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1.
Proc Natl Acad Sci U S A ; 121(25): e2405588121, 2024 Jun 18.
Article in English | MEDLINE | ID: mdl-38861607

ABSTRACT

Many animals can extract useful information from the vocalizations of other species. Neuroimaging studies have evidenced areas sensitive to conspecific vocalizations in the cerebral cortex of primates, but how these areas process heterospecific vocalizations remains unclear. Using fMRI-guided electrophysiology, we recorded the spiking activity of individual neurons in the anterior temporal voice patches of two macaques while they listened to complex sounds including vocalizations from several species. In addition to cells selective for conspecific macaque vocalizations, we identified an unsuspected subpopulation of neurons with strong selectivity for human voice, not merely explained by spectral or temporal structure of the sounds. The auditory representational geometry implemented by these neurons was strongly related to that measured in the human voice areas with neuroimaging and only weakly to low-level acoustical structure. These findings provide new insights into the neural mechanisms involved in auditory expertise and the evolution of communication systems in primates.


Subject(s)
Auditory Perception , Magnetic Resonance Imaging , Neurons , Vocalization, Animal , Voice , Animals , Humans , Neurons/physiology , Voice/physiology , Magnetic Resonance Imaging/methods , Vocalization, Animal/physiology , Auditory Perception/physiology , Male , Macaca mulatta , Brain/physiology , Acoustic Stimulation , Brain Mapping/methods
2.
Proc Natl Acad Sci U S A ; 119(28): e2122395119, 2022 07 12.
Article in English | MEDLINE | ID: mdl-35867763

ABSTRACT

To understand the cortical neuronal dynamics behind movement generation and control, most studies have 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 cortex (PMd) of monkeys performing a countermanding reaching task that requires, in a subset of trials, them 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.


Subject(s)
Motor Activity , Motor Cortex , Neurons , Psychomotor Performance , Animals , Macaca mulatta , Motor Activity/physiology , Motor Cortex/cytology , Motor Cortex/physiology , Neurons/physiology , Psychomotor Performance/physiology
3.
J Neurosci ; 41(36): 7591-7606, 2021 09 08.
Article in English | MEDLINE | ID: mdl-34330772

ABSTRACT

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.


Subject(s)
Cognition/physiology , Motivation/physiology , Motor Cortex/physiology , Neural Inhibition/physiology , Neurons/physiology , Psychomotor Performance/physiology , Animals , Behavior, Animal/physiology , Cues , Macaca mulatta , Male , Reaction Time/physiology
4.
Cortex ; 135: 326-340, 2021 02.
Article in English | MEDLINE | ID: mdl-33308980

ABSTRACT

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.


Subject(s)
Motor Cortex , Animals , Macaca mulatta , Movement , Neurons , Psychomotor Performance
5.
Brain Sci ; 9(4)2019 Apr 03.
Article in English | MEDLINE | ID: mdl-30987170

ABSTRACT

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.

6.
Neuroscience ; 406: 150-158, 2019 May 15.
Article in English | MEDLINE | ID: mdl-30876984

ABSTRACT

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.


Subject(s)
Attention/physiology , Motivation/physiology , Orientation, Spatial/physiology , Photic Stimulation/methods , Psychomotor Performance/physiology , Reaction Time/physiology , Animals , Macaca mulatta , Male
7.
Sci Rep ; 8(1): 14265, 2018 09 24.
Article in English | MEDLINE | ID: mdl-30250230

ABSTRACT

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.


Subject(s)
Behavior, Animal/physiology , Motor Cortex/physiology , Neurons/physiology , Psychomotor Performance/physiology , Animals , Fixation, Ocular/physiology , Humans , Macaca mulatta/physiology , Movement/physiology , Neural Inhibition/physiology , Photic Stimulation , Reaction Time
9.
Exp Brain Res ; 235(10): 2971-2981, 2017 10.
Article in English | MEDLINE | ID: mdl-28717819

ABSTRACT

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.


Subject(s)
Executive Function/physiology , Friedreich Ataxia/pathology , Friedreich Ataxia/physiopathology , Inhibition, Psychological , Motor Activity/physiology , Psychomotor Performance/physiology , Spinocerebellar Ataxias/pathology , Spinocerebellar Ataxias/physiopathology , Adult , Atrophy/pathology , Cerebellar Cortex/pathology , Female , Humans , Male , Middle Aged
10.
Exp Brain Res ; 235(7): 2203-2214, 2017 07.
Article in English | MEDLINE | ID: mdl-28439628

ABSTRACT

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.


Subject(s)
Inhibition, Psychological , Movement/physiology , Neural Inhibition/physiology , Psychomotor Performance/physiology , Visual Perception/physiology , Adult , Analysis of Variance , Eye Movements/physiology , Female , Humans , Male , Middle Aged , Photic Stimulation , Reaction Time/physiology
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