Grasping objects requires the selection of specific grip postures in relation to the objects' physical properties. Furthermore, grasping acts can be embedded in actions aimed at different goals, depending on the context in which the action is performed. Here we assessed whether information on grip and action type integrate at the single-neuron level within the parieto-frontal motor system. For this purpose, we trained three monkeys to perform simple grasp-to-eat and grasp-to-place actions, depending on contextual cues, in which different grip types were required in relation to target features. We recorded 173 grasping neurons: 86 from the inferior parietal area PFG and 87 from the ventral premotor area F5. Results showed that most neurons in both areas are selective for grip type, but the discharge of many of them, particularly in PFG, appears to differ in relation to action context. Kinematics data and control experiments indicated that neuronal selectivity appears more likely to depend on the action goal triggered by the context than on specific contextual elements. The temporal dynamics of grip and goal selectivity showed that grasping neurons reflect first “how” the object has to be grasped (grip), to guide and monitor the hand shaping phase, and then “why” the action is performed (goal), very likely to facilitate subsequent motor acts following grasping. These findings suggest that, in the parieto-frontal system, grip types and action goals are processed by both parallel and converging pathways, and area PFG appears to be particularly relevant for integrating this information for action organization.

The prefrontal cortex (PFC) is deemed to underlie the complexity, flexibility, and goal-directedness of primates' behavior. Most neurophysiological studies performed so far investigated PFC functions with arm-reaching or oculomotor tasks, thus leaving unclear whether, and to which extent, PFC neurons also play a role in goal-directed manipulative actions, such as those commonly used by primates during most of their daily activities. Here we trained two macaques to perform or withhold grasp-to-eat and grasp-to-place actions, depending on the combination of two subsequently presented cues: an auditory go/no-go cue (high/low tone) and a visually presented target (food/object). By varying the order of presentation of the two cues, we could segment and independently evaluate the processing and integration of contextual information allowing the monkey to make a decision on whether or not to act, and what action to perform. We recorded 403 task-related neurons from the ventrolateral prefrontal cortex (VLPFC): unimodal sensory-driven (37%), motor-related (21%), unimodal sensory-and-motor (23%), and multisensory (19%) neurons. Target and go/no-go selectivity characterized most of the recorded neurons, particularly those endowed with motor-related discharge. Interestingly, multisensory neurons appeared to encode a behavioral decision independently from the sensory modality of the stimulus allowing the monkey to make it: some of them reflected the decision to act or refraining from acting (56%), whereas others (44%) encoded the decision to perform (or withhold) a specific action (e.g., grasp-to-eat). Our findings indicate that VLPFC neurons play a role in the processing of contextual information underlying motor decision during goal-directed manipulative actions.

One of the fundamental challenges in behavioral neurophysiology in awake animals is the steady recording of action potentials of many single neurons for as long as possible. Here, we present single neuron data obtained during acute recordings mainly from premotor cortices of three macaque monkeys using a silicon-based linear multielectrode array. The most important aspect of these probes, compared with similar models commercially available, is that, once inserted into the brain using a dedicated insertion device providing an intermediate probe fixation by means of vacuum, they can be released and left floating in the brain. On the basis of our data, these features appear to provide (i) optimal physiological conditions for extracellular recordings, (ii) good or even excellent signal-to-noise ratio depending on the recorded brain area and cortical layer, and (iii) extreme stability of the signal over relatively long periods. The quality of the recorded signal did not change significantly after several penetrations into the same restricted cortical sector, suggesting limited tissue damage due to probe insertion. These results indicate that these probes offer several advantages for acute neurophysiological experiments in awake monkeys, and suggest the possibility to employ them for semichronic or even chronic studies.