Visual and motor properties of single neurons of monkey ventral premotor cortex (area F5) were studied in a behavioral paradigm consisting of four conditions: object grasping in light, object grasping in dark, object fixation, and fixation of a spot of light. The employed objects were six different three-dimensional (3-D) geometric solids. Two main types of neurons were distinguished: motor neurons (n = 25) and visuomotor neurons (n = 24). Motor neurons discharged in association with grasping movements. Most of them (n = 17) discharged selectively during a particular type of grip. Different objects, if grasped in similar way, determined similar neuronal motor responses. Visuomotor neurons also discharged during active movements, but, in addition, they fired also in response to the presentation of 3-D objects. The majority of visuomotor neurons (n = 16) showed selectivity for one or few objects. The response was present both in object grasping in light and in object fixation conditions. Visuomotor neurons that selectively discharged to the presentation of a given object discharged also selectively during grasping of that object. In conclusion, object shape is coded in F5 even when a response to that object is not required. The possible visual or motor nature of this object coding is discussed.
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.
Brain control of prehension is thought to rely on two specific brain circuits: a dorsomedial one (involving the areas of the superior parietal lobule and the dorsal premotor cortex) involved in the transport of the hand toward the object and a dorsolateral one (involving the inferior parietal lobule and the ventral premotor cortex) dealing with the preshaping of the hand according to the features of the object. The present study aimed at testing whether a pivotal component of the dorsomedial pathway (area V6A) is involved also in hand preshaping and grip formation to grasp objects of different shapes.Two macaque monkeys were trained to reach and grasp different objects. For each object, animals used a different grip: whole-hand prehension, finger prehension, hook grip, primitive precision grip, and advanced precision grip. Almost half of 235 neurons recorded from V6A displayed selectivity for a grip or a group of grips. Several experimental controls were used to ensure that neural modulation was attributable to grip only.Thesefindings,inconcertwithpreviousstudiesdemonstratingthatV6Aneuronsaremodulatedbyreachdirectionandwristorientation,that lesion of V6A evokes reaching and grasping deficits, and that dorsal premotor cortex contains both reaching and grasping neurons, indicate that the dorsomedial parieto-frontal circuit may play a central role in all phases of reach-to-grasp action. Our data suggest new directions for the modeling of prehension movements and testable predictions for new brain imaging and neuropsychological experiments.
We investigated the properties of neurons located in the distal forelimb field of dorsal premotor area F2 of macaque monkey using a behavioral paradigm for studying the neuronal discharge during observation (object fixation condition) and grasping of different 3-dimensional objects with and without visual guidance of the movement (movement in light and movement in dark conditions, respectively). The main result is that almost all studied neurons were selective for both the type of prehension and the wrist orientation required for grasping an object. Three categories of neurons were found: purely motor, visually modulated, and visuomotor neurons. The discharge of purely motor neurons was not affected by either object presentation or by the visual feedback of the hand approaching to and interacting with the object. Visually modulated neurons presented a different discharge in the 2 movement conditions, this determining a decrease in selectivity for the grip and wrist orientation in the movement in dark condition. Visuomotor neurons typically discharged during the object fixation task even in the absence of any grasping movement. Nine of them also displayed a different discharge rate between the 2 movement conditions. Congruence was observed between the neuron response during the most effective type of prehension and the neuron response during observation of the object requiring that particular prehension. These results indicate an important role of F2 in the control of goal-related hand movements.
We used the quantitative 14 C-deoxyglucose method to map the activity pattern throughout the frontal cortex of rhesus monkeys, which either grasped a three-dimensional object or observed the same grasping movements executed by a human. We found that virtually the same frontal cortical networks were recruited for the generation and the perception of action, including the primary motor cortex (MI/F1), premotor cortical areas (F2, F5, and F6), the primary (SI) and supplementary (SSA) somatosensory cortex, medial cortical areas (8m and 9m), and the anterior cingulate. The overlapping networks for action execution and action observation support the notion that mental simulation of action could underlie the perception of others' actions. We suggest that the premotor and the somatotopic MI/F1 activations induced by action observation reflect motor grasp of the observed action, whereas the somatotopic SI and the SSA activations reflect recruitment of learned sensory-motor associations enabling perceptual understanding of the anticipated somatosensory feedback. We also found that the premotor activations were stronger for action observation, in contrast to the primary somatosensory-motor ones, which were stronger for action execution, and that activations induced by observation were bilateral, whereas those induced by execution were contralateral to the moving forelimb. We suggest that these differences in intensity and lateralization of activations between the executive and the perceptual networks help attribute the action to the correct agent, i.e., to the "self" during action execution and to the "other" during action observation. Accordingly, the "sense of agency" could be articulated within the core components of the circuitry supporting action execution/observation.
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