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The ventral part of lateral prefrontal cortex (VLPF) of the monkey receives strong visual input, mainly from inferotemporal cortex. It has been shown that VLPF neurons can show visual responses during paradigms requiring to associate arbitrary visual cues to behavioral reactions. Further studies showed that there are also VLPF neurons responding to the presentation of specific visual stimuli, such as objects and faces. However, it is largely unknown whether VLPF neurons respond and differentiate between stimuli belonging to different categories, also in absence of a specific requirement to actively categorize or to exploit these stimuli for choosing a given behavior. The first aim of the present study is to evaluate and map the responses of neurons of a large sector of VLPF to a wide set of visual stimuli when monkeys simply observe them. Recent studies showed that visual responses to objects are also present in VLPF neurons coding action execution, when they are the target of the action. Thus, the second aim of the present study is to compare the visual responses of VLPF neurons when the same objects are simply observed or when they become the target of a grasping action. Our results indicate that: (1) part of VLPF visually responsive neurons respond specifically to one stimulus or to a small set of stimuli, but there is no indication of a "passive" categorical coding; (2) VLPF neuronal visual responses to objects are often modulated by the task conditions in which the object is observed, with the strongest response when the object is target of an action. These data indicate that VLPF performs an early passive description of several types of visual stimuli, that can then be used for organizing and planning behavior. This could explain the modulation of visual response both in associative learning and in natural behavior.

Background . Recent evidence suggested that Action Observation Therapy (AOT), based on observation of actions followed by immediate reproduction, could be a useful rehabilitative strategy for promoting functional recovery of children affected by unilateral cerebral palsy (UCP). AOT most likely exploits properties of the parieto-premotor mirror neuron system (MNS). This is more intensely activated when participants observe actions belonging to their own motor repertoire. Objective . The aim of the present study was to investigate the issue of whether MNS of UCP children is better activated by actions performed by a paretic hand rather than a healthy one. Methods . Using functional magnetic resonance imaging, we assessed brain activation in a homogeneous group of 10 right UCP children compared with that of 10 right-handed typically developing (TD) children, during observation of grasping actions performed by a healthy or a paretic hand. Results . The results revealed a significant activation within the MNS in both UCP and TD children, more lateralized to the left hemisphere in the TD group. Most important, region of interest (ROI) analysis on parietal and premotor regions showed that, in UCP, the MNS was more strongly activated by observation of actions performed by the paretic hand, a motor model more similar to the observer's motor repertoire. Conclusions . This study shows that children affected by spastic UCP exhibit enhanced activation of the MNS during observation of goal-directed actions performed by a pathological model with respect to a healthy one.

Current knowledge regarding the processing of observed manipulative actions (OMAs) (e.g., grasping, dragging, or dropping) is limited to grasping and underlying neural circuitry remains controversial. Here, we addressed these issues by combining chronic neuronal recordings along the anteroposterior extent of monkeys' anterior intraparietal (AIP) area with tracer injections into the recorded sites. We found robust neural selectivity for 7 distinct OMAs, particularly in the posterior part of AIP (pAIP), where it was associated with motor coding of grip type and own-hand visual feedback. This cluster of functional properties appears to be specifically grounded in stronger direct connections of pAIP with the temporal regions of the ventral visual stream and the prefrontal cortex, as connections with skeletomotor related areas and regions of the dorsal visual stream exhibited opposite or no rostrocaudal gradients. Temporal and prefrontal areas may provide visual and contextual information relevant for manipulative action processing. These results revise existing models of the action observation network, suggesting that pAIP constitutes a parietal hub for routing information about OMA identity to the other nodes of the network., (© The Author(s) 2019. Published by Oxford University Press.)

Visuo-motor neurons of the ventral premotor area F5 encode "pragmatic" representations of object in terms of the potential motor acts (e.g., precision grip) afforded by it. Likewise, objects with identical pragmatic features (e.g., small spheres) but different behavioral value (e.g., edible or inedible) convey different "semantic" information and thus afford different goal-directed behaviors (e.g., grasp-to-eat or grasp-to-place). However, whether F5 neurons can extract distinct behavioral affordances from objects with similar pragmatic features is unknown. We recorded 134 F5 visuo-motor neurons in 2 macaques during a contextually cued go/no-go task in which the monkey grasped, or refrained from grasping, a previously presented edible or inedible target to eat it or placing it, respectively. Sixty-nine visuo-motor neurons showed motor selectivity for the target (35 food and 34 object), and about half of them (N = 35) exhibited congruent visual preference. Interestingly, when the monkey grasped in complete darkness and could identify the target only based on haptic feedback, visuo-motor neurons lost their precontact selectivity, but most of them (80%) showed it again 60 ms after hand-target contact. These findings suggest that F5 neurons possess a multimodal access to semantic information on objects, which are transformed into motor representations of the potential goal-directed actions afforded by them., (© The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.)

Grasping relies on a network of parieto-frontal areas lying on the dorsolateral and dorsomedial parts of the hemispheres. However, the initiation and sequencing of voluntary actions also requires the contribution of mesial premotor regions, particularly the pre-supplementary motor area F6. We recorded 233 F6 neurons from 2 monkeys with chronic linear multishank neural probes during reaching-grasping visuomotor tasks. We showed that F6 neurons play a role in the control of forelimb movements and some of them (26%) exhibit visual and/or motor specificity for the target object. Interestingly, area F6 neurons form 2 functionally distinct populations, showing either visually-triggered or movement-related bursts of activity, in contrast to the sustained visual-to-motor activity displayed by ventral premotor area F5 neurons recorded in the same animals and with the same task during previous studies. These findings suggest that F6 plays a role in object grasping and extend existing models of the cortical grasping network., (© The Author 2016. Published by Oxford University Press.)

Our environment offers us a number of opportunities for action. However, sometimes we also have to refrain from acting, for example, when facing a "do not touch" sign placed over a desirable object on the shelf of a shop. Previous findings emphasized the role of mesial frontal and prefrontal regions in the inhibition of stimulus-driven motor responses [1-3], leading to the prediction that motor areas should not become active when one inhibits a motor response. Nevertheless, refraining from performing a specific action might require one to internally represent what one is not doing. Is the motor system simply inhibited in this condition, or does it play an active role in the representation of the withheld action? Here, we show that while the majority of macaque ventral premotor neurons remain silent when the monkey refrains from grasping an object, others, recorded simultaneously with the former, discharge both when the monkey grasps an object ("action") and when it refrains from doing so ("inaction"). The same effect has been shown to be present for mirror neurons [4]. Some of them, besides discharging during action observation, also fire when the observed agent refrains from acting. Notably, neurons discharging during inaction specifically encode either the monkey's own or other's inaction, not both. Our findings indicate that ventral premotor cortex encodes representations of our own or others' action not only when we perform or observe that action but also when its negation is represented., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

Repetitive presentation of the same visual stimulus entails a response decrease in the action potential discharge of neurons in various areas of the monkey visual cortex. It is still unclear whether this repetition suppression effect is also present in single neurons in cortical premotor areas responding to visual stimuli, as suggested by the human functional magnetic resonance imaging literature. Here we report the responses of 'mirror neurons' in monkey area F5 to the repeated presentation of action movies. We find that most single neurons and the population at large do not show a significant decrease of the firing rate. On the other hand, simultaneously recorded local field potentials exhibit repetition suppression. As local field potentials are believed to be better linked to the blood-oxygen-level-dependent (BOLD) signal exploited by functional magnetic resonance imaging, these findings suggest caution when trying to derive conclusions on the spiking activity of neurons in a given area based on the observation of BOLD repetition suppression.

Objects grasped by an agent have a value not only for the acting agent, but also for an individual observing the grasping act. The value that the observer attributes to the object that is grasped can be pivotal for selecting a possible behavioral response. Mirror neurons in area F5 of the monkey premotor cortex have been suggested to play a crucial role in the understanding of action goals. However, it has not been addressed if these neurons are also involved in representing the value of the grasped object. Here we report that observation-related neuronal responses of F5 mirror neurons are indeed modulated by the value that the monkey associates with the grasped object. These findings suggest that during action observation F5 mirror neurons have access to key information needed to shape the behavioral responses of the observer.

Converging experimental evidence indicates that mirror neurons in the monkey premotor area F5 encode the goals of observed motor acts [1-3]. However, it is unknown whether they also contribute to encoding the perspective from which the motor acts of others are seen. In order to address this issue, we recorded the visual responses of mirror neurons of monkey area F5 by using a novel experimental paradigm based on the presentation of movies showing grasping motor acts from different visual perspectives. We found that the majority of the tested mirror neurons (74%) exhibited view-dependent activity with responses tuned to specific points of view. A minority of the tested mirror neurons (26%) exhibited view-independent responses. We conclude that view-independent mirror neurons encode action goals irrespective of the details of the observed motor acts, whereas the view-dependent ones might either form an intermediate step in the formation of view independence or contribute to a modulation of view-dependent representations in higher-level visual areas, potentially linking the goals of observed motor acts with their pictorial aspects., (Copyright © 2011 Elsevier Ltd. All rights reserved.)

Classic mirror self-recognition mark tests involve familiarizing the subject with its mirror image, surreptitiously applying a mark on the subject's eyebrow, nose, or ear, and measuring self-directed behaviors toward the mark. For many non-human primate species, however, direct gaze at the face constitutes an aggressive and threatening signal. It is therefore possible that monkeys fail the mark test because they do not closely inspect their faces in a mirror and hence they have no expectations about their physical appearance. In the current study, we prevented two pig-tailed macaques (Macaca nemestrina) from seeing their own faces in a mirror, and we adopted a modified version of the classic mark test in which monkeys were marked on the chest, a body region to which they normally have direct visual access but that in the current study was visible only via a mirror. Neither monkey tried to touch the mark on its chest, possibly due to a failure to understand the mirror as a reflective surface. To further the monkeys' understanding of the mirror image, we trained them to reach for food using the mirror as the only source of information. After both monkeys had learned mirror-mediated reaching, we replicated the mark test. In this latter phase of the study, only one monkey scratched the red dye on the chest once. The results are consistent with other findings suggesting that monkeys are not capable of passing a mark test and imply that face and body recognition rely on the same cognitive abilities.

Actions performed by others may have different relevance for the observer, and thus lead to different behavioral responses, depending on the regions of space in which they are executed. We found that in rhesus monkeys, the premotor cortex neurons activated by both the execution and the observation of motor acts (mirror neurons) are differentially modulated by the location in space of the observed motor acts relative to the monkey, with about half of them preferring either the monkey's peripersonal or extrapersonal space. A portion of these spatially selective mirror neurons encode space according to a metric representation, whereas other neurons encode space in operational terms, changing their properties according to the possibility that the monkey will interact with the object. These results suggest that a set of mirror neurons encodes the observed motor acts not only for action understanding, but also to analyze such acts in terms of features that are relevant to generating appropriate behaviors.

We investigated the motor and visual properties of F5 grasping neurons, using a controlled paradigm that allows the study of the neuronal discharge during both observation and grasping of many different three-dimensional objects with and without visual guidance. All neurons displayed a preference for grasping of an object or a set of objects. The same preference was maintained when grasping was performed in the dark without visual feedback. In addition to the motor-related discharge, about half of the neurons also responded to the presentation of an object or a set of objects, even when a grasping movement was not required. Often the object evoking the strongest activity during grasping also evoked optimal activity during its visual presentation. Hierarchical cluster analysis indicated that the selectivity of both the motor and the visual discharge of the F5 neurons is determined not by the object shape but by the grip posture used to grasp the object. Because the same paradigm has been used to study the properties of hand-grasping neurons in the dorsal premotor area F2, and in the anterior intraparietal area (AIP), a comparison of the functional properties of grasping-related neurons in the three cortical areas (F5, F2, AIP) is addressed for the first time.

Many object-related actions can be recognized both by their sound and by their vision. Here we describe a population of neurons in the ventral premotor cortex of the monkey that discharge both when the animal performs a specific action and when it hears or sees the same action performed by another individual. These 'audiovisual mirror neurons' therefore represent actions independently of whether these actions are performed, heard or seen. The magnitude of auditory and visual responses did not differ significantly in half the neurons. A neurometric analysis revealed that based on the response of these neurons, two actions could be discriminated with 97% accuracy.

Functional magnetic resonance imaging (fMRI) was used to localize brain areas that were active during the observation of actions made by another individual. Object- and non-object-related actions made with different effectors (mouth, hand and foot) were presented. Observation of both object- and non-object-related actions determined a somatotopically organized activation of premotor cortex. The somatotopic pattern was similar to that of the classical motor cortex homunculus. During the observation of object-related actions, an activation, also somatotopically organized, was additionally found in the posterior parietal lobe. Thus, when individuals observe an action, an internal replica of that action is automatically generated in their premotor cortex. In the case of object-related actions, a further object-related analysis is performed in the parietal lobe, as if the subjects were indeed using those objects. These results bring the previous concept of an action observation/execution matching system (mirror system) into a broader perspective: this system is not restricted to the ventral premotor cortex, but involves several somatotopically organized motor circuits.

Many neurons in inferior area 6, a cortical premotor area, respond to visual stimuli presented in the space around the animal. We were interested to learn whether the receptive fields of these neurons are coded in retinotopic or in body-centered coordinates. To this purpose we recorded single neurons from inferior area 6 (F4 sector) in a monkey trained to fixate a light and detect its dimming. During fixation visual stimuli were moved towards the monkey both within and outside the neuron's receptive field. The fixation point was then moved and the neuron retested with the monkey's gaze deviated to the new location. The results showed that most inferior area 6 visual neurons code the stimulus position in spatial and not in retinal coordinates. It is proposed that these visual neurons are involved in generating the stable body-centered frame of reference necessary for programming visually guided movements.