The macaque ventral premotor area F5 hosts two types of visuomotor grasping neurons: "canonical" neurons, which respond to visually presented objects and underlie visuomotor transformation for grasping, and "mirror" neurons, which respond during the observation of others' action, likely playing a role in action understanding. Some previous evidence suggested that canonical and mirror neurons could be anatomically segregated in different sectors of area F5. Here we investigated the functional properties of single neurons in the hand field of area F5 using various tasks similar to those originally designed to investigate visual responses to objects and actions. By using linear multielectrode probes, we were able to simultaneously record different types of neurons and to precisely localize their cortical depth. We recorded 464 neurons, of which 243 showed visuomotor properties. Canonical and mirror neurons were often present in the same cortical sites; and, most interestingly, a set of neurons showed both canonical and mirror properties, discharging to object presentation as well as during the observation of experimenter's goal-directed acts (canonical-mirror neurons). Typically, visual responses to objects were constrained to the monkey peripersonal space, whereas action observation responses were less space-selective. Control experiments showed that space-constrained coding of objects mostly relies on an operational (action possibility) rather than metric (absolute distance) reference frame. Interestingly, canonical-mirror neurons appear to code object as target for both one's own and other's action, suggesting that they could play a role in predictive representation of others' impending actions.

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.

A fundamental capacity of social animals consists in the predictive representation of upcoming events in the outside world, such as the actions of others. Here, we tested the activity of ventral premotor area F5 mirror neurons (MNs) while monkeys observed an experimenter performing (Action condition) or withholding (Inaction condition) a grasping action, which could be predicted on the basis of previously presented auditory instructions. Many of the recorded MNs discharged only during action observation (Action MNs), but one-third also encoded the experimenter's withheld action (Inaction MNs). Interestingly, while most of Action MNs exhibited reactive discharge during action observation, becoming active after the go signal, the majority of Inaction MNs showed predictive discharge. MN population activity as a whole displayed an overall predictive activation pattern, becoming active, on average, 340 ms before the go signal. Furthermore, MNs became active earlier when the observed action was performed in the monkeys' extrapersonal rather than peripersonal space, suggesting that context-based neural prediction of others' actions plays different roles depending on the monkeys' ability to interact with the observed agent.

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.

With the novel probes it is possible to record stable biologically relevant data over a time span exceeding the usual time needed for epileptic focus localisation in human patients. This is the first time that single units are recorded along cylindrical polyimide probes chronically implanted 22 mm deep into the brain of a monkey, which suggests the potential usefulness of this probe for human applications.