Cortical and subcortical connections of parietal and premotor nodes of the monkey hand mirror neuron network.

Mirror neurons (MNs) are a class of cells originally discovered in the monkey ventral premotor cortex (PMv) and inferior parietal lobule (IPL). They discharge during both action execution and action observation and appear to play a crucial role in understanding others' actions. It has been proposed that the mirror mechanism is based on a match between the visual description of actions, encoded in temporal cortical regions, and their motor representation, provided by PMv and IPL. However, neurons responding to action observation have been recently found in other cortical regions, suggesting that the mirror mechanism relies on a wider network. Here we provide the first description of this network by injecting neural tracers into physiologically identified IPL and PMv sectors containing hand MNs. Our results show that these sectors are reciprocally connected, in line with the current view, but IPL MN sectors showed virtually no direct connection with temporal visual areas. In addition, we found that PMv and IPL MN sectors share connections with several cortical regions, including the dorsal and mesial premotor cortex, the primary motor cortex, the secondary somatosensory cortex, the mid-dorsal insula and the ventrolateral prefrontal cortex, as well as subcortical structures, such as motor and polysensory thalamic nuclei and the mid-dorsal claustrum. We propose that each of these regions constitutes a node of an "extended network", through which information relative to ongoing movements, social context, environmental contingencies, abstract rules, and internal states can influence MN activity and contribute to several socio-cognitive functions.

Grasping neurons of monkey parietal and premotor cortices encode action goals at distinct levels of abstraction during complex action sequences.

Natural actions are formed by distinct motor acts, each of which is endowed with its own motor purpose (i.e., grasping), chained together to attain the final action goal. Previous studies have shown that grasping neurons of parietal area PFG and premotor area F5 can code the goal of simple actions in which grasping is embedded. While during simple actions the target is usually visible, directly cueing the final goal, during complex action sequences is often concealed and has to be kept in mind to shape action unfolding. The aim of this study was to assess the relative contribution of sensory-cued or memory-driven information about the final goal to PFG and F5 grasping neurons activity. To this purpose, we trained two monkeys to perform complex action sequences, each including two successive grasping acts, aimed at specific final goals (eating or placing). We recorded 122 PFG and 89 F5 neurons. Forty-seven PFG and 26 F5 neurons displayed action goal selectivity only during the late phase of the action, when sensory information cueing the action goal became available. Reward contingency did not affect neuronal selectivity. Notably, 17 PFG neurons reflected the final goal from the early phase of action unfolding, when only memory-driven information was available. Crucially, when monkeys were prevented from obtaining such information before action onset, neurons lost their early selectivity. Our findings suggest that external sensory cues and individual's motor intention integrate at different level of abstraction within a large anatomo-functional network, encompassing parietal and premotor cortices.

Ventral premotor and inferior parietal cortices make distinct contribution to action organization and intention understanding.

It is well known that ventral premotor area F5 codes the goal of executed and observed motor acts. This area is anatomically connected with part of the inferior parietal cortex (area PFG), which has been recently shown to play a role in action organization and intention understanding. The aims of the present study were 1) to assess whether the discharge of F5 motor neurons and mirror neurons (MNs) codes action goals and 2) to clarify the relative contribution of F5 and PFG in action organization and intention understanding. To this purpose, we first recorded from F5 motor neurons and MNs of 2 monkeys while performing a motor task constituted by 2 actions ("grasp-to-eat" and "grasp-to-place") or observing the same task done by an experimenter. Results showed that some F5 neurons code grasping according to the goal of the action in which it is embedded. Subsequently, we recorded from PFG motor neurons and MNs of the same monkeys, using the same tasks. The comparison between the neuronal properties of F5 and PFG motor neurons suggests that PFG plays a major role in organizing natural actions. Furthermore, the similarities between MNs properties of the 2 areas indicate that they constitute a functional circuit underlying others' intention understanding.