signal - termed the Ignore signal - capable of influencing the inhibition of movements only within a specific strategy. We simultaneously recorded multisite neuronal activity from the dorsal premotor (PMd) cortex of macaque monkeys during the 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 behavioural strategy is adopted. Moreover, neuronal signatures during the inhibitory process were predictive of how PMd processes inhibitory signals, allowing the classification of the resulting behavioural strategy. Our data further corroborate the PMd as a critical node in movement inhibition.
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http://dx.doi.org/10.1016/j.cortex.2020.09.032DOI Listing
February 2021

Dorsal Premotor Cortex Neurons Signal the Level of Choice Difficulty during Logical Decisions.

Cell Rep 2020 07;32(4):107961

Department of Physiology and Pharmacology, Sapienza University, 00185 Rome, Italy.

Studies on the neuronal correlates of decision making have demonstrated that the continuous flow of sensorial information is integrated by sensorimotor brain areas in order to select one among simultaneously represented targets and potential actions. In contrast, little is known about how these areas integrate memory information to lead to similar decisions. Using serial order learning, we explore how fragments of information, learned and stored independently (e.g., A > B and B > C), are linked in an abstract representation according to their reciprocal relations (such as A > B > C) and how this representation can be accessed and manipulated to make decisions. We show that manipulating information after learning occurs with increased difficulty as logical relationships get closer in the mental map and that the activity of neurons in the dorsal premotor cortex (PMd) encodes the difficulty level during target selection for motor decision making at the single-neuron and population levels.
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http://dx.doi.org/10.1016/j.celrep.2020.107961DOI Listing
July 2020

The small scale functional topology of movement control: Hierarchical organization of local activity anticipates movement generation in the premotor cortex of primates.

Neuroimage 2020 02 16;207:116354. Epub 2019 Nov 16.

Department of Physiology and Pharmacology, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185, Rome, Italy. Electronic address:

How neurons coordinate their collective activity for behavioural control is an open question in neuroscience. Several studies have progressively proven, on various scales, that the patterns of neural synchronization change accordingly with behavioural events. However, the topological features of the neural dynamics that underlie task-based cognitive decisions on the small scale level are not understood. We analysed the multiunit activity (MUA) from a multielectrode (96 channels) array of the dorsal premotor cortex (PMd) in rhesus monkeys during a countermanding reaching task. Within the framework of graph theory, we found that in the local PMd network motor execution is preceded by the emergence of hubs of anti-correlation that are organized in a hierarchical manner. Conversely, this organization is absent when monkeys correctly inhibit programmed movements. Thus, we interpret the presence of hubs as reflecting the readiness of the motor plan and the irrevocable signature of the onset of the incoming movement.
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http://dx.doi.org/10.1016/j.neuroimage.2019.116354DOI Listing
February 2020

High Cervical Spinal Cord Stimulation: A One Year Follow-Up Study on Motor and Non-Motor Functions in Parkinson's Disease.

Brain Sci 2019 Apr 3;9(4). Epub 2019 Apr 3.

Department of Biotechnological and Applied Clinical Sciences (DISCAB), University of L'Aquila, 67100 L'Aquila, Italy.

Background: The present study investigated the effectiveness of stimulation applied at cervical levels on pain and Parkinson's disease (PD) symptoms using either tonic or burst stimulation mode.

Methods: Tonic high cervical spinal cord stimulation (T-HCSCS) was applied on six PD patients suffering from low back pain and failed back surgery syndrome, while burst HCSCS (B-HCSCS) was applied in twelve PD patients to treat primarily motor deficits. Stimulation was applied percutaneously with quadripolar or octapolar electrodes. Clinical evaluation was assessed by the Unified Parkinson's Disease Rating Scale (UPDRS) and the Hoehn and Yahr (H&Y) scale. Pain was evaluated by a visual analog scale. Evaluations of gait and of performance in a cognitive motor task were performed in some patients subjected to B-HCSCS. One patient who also suffered from severe autonomic cardiovascular dysfunction was investigated to evaluate the effectiveness of B-HCSCS on autonomic functions.

Results: B-HCSCS was more effective and had more consistent effects than T-HCSCS in reducing pain. In addition, B-HCSCS improved UPDRS scores, including motor sub-items and tremor and H&Y score. Motor benefits appeared quickly after the beginning of B-HCSCS, in contrast to long latency improvements induced by T-HCSCS. A slight decrease of effectiveness was observed 12 months after implantation. B-HCSCS also improved gait and ability of patients to correctly perform a cognitive-motor task requiring inhibition of a prepared movement. Finally, B-HCSCS ameliorated autonomic control in the investigated patient.

Conclusions: The results support a better usefulness of B-HCSCS compared to T-HCSCS in controlling pain and specific aspects of PD motor and non-motor deficits for at least one year.
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http://dx.doi.org/10.3390/brainsci9040078DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6523357PMC
April 2019

The Puzzling Relationship between Attention and Motivation: Do Motor Biases Matter?

Neuroscience 2019 May 12;406:150-158. Epub 2019 Mar 12.

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy. Electronic address:

The relationship between attention and incentive motivation has been mostly examined by administering Posner style cueing tasks in humans and varying monetary stakes. These studies found that higher incentives improved performance independently of spatial attention. However, the ability of the cueing task to measure actual attentional orienting has been debated by several groups that have highlighted the function of the motor system in affecting the behavioral features that are commonly attributed to spatial attention. To determine the impact of motor influences on the interplay between attention and motivation, we administered 2 reaching versions of a cueing task to monkeys in various motor scenarios. In both tasks, a central stimulus indicated the reward stake and predicted the stimulus target location in 80% of trials. In Experiment 1, subjects were requested to report the detection of a target stimulus in each trial. In Experiment 2, the task was modified to fit a paradigm of Go/NoGo target identification. We found that attention and motivation interacted exclusively in Experiment 2, wherein anticipated motor activation was discouraged and more demanding visual processing was imposed. Consequently, we suggest a protocol that provides novel insights into the study of the relationship between spatial attention and motivation and highlights the influence of the arm motor system in the estimation of the deployment of spatial attention.
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http://dx.doi.org/10.1016/j.neuroscience.2019.03.011DOI Listing
May 2019

Visual salience of the stop signal affects the neuronal dynamics of controlled inhibition.

Sci Rep 2018 09 24;8(1):14265. Epub 2018 Sep 24.

Department of Physiology and Pharmacology, Sapienza University, Rome, Italy.

The voluntary control of movement is often tested by using the countermanding, or stop-signal task that sporadically requires the suppression of a movement in response to an incoming stop-signal. Neurophysiological recordings in monkeys engaged in the countermanding task have shown that dorsal premotor cortex (PMd) is implicated in movement control. An open question is whether and how the perceptual demands inherent the stop-signal affects inhibitory performance and their underlying neuronal correlates. To this aim we recorded multi-unit activity (MUA) from the PMd of two male monkeys performing a countermanding task in which the salience of the stop-signals was modulated. Consistently to what has been observed in humans, we found that less salient stimuli worsened the inhibitory performance. At the neuronal level, these behavioral results were subtended by the following modulations: when the stop-signal was not noticeable compared to the salient condition the preparatory neuronal activity in PMd started to be affected later and with a less sharp dynamic. This neuronal pattern is probably the consequence of a less efficient inhibitory command useful to interrupt the neural dynamic that supports movement generation in PMd.
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http://dx.doi.org/10.1038/s41598-018-32669-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6155270PMC
September 2018

Coding of Self and Other's Future Choices in Dorsal Premotor Cortex during Social Interaction.

Cell Rep 2018 08;24(7):1679-1686

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy. Electronic address:

Representing others' intentions is central to primate social life. We explored the role of dorsal premotor cortex (PMd) in discriminating between self and others' behavior while two male rhesus monkeys performed a non-match-to-goal task in a monkey-human paradigm. During each trial, two of four potential targets were randomly presented on the right and left parts of a screen, and the monkey or the human was required to choose the one that did not match the previously chosen target. Each agent had to monitor the other's action in order to select the correct target in that agent's own turn. We report neurons that selectively encoded the future choice of the monkey, the human agent, or both. Our findings suggest that PMd activity shows a high degree of self-other differentiation during face-to-face interactions, leading to an independent representation of what others will do instead of entailing self-centered mental rehearsal or mirror-like activities.
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http://dx.doi.org/10.1016/j.celrep.2018.07.030DOI Listing
August 2018

Persistence of cortical neuronal activity in the dying brain.

Resuscitation 2018 Sep 5;130:e5-e7. Epub 2018 Jul 5.

Department of Physiology and Pharmacology, Sapienza University, 00185, Rome, Italy.

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http://dx.doi.org/10.1016/j.resuscitation.2018.07.001DOI Listing
September 2018

Neural activity in macaque medial frontal cortex represents others' choices.

Sci Rep 2017 10 4;7(1):12663. Epub 2017 Oct 4.

Department of Physiology and Pharmacology, Sapienza - University of Rome, Piazzale Aldo Moro 5, 00185, Rome, Italy.

Predicting the behavior of others is a fundamental skill in primate social life. We tested the role of medial frontal cortex in the prediction of other agents' behavior in two male macaques, using a monkey-human interactive task in which their actor-observer roles were intermixed. In every trial, the observer monitored the actor's choice to reject it for a different one when he became the actor on the subsequent trial. In the delay period preceding the action, we identified neurons modulated by the agent's identity, as well as a group of neurons encoding the agent's future choice, some of which were neurons that showed differential patterns of activity between agents. The ability of these neurons to flexibly move from 'self-oriented' to 'other-oriented' representations could correspond to the "other side of the coin" of the simulative mirroring activity. Neurons that changed coding scheme, together with neurons exclusively involved in the prediction of the other agent's choice, show a neural substrate for predicting or anticipating others' choices beyond simulation.
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http://dx.doi.org/10.1038/s41598-017-12822-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5627293PMC
October 2017

Atrophic degeneration of cerebellum impairs both the reactive and the proactive control of movement in the stop signal paradigm.

Exp Brain Res 2017 10 17;235(10):2971-2981. Epub 2017 Jul 17.

Department of Physiology and Pharmacology, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185, Rome, Italy.

The cognitive control of movement suppression, including performance monitoring, is one of the core properties of the executive system. A complex cortical and subcortical network involving cerebral cortex, thalamus, subthalamus, and basal ganglia has been regarded as the neural substrate of inhibition of programmed movements. Using the countermanding task, a suitable tool to explore behavioral components of movement suppression, the contribution of the cerebellum in the proactive control and monitoring of voluntary action has been recently described in patients affected by focal lesions involving in particular the cerebellar dentate nucleus. Here, we evaluated the performance on the countermanding task in a group of patients with cerebellar degeneration, in which the cerebellar cortex was diffusely affected, and showed that they display additionally a longer latency in countermanding engaged movements. Overall, the present data confirm the role of the cerebellum in executive control of action inhibition by extending the contribution to reactive motor suppression.
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http://dx.doi.org/10.1007/s00221-017-5027-zDOI Listing
October 2017

Visual salience of the stop-signal affects movement suppression process.

Exp Brain Res 2017 07 24;235(7):2203-2214. Epub 2017 Apr 24.

Department of Physiology and Pharmacology, Sapienza University, Rome, Italy.

We investigated how the ability to suppress an impending movement is affected by the visual salience of the stop-signal in a reaching countermanding task. We found that when the stop-signal was easy to detect, stop performance was better than when the stop-signal was difficult to detect. In an exploratory analysis, we also found that the change in salience of the stop-signal can have an effect on the speed of response in trials following the stop-signal. This effect occurred together with strategic slowing down after an error in inhibiting was committed and together with a repetition priming effect due to the stop-signal presented in the previous trial. Our results suggest the need to investigate more in depth the afferent processing stage of the inhibitory control of movement and how task demands can affect its functioning.
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http://dx.doi.org/10.1007/s00221-017-4961-0DOI Listing
July 2017

Evaluation of relational reasoning by a transitive inference task in attention-deficit/hyperactivity disorder.

Neuropsychology 2017 02 21;31(2):200-208. Epub 2016 Nov 21.

Department of Neuroscience, Child Neuropsychiatry Unit, Bambino Gesù Children's Hospital, IRCCS.

Objective: Here we explored whether children with ADHD have a deficit in relational reasoning, a skill subtending the acquisition of many cognitive abilities and social rules.

Method: We analyzed the performance of a group of children with ADHD during a transitive inference task, a task requiring first to learn the reciprocal relationship between adjacent items of a rank ordered series (e.g., A>B; B>C; C>D; D>E; E>F), and second, to deduct the relationship between novel pairs of items never matched during the learning (e.g., B>D; C>E).

Results: As a main result, we observed that children with ADHD were impaired in performing inferential reasoning problems. The deficit in relational reasoning was found to be related to the difficulty in managing a unified representation of ordered items.

Conclusion: The present finding documented a novel deficit in ADHD, contributing to improving the understanding of the disorder. (PsycINFO Database Record
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http://dx.doi.org/10.1037/neu0000332DOI Listing
February 2017

Reaching-related Neurons in Superior Parietal Area 5: Influence of the Target Visibility.

J Cogn Neurosci 2016 Nov 5;28(11):1828-1837. Epub 2016 Jul 5.

Sapienza University, Rome, Italy.

Reaching movements require the integration of both somatic and visual information. These signals can have different relevance, depending on whether reaches are performed toward visual or memorized targets. We tested the hypothesis that under such conditions, therefore depending on target visibility, posterior parietal neurons integrate differently somatic and visual signals. Monkeys were trained to execute both types of reaches from different hand resting positions and in total darkness. Neural activity was recorded in Area 5 (PE) and analyzed by focusing on the preparatory epoch, that is, before movement initiation. Many neurons were influenced by the initial hand position, and most of them were further modulated by the target visibility. For the same starting position, we found a prevalence of neurons with activity that differed depending on whether hand movement was performed toward memorized or visual targets. This result suggests that posterior parietal cortex integrates available signals in a flexible way based on contextual demands.
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http://dx.doi.org/10.1162/jocn_a_01004DOI Listing
November 2016

Modulation of Neural Variability in Premotor, Motor, and Posterior Parietal Cortex during Change of Motor Intention.

J Neurosci 2016 Apr;36(16):4614-23

Department of Physiology and Pharmacology, SAPIENZA University of Rome, Rome 00185, Italy

Unlabelled: The time course of neural variability was studied in three nodes of the parieto-frontal system: the dorsal premotor cortex (PMd, area 6), primary motor cortex (MI, area 4), and posterior parietal cortex (PPC, area 5) while monkeys made either direct reaches to visual targets or changed reach direction in response to an unexpected change of target location. These areas are crucial nodes in the distributed control of reaching and their lesion impairs trajectory formation and correction under different circumstances. During unperturbed reaches, neural variability declined before the onset of hand movement in both frontal and parietal cortex. When the original motor intention suddenly changed, neural variability displayed a complex and area-specific modulation because the perturbation of the motor state was signaled earlier in PMd than in MI and PPC. The comparison of perturbed versus unperturbed reaches revealed that, in the time between the onset of correction signal and trajectory change, identical hand movements were associated with different, therefore context-dependent, patterns of neural variability induced by the instruction to change hand movement direction. In PMd, neural variability was higher before the initiation of hand reach than before its correction, thus providing a neural underpinning to the phenomenon that it takes less time to correct than to initiate hand movement. Furthermore, neural variability was an excellent predictor of slow and fast reach corrections because it was lower during the latter than the former. We conclude that the analysis of neural variability can be an important tool for the study of complex forms of motor cognition.

Significance Statement: No single study has been performed on neural variability during update of motor intention across monkey premotor, motor, and posterior parietal cortex. In perturbed reaches, target location changed unexpectedly during reaction time and the correction of hand trajectory required updating the original motor plan. Comparing unperturbed versus perturbed reaches revealed that neural variability displayed a complex context- and area-dependent pattern of modulation because, before trajectory correction, similar initial hand movements were associated with different patterns of variability depending on the instruction signal, and therefore on the future hand path and final destination. Furthermore, neural variability predicted both slow and fast hand movement corrections, also offering a neural underpinning to the phenomenon that it takes less time to correct than to initiate hand movement.
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http://dx.doi.org/10.1523/JNEUROSCI.3300-15.2016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6601830PMC
April 2016

Neuronal Modulation in the Prefrontal Cortex in a Transitive Inference Task: Evidence of Neuronal Correlates of Mental Schema Management.

J Neurosci 2016 Jan;36(4):1223-36

Department Physiology and Pharmacology, Sapienza University, 00185 Rome, Italy

Unlabelled: When informed that A > B and B > C, humans and other animals can easily conclude that A > C. This remarkable trait of advanced animals, which allows them to manipulate knowledge flexibly to infer logical relations, has only recently garnered interest in mainstream neuroscience. How the brain controls these logical processes remains an unanswered question that has been merely superficially addressed in neuroimaging and lesion studies, which are unable to identify the underlying neuronal computations. We observed that the activation pattern of neurons in the prefrontal cortex (PFC) during pair comparisons in a highly demanding transitive inference task fully supports the behavioral performance of the two monkeys that we tested. Our results indicate that the PFC contributes to the construction and use of a mental schema to represent premises. This evidence provides a novel framework for understanding the function of various areas of brain in logic processes and impairments to them in degenerative, traumatic, and psychiatric pathologies.

Significance Statement: In cognitive neuroscience, it is unknown how information that leads to inferential deductions are encoded and manipulated at the neuronal level. We addressed this question by recording single-unit activity from the dorsolateral prefrontal cortex of monkeys that were performing a transitive inference (TI) task. The TI required one to choose the higher ranked of two items, based on previous, indirect experience. Our results demonstrated that single-neuron activity supports the construction of an abstract, mental schema of ordered items in solving the task and that this representation is independent of the reward value that is experienced for the single items. These findings identify the neural substrates of abstract mental representations that support inferential thinking.
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http://dx.doi.org/10.1523/JNEUROSCI.1473-15.2016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6604826PMC
January 2016

Neural Encoding of Self and Another Agent's Goal in the Primate Prefrontal Cortex: Human-Monkey Interactions.

Cereb Cortex 2016 12 13;26(12):4613-4622. Epub 2015 Oct 13.

Department of Physiology and Pharmacology, SAPIENZA University of Rome, 00185 Rome, Italy

The primate prefrontal cortex represents both past and future goals. To investigate its role in representing the goals of other agents, we designed a nonmatch-to-goal task that involved a human-monkey (H-M) interaction. During each trial, 2 of 4 potential goal objects were presented randomly to the left or right part of a display screen, and the monkey's (or human's) task was to choose the one that did not match the object goal previously chosen. Human and monkey trials were intermixed, and each agent, when acting as observer, was required to monitor the other actor's choice to switch the object goal choice in case it became the actor on the subsequent trial. We found neurons encoding the actor, either the monkey itself or the human, neurons encoding the agent future goal position and neurons encoding the agent previous goal position. In the category of neurons encoding the human future goal, we differentiated between those encoding the future goal of both agents and those encoding only the human agent future goal. While the first one might represent a covert mental simulation in the human trials, the other one could represent a prediction signal of the other's agent choice.
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http://dx.doi.org/10.1093/cercor/bhv224DOI Listing
December 2016

Both the COMT Val158Met single-nucleotide polymorphism and sex-dependent differences influence response inhibition.

Front Behav Neurosci 2015 19;9:127. Epub 2015 May 19.

Department of Physiology and Pharmacology, Sapienza University Rome, Italy.

Reactive and proactive controls of actions are cognitive abilities that allow one to deal with a continuously changing environment by adjusting already programmed actions. They also set forthcoming actions by evaluating the outcome of the previous ones. Earlier studies highlighted sex-related differences in the strategies and in the pattern of brain activation during cognitive tasks involving reactive and proactive control. To further identify sex-dependent characteristics in the cognitive control of actions, in this study, we have assessed whether/how differences in performance are modulated by the COMT Val158Met single-nucleotide polymorphism (SNP), a genetic factor known to influence the functionality of the dopaminergic system-in particular, at the level of the prefrontal cortex. Two groups of male and female participants were sorted according to their genotype (Val/Val, Val/Met, and Met/Met) and tested in a stop signal task, a consolidated tool for measuring executive control in experimental and clinical settings. In each group of participants, we estimated both a measure of the capacity to react to unexpected events and the ability to monitor their performance. The between-group comparison of these measures indicated a poorer ability of male individuals and Val/Val subjects in error-monitoring. These observations suggest that sex differences in inhibitory control could be influenced by the efficiency of COMT and that other sex-specific factors have to be considered. Understanding the inter-group variability of behavioral and physiological correlates of cognitive control could provide more accurate diagnostic tools for predicting the incidence and/or the development of pathologies, like ADHD, or deviant behaviors, such as drug or alcohol abuse.
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http://dx.doi.org/10.3389/fnbeh.2015.00127DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4436879PMC
June 2015

Alpha- and beta-band oscillations subserve different processes in reactive control of limb movements.

Front Behav Neurosci 2014 5;8:383. Epub 2014 Nov 5.

Department Physiology and Pharmacology, Sapienza University of Rome Rome, Italy.

The capacity to rapidly suppress a behavioral act in response to sudden instruction to stop is a key cognitive function. This function, called reactive control, is tested in experimental settings using the stop signal task, which requires subjects to generate a movement in response to a go signal or suppress it when a stop signal appears. The ability to inhibit this movement fluctuates over time: sometimes, subjects can stop their response, and at other times, they can not. To determine the neural basis of this fluctuation, we recorded local field potentials (LFPs) in the alpha (6-12 Hz) and beta (13-35 Hz) bands from the dorsal premotor cortex of two nonhuman primates that were performing the task. The ability to countermand a movement after a stop signal was predicted by the activity of both bands, each purportedly representing a distinct neural process. The beta band represents the level of movement preparation; higher beta power corresponds to a lower level of movement preparation, whereas the alpha band supports a proper phasic, reactive inhibitory response: movements are inhibited when alpha band power increases immediately after a stop signal. Our findings support the function of LFP bands in generating the signatures of various neural computations that are multiplexed in the brain.
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http://dx.doi.org/10.3389/fnbeh.2014.00383DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4220745PMC
November 2014

iTBS-induced LTP-like plasticity parallels oscillatory activity changes in the primary sensory and motor areas of macaque monkeys.

PLoS One 2014 10;9(11):e112504. Epub 2014 Nov 10.

Department Physiology & Pharmacology, Sapienza University Rome, Rome, Italy.

Recently, neuromodulation techniques based on the use of repetitive transcranial magnetic stimulation (rTMS) have been proposed as a non-invasive and efficient method to induce in vivo long-term potentiation (LTP)-like aftereffects. However, the exact impact of rTMS-induced perturbations on the dynamics of neuronal population activity is not well understood. Here, in two monkeys, we examine changes in the oscillatory activity of the sensorimotor cortex following an intermittent theta burst stimulation (iTBS) protocol. We first probed iTBS modulatory effects by testing the iTBS-induced facilitation of somatosensory evoked potentials (SEP). Then, we examined the frequency information of the electrocorticographic signal, obtained using a custom-made miniaturised multi-electrode array for electrocorticography, after real or sham iTBS. We observed that iTBS induced facilitation of SEPs and influenced spectral components of the signal, in both animals. The latter effect was more prominent on the θ band (4-8 Hz) and the high γ band (55-90 Hz), de-potentiated and potentiated respectively. We additionally found that the multi-electrode array uniformity of β (13-26 Hz) and high γ bands were also afflicted by iTBS. Our study suggests that enhanced cortical excitability promoted by iTBS parallels a dynamic reorganisation of the interested neural network. The effect in the γ band suggests a transient local modulation, possibly at the level of synaptic strength in interneurons. The effect in the θ band suggests the disruption of temporal coordination on larger spatial scales.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0112504PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4226540PMC
December 2015

The influence of recent decisions on future goal selection.

Philos Trans R Soc Lond B Biol Sci 2014 Nov;369(1655)

Department of Physiology and Pharmacology, Sapienza University, Rome 00185, Italy.

Recent decisions about actions and goals can have effects on future choices. Several studies have shown an effect of the previous trial history on neural activity in a subsequent trial. Often, but not always, these effects originate from task requirements that make it necessary to maintain access to previous trial information to make future decisions. Maintaining the information about recent decisions and their outcomes can play an important role in both adapting to new contingencies and learning. Previous goal decisions must be distinguished from goals that are currently being planned to avoid perseveration or more general errors. Output monitoring is probably based on this separation of accomplished past goals from pending future goals that are being pursued. Behaviourally, it has been shown that the history context can influence the location, error rate and latency of successive responses. We will review the neurophysiological studies in the literature, including data from our laboratory, which support a role for the frontal lobe in tracking previous goal selections and outputs when new goals need to be accomplished.
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http://dx.doi.org/10.1098/rstb.2013.0477DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4186230PMC
November 2014

The NMDAr antagonist ketamine interferes with manipulation of information for transitive inference reasoning in non-human primates.

J Psychopharmacol 2014 Sep 18;28(9):881-7. Epub 2014 Jun 18.

Department of Physiology and Pharmacology, Sapienza University, Rome, Italy

One of the most remarkable traits of highly encephalized animals is their ability to manipulate knowledge flexibly to infer logical relationships. Operationally, the corresponding cognitive process can be defined as reasoning. One hypothesis is that this process relies on the reverberating activity of glutamate neural circuits, sustained by NMDA receptor (NMDAr) mediated synaptic transmission, in both parietal and prefrontal areas. We trained two macaque monkeys to perform a form of deductive reasoning - the transitive inference task - in which they were required to learn the relationship between six adjacent items in a single session and then deduct the relationship between nonadjacent items that had not been paired in the learning phase. When the animals had learned the sequence, we administered systemically a subanaesthetic dose of ketamine (a NMDAr antagonist) and measured their performance on learned and novel problems. We observed impairments in determining the relationship between novel pairs of items. Our results are consistent with the hypothesis that transitive inference premises are integrated during learning in a unified representation and that reducing NMDAr activity interferes with the use of this mental model, when decisions are required in comparing pairs of items that have not been learned.
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http://dx.doi.org/10.1177/0269881114538543DOI Listing
September 2014

Correction and suppression of reaching movements in the cerebral cortex: physiological and neuropsychological aspects.

Neurosci Biobehav Rev 2014 May 13;42:232-51. Epub 2014 Mar 13.

Cognitive Neuropsychology and Neuroimaging Laboratory, International School for Advanced Studies (SISSA), 34136 Trieste, Italy; Institute of Cognitive Neuroscience, University College London, London, UK.

Modification or suppression of reaches occurs in everyday life. We argue that a common modular architecture, based on similar neural structures and principles of kinematic and kinetic control, is used for both direct reaches and for their on-line corrections. When a reach is corrected, both the pattern of neural activity in parietal, premotor and motor cortex and the muscle synergies associated with the first movement can be smoothly blended or sharply substituted into those associated with the second one. Premotor cortex provides the early signaling for trajectory updating, while parietal and motor cortex provide the fine-grained encoding of hand kinematics necessary to reshape the motor plan. The cortical contribution to the inhibitory control of reaching is supported by the activity of a network of frontal areas. Premotor cortex has been proposed as a key structure for reaching suppression. Consistent with this, lesions in different nodes of this network result in different forms of motor deficits, such as Optic Ataxia in parietal patients, and commission errors in frontal ones.
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http://dx.doi.org/10.1016/j.neubiorev.2014.03.002DOI Listing
May 2014

Cerebellar damage impairs executive control and monitoring of movement generation.

PLoS One 2014 17;9(1):e85997. Epub 2014 Jan 17.

Department of Psychology, Sapienza University, Rome, Italy ; Ataxia Research Lab, IRCCS Santa Lucia Foundation, Rome, Italy.

Executive control of motor responses is a psychological construct of the executive system. Several studies have demonstrated the involvement of the cerebral cortex, basal ganglia, and thalamus in the inhibition of actions and monitoring of performance. The involvement of the cerebellum in cognitive function and its functional interaction with basal ganglia have recently been reported. Based on these findings, we examined the hypothesis of cerebellar involvement in executive control by administering a countermanding task in patients with focal cerebellar damage. The countermanding task requires one to make a movement in response to a 'go' signal and to halt it when a 'stop' signal is presented. The duration of the go process (reaction time; RT), the duration of the stop process (stop signal reaction time; SSRT), and their relationship, expressed by a psychometric function, are recorded as measures of executive control. All patients had longer go process duration in general and in particular, as a proactive control, as demonstrated by the increase in RT after erroneously performed stop trials. Further, they were defective in the slope of the psychometric function indicating a difficulty on triggering the stop process, although the SSRT did not differ from controls. Notably, their performance was worse when lesions affected deep cerebellar nuclei. Our results support the hypothesis that the cerebellum regulates the executive control of voluntary actions. We speculate that its activity is attributed to specific cerebellar influence over the cortico-striatal loop.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0085997PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3895022PMC
September 2014

Shared action spaces: a basis function framework for social re-calibration of sensorimotor representations supporting joint action.

Front Hum Neurosci 2013 26;7:800. Epub 2013 Nov 26.

Institute of Cognitive Sciences and Technologies, National Research Council Rome, Italy.

The article explores the possibilities of formalizing and explaining the mechanisms that support spatial and social perspective alignment sustained over the duration of a social interaction. The basic proposed principle is that in social contexts the mechanisms for sensorimotor transformations and multisensory integration (learn to) incorporate information relative to the other actor(s), similar to the "re-calibration" of visual receptive fields in response to repeated tool use. This process aligns or merges the co-actors' spatial representations and creates a "Shared Action Space" (SAS) supporting key computations of social interactions and joint actions; for example, the remapping between the coordinate systems and frames of reference of the co-actors, including perspective taking, the sensorimotor transformations required for lifting jointly an object, and the predictions of the sensory effects of such joint action. The social re-calibration is proposed to be based on common basis function maps (BFMs) and could constitute an optimal solution to sensorimotor transformation and multisensory integration in joint action or more in general social interaction contexts. However, certain situations such as discrepant postural and viewpoint alignment and associated differences in perspectives between the co-actors could constrain the process quite differently. We discuss how alignment is achieved in the first place, and how it is maintained over time, providing a taxonomy of various forms and mechanisms of space alignment and overlap based, for instance, on automaticity vs. control of the transformations between the two agents. Finally, we discuss the link between low-level mechanisms for the sharing of space and high-level mechanisms for the sharing of cognitive representations.
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http://dx.doi.org/10.3389/fnhum.2013.00800DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3840313PMC
December 2013

Heterogeneous attractor cell assemblies for motor planning in premotor cortex.

J Neurosci 2013 Jul;33(27):11155-68

Department of Technologies and Health, Istituto Superiore di Sanità, 00161 Rome, Italy.

Cognitive functions like motor planning rely on the concerted activity of multiple neuronal assemblies underlying still elusive computational strategies. During reaching tasks, we observed stereotyped sudden transitions (STs) between low and high multiunit activity of monkey dorsal premotor cortex (PMd) predicting forthcoming actions on a single-trial basis. Occurrence of STs was observed even when movement was delayed or successfully canceled after a stop signal, excluding a mere substrate of the motor execution. An attractor model accounts for upward STs and high-frequency modulations of field potentials, indicative of local synaptic reverberation. We found in vivo compelling evidence that motor plans in PMd emerge from the coactivation of such attractor modules, heterogeneous in the strength of local synaptic self-excitation. Modules with strong coupling early reacted with variable times to weak inputs, priming a chain reaction of both upward and downward STs in other modules. Such web of "flip-flops" rapidly converged to a stereotyped distributed representation of the motor program, as prescribed by the long-standing theory of associative networks.
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http://dx.doi.org/10.1523/JNEUROSCI.4664-12.2013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3718385PMC
July 2013

Median nerve stimulation modulates extracellular signals in the primary motor area of a macaque monkey.

Neurosci Lett 2013 Aug 25;550:184-8. Epub 2013 Jun 25.

Department of Physiology and Pharmacology, Sapienza University, 00185 Rome, Italy.

Aiming to better define the functional influence of somatosensory stimuli on the primary motor cortex (M1) of primates, we investigated changes in extracellular neural activity induced by repetitive median nerve stimulation (MNS). We described neural adaptation and signal integration in both the multiunit activity (MUA) and the local field potential (LFP). To identify integration of initial M1 activity in the MNS response, we tested the correlation between peak amplitude responses and band energy preceding the peaks. Most of the sites studied in the M1 resulted responsive to MNS. MUA response peak amplitude decreased significantly in time in all sites during repetitive MNS, LFP response peak amplitude instead resulted more variable. Similarly, correlation analysis with the initial activity revealed a significant influence when tested using MUA peak amplitude modulation and a less significant correlation when tested using LFP peak amplitude. Our findings improve current knowledge on mechanisms underlying early M1 changes consequent to afferent somatosensory stimuli.
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http://dx.doi.org/10.1016/j.neulet.2013.06.024DOI Listing
August 2013

Neural variability in premotor cortex is modulated by trial history and predicts behavioral performance.

Neuron 2013 Apr;78(2):249-55

Laboratory of Synthetic Perceptive, Emotive and Cognitive Systems-SPECS, Center for Autonomous Systems and Neuro-Robotics-N-RAS, Technology Department, Universitat Pompeu Fabra, Roc Boronat 138, 08018 Barcelona, Spain.

In the study of decision making, emphasis is placed on different forms of perceptual integration, while the influence of other factors, such as memory, is ignored. In addition, it is believed that the information underlying decision making is carried in the rate of the neuronal response, while its variability is considered unspecific. Here we studied the influence of recent experience on motor decision making by analyzing the activity of neurons in the dorsal premotor area of two monkeys performing a countermanding arm task. We observe that the across-trial variability of the neural response strongly correlates with trial history-dependent changes in reaction time. Using a theoretical model of decision making, we show that a trial history-monitoring signal can explain the observed behavioral and neural modulation. Our study reveals that, in the neural processes that culminate in motor plan maturation, the evidence provided by perception and memory is reflected in mean rate and variance respectively.
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http://dx.doi.org/10.1016/j.neuron.2013.02.006DOI Listing
April 2013

Macaque monkeys can learn token values from human models through vicarious reward.

PLoS One 2013 27;8(3):e59961. Epub 2013 Mar 27.

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy.

Monkeys can learn the symbolic meaning of tokens, and exchange them to get a reward. Monkeys can also learn the symbolic value of a token by observing conspecifics but it is not clear if they can learn passively by observing other actors, e.g., humans. To answer this question, we tested two monkeys in a token exchange paradigm in three experiments. Monkeys learned token values through observation of human models exchanging them. We used, after a phase of object familiarization, different sets of tokens. One token of each set was rewarded with a bit of apple. Other tokens had zero value (neutral tokens). Each token was presented only in one set. During the observation phase, monkeys watched the human model exchange tokens and watched them consume rewards (vicarious rewards). In the test phase, the monkeys were asked to exchange one of the tokens for food reward. Sets of three tokens were used in the first experiment and sets of two tokens were used in the second and third experiments. The valuable token was presented with different probabilities in the observation phase during the first and second experiments in which the monkeys exchanged the valuable token more frequently than any of the neutral tokens. The third experiments examined the effect of unequal probabilities. Our results support the view that monkeys can learn from non-conspecific actors through vicarious reward, even a symbolic task like the token-exchange task.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0059961PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3609781PMC
September 2013

Gaze orientation interferes with mental numerical representation.

Cogn Process 2012 Nov 1;13(4):375-9. Epub 2012 Aug 1.

Department of Physiology and Pharmacology, Sapienza University, Rome, Italy.

Number comparison tasks are characterized by distance and size effects. The distance effect reveals that the higher the distance is between two numbers, the easier their magnitude comparison is. Accordingly, people are thought to represent numbers on a spatial dimension, the mental number line, on which any given number corresponds to a location on the line. The size effect, instead, states that at any given distance, comparing two small numbers is easier than comparing two large numbers, thus suggesting that larger numbers are more vaguely represented than smaller ones. In the present work we first tested whether the participants were adopting a spatial strategy to solve a very simple numbers comparison task, by assessing the presence of the distance and the magnitude effect. Secondarily, we focused on the influence of gaze position on their performance. The present results provide evidence that gaze direction interferes with number comparisons, worsening the vague representation of larger numbers and further supporting the hypothesis of the overlapping between physical and mental spaces.
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http://dx.doi.org/10.1007/s10339-012-0517-1DOI Listing
November 2012
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