Neurophysiological study of the monkey brain during target oriented movements

Abstract

In the past, we demonstrated that the neural system which supports both the generation of an action and the perception of the same action performed by another subject encompasses widespread areas in a parieto-frontal cortical network. In the present study we examined whether this system that helps match action perception to action generation extends beyond these areas to early visual cortices. We applied the quantitative autoradiographic method of [14C]- deoxyglucose, combined with cytoarchitectonic identification of cortical areas, to explore early visual cortical areas throughout the cortex of the occipital operculum, lunate and inferior occipital sulci of twelve adult female monkeys (Macaca mulatta) performing three behavioural tasks: (a) grasping-in-the-light (Gl), (b) grasping-observation (O), and (c) grasping-in-the-dark (Gd). In order to disambiguate the effects of the purposely reaching/grasping action from the effects of (a) the non-goal-directed biological-motion elicited by a purposelessly moving forelimb in front of the monkey, and (b) the visual stimulation induced by mere presentation of the 3D-object, we compared the functional activity in the Gl and O monkeys with that in two arm-motion control (Cm) monkeys. To reveal the effects induced by reaching-to-grasp in the dark, we compared the functional activity in the two Gd monkeys with that in two control-in-the-dark monkeys (Cd). In order to reveal the effects induced by the behavioural tasks, we produced and compared twodimensional reconstructions (2D-maps) of the spatio-intensive pattern of metabolic activity (LCGU values in #mol/100 g/min) throughout the full extent of the visual areas V1, V2, V3, V3A, and V4. During grasping-in-the-light increased metabolic activity was evident in extrastriate areas V3d, V3A and V4 with the two segments of area V3d, the occipito-parietal reflecting peripheral vision and the occipito-temporal reflecting central vision being equally activated. During grasping-observation, area V4 was not activated, marginal activation was displayed in the representation of the central visual field of area V1 and significant activation was displayed in areas V3d and V3A with the occipito-temporal region of area V3d being more activated than the occipito-parietal. During grasping-in-the-dark activation was observed in areas V1, V2, V3A, and V3v. Area V3d was markedly activated in its occipito-parietal segment, contrary to the occipito-temporal which was not activated. According to our previous proposal, the activations induced by grasping-observation in the parietal and motor cortex imply that observation of an action corresponds to simulation of its overt counterpart. Based on our present findings, we suggest that the activation of areas V3d and V3A for action-observation and for action-execution in the dark reflects the processing of visual information xv Summary related to the mental simulation of the action. Area V3 may relay to the motor system, via the parieto-frontal visuo-motor stream, visuospatial information required for the reaching component of the action and 3D-object-related information useful for the grasping constituent. Therefore, as the somatotopic activation of the primary somatosensory cortex during action-observation in our previous study supported an introspective kinesthetic feeling of the movement by the observer in a first person perspective, the activation of the early visual cortices during action-generation in the dark in the present study supports an internalized visual representation of the spatial-location and the 3D-form of the invisible object to be reached and grasped, i.e. visual imagery during action control.