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.
Grasping actions require the integration of two neural processes, one enabling the transformation of object properties into corresponding motor acts, and the other involved in planning and controlling action execution on the basis of contextual information. The first process relies on parieto-premotor circuits, whereas the second is considered to be a prefrontal function. Up to now, the prefrontal cortex has been mainly investigated with conditional visuomotor tasks requiring a learned association between cues and behavioural output. To clarify the functional role of the prefrontal cortex in grasping actions, we recorded the activity of ventrolateral prefrontal (VLPF) neurons while monkeys (Macaca mulatta) performed tasks requiring reaching-grasping actions in different contextual conditions (in light and darkness, memory-guided, and in the absence of abstract learned rules). The results showed that the VLPF cortex contains neurons that are active during action execution (movement-related neurons). Some of them showed grip selectivity, and some also responded to object presentation. Most movement-related neurons discharged during action execution both with and without visual feedback, and this discharge typically did not change when the action was performed with object mnemonic information and in the absence of abstract rules. The findings of this study indicate that a population of VLPF neurons play a role in controlling goal-directed grasping actions in several contexts. This control is probably exerted within a wider network, involving parietal and premotor regions, where the role of VLPF movement-related neurons would be that of activating, on the basis of contextual information, the representation of the motor goal of the intended action (taking possession of an object) during action planning and execution.
Mirror neurons (MNs) of the monkey ventral premotor cortex (area F5) are a class of cells that match the visual descriptions of others' actions with correspondent motor representations in the observer's brain. Several human studies suggest that one's own motor representations activated during action observation play a role in directing proactive eye movements to the site of the upcoming hand-target interaction. However, there are no data on the possible relationship between gaze behaviour and MN activity. Here we addressed this issue by simultaneously recording eye position and F5 MN activity in two macaques during free observation of a grasping action. More than half of the recorded neurons discharged stronger when the monkey looked at the action than when it did not look at it, but their firing rate was better predicted by 'when' rather than by 'how long' the monkey gazed at the location of the upcoming hand-target interaction. Interestingly, the onset of MN response was linked to the onset of the experimenter's movement, thus making motor representations potentially exploitable to drive eye movements. Furthermore, MNs discharged stronger and earlier when the gaze was 'proactive' compared with 'reactive', indicating that gaze behaviour influences MN activity. We propose that feedforward, automatic representations of other's actions could lead eye movements that, in turn, would provide the motor system with feedback information that enhances the neural representations of the ongoing action.
The desynchronization of alpha and beta oscillations (mu rhythm) in the central scalp EEG during action observation and action execution is thought to reflect neural mirroring processes. However, the extent to which mirror neurons (MNs) or other populations of neurons contribute to such EEG desynchronization is still unknown. Here, we provide the first evidence that, in the monkey, the neuronal activity recorded from the ventral premotor cortex (PMv) strongly contributes to the EEG changes occurring in the beta band over central scalp electrodes, during executed and observed actions. We simultaneously recorded scalp EEG and extracellular activity, Multi Unit Activity (MUA) and Local Field Potentials (LFP), from area F5 of two macaques executing and observing grasping actions. We found that MUA highly correlates with an increase in high gamma LFP power and, interestingly, such LFP power increase also correlates to EEG beta - and in part also to alpha - desynchronization. In terms of timing of signal changes, the increase in high gamma LFP power precedes the EEG desynchronization, during both action observation and execution, thus suggesting a causal role of PMv neuronal activity in the modulation of the alpha and beta mu-rhythm. Lastly, neuronal signals from deeper layers of PMv exert a greater contribution than superficial layers to the EEG beta rhythm modulation, especially during the motor task. Our findings have clear implications for EEG studies in that they demonstrate that the activity of different populations of neurons in PMv contribute to the generation of the mu-rhythm.
Prefrontal cortex is crucial for exploiting contextual information for the planning and guidance of behavioral responses. Among contextual cues, those provided by others’ behavior are particularly important, in primates, for selecting appropriate reactions and suppressing the inappropriate ones. These latter functions deeply rely on the ability to understand others’ actions. However, it is largely unknown whether prefrontal neurons are activated by action observation. To address this issue, we recorded the activity of ventrolateral prefrontal (VLPF) neurons of macaque monkeys during the observation of videos depicting biological movements performed by a monkey or a human agent, and object motion. Our results show that a population of VLPF neurons respond to the observation of biological movements, in particular those representing goal directed actions. Many of these neurons also show a preference for the agent performing the action. The neural response is present also when part of the observed movement is obscured, suggesting that these VLPF neurons code a high order representation of the observed action rather than a simple visual description of it.
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