Functional Imaging of the Cerebellum during Action Execution and Observation.

We employed the C-deoxyglucose autoradiographic method to map the activity in the cerebellar cortex of rhesus monkeys that performed forelimb movements either in the light or in the dark and of monkeys that observed forelimb movements executed by a human experimenter. The execution of forelimb movements, both in the light and in the dark, activated the forelimb representations in the cerebellar hemispheric extensions of 1) vermian lobules IV-VI and 2) vermian lobule VIIIB, ipsilaterally to the moving forelimb. Activations in the former forelimb representation involved both a paravermal and a lateral hemispheric region.

Action Observation Responses Are Influenced by Movement Kinematics and Target Identity.

In order to inform the debate whether cortical areas related to action observation provide a pragmatic or a semantic representation of goal-directed actions, we performed 2 functional magnetic resonance imaging (fMRI) experiments in humans. The first experiment, involving observation of aimless arm movements, resulted in activation of most of the components known to support action execution and action observation. Given the absence of a target/goal in this experiment and the activation of parieto-premotor cortical areas, which were associated in the past with direction, amplitude, and velocity of movement of biological effectors, our findings suggest that during action observation we could be monitoring movement kinematics.

Action perception and motor imagery: Mental practice of action.

Motor cognition is related to the planning and generation of actions as well as to the recognition and imagination of motor acts. Recently, there is evidence that the motor system participates not only in overt actions but also in mental processes supporting covert actions. Within this framework, we have investigated the cortical areas engaged in execution, observation, and imagination of the same action, by the use of the high resolution quantitative C-deoxyglucose method in monkeys and by fMRI in humans, throughout the entire primate brain.

Neural foundations of overt and covert actions.

We used fMRI to assess the human brain areas activated for execution, observation and 1st person motor imagery of a visually guided tracing task with the index finger. Voxel-level conjunction analysis revealed several cortical areas activated in common across all three motor conditions, namely, the upper limb representation of the primary motor and somatosensory cortices, the dorsal and ventral premotor, the superior and inferior parietal cortices as well as the posterior part of the superior and middle temporal gyrus including the temporo-parietal junction (TPj) and the extrastriate body area (EBA). Functional connectivity analyses corroborated the notion that a common sensory-motor fronto-parieto-temporal cortical network is engaged for execution, observation, and imagination of the very same action.

The Role of the Prefrontal Cortex in Action Perception.

In an attempt to shed light on the role of the prefrontal cortex in action perception, we used the quantitative 14C-deoxyglucose method to reveal the effects elicited by reaching-to-grasp in the light or in the dark and by observation of the same action executed by an external agent. We analyzed the cortical areas in the principal sulcus, the superior and inferior lateral prefrontal convexities and the orbitofrontal cortex of monkeys. We found that execution in the light and observation activated in common most of the lateral prefrontal and orbitofrontal cortical areas, with the exception of 9/46-dorsal activated exclusively for observation and 9/46-ventral, 11 and 13 activated only for execution.

Perception of actions performed by external agents presupposes knowledge about the relationship between action and effect.

We used the (14)C-deoxyglucose method to reveal changes in activity, in the lateral sulcus of monkeys, elicited by reaching-to-grasp in the light or in the dark and by observation of the same action executed by an external agent. Both visually-guided execution and observation of the same action activated the secondary somatosensory cortex, the ventral somatosensory area, the somatorecipient parietal ventral area, the retroinsula and the caudo-medial area of the auditory belt. These matching activations indicate that the somesthetic consequences of movements, generated bottom-up during action execution, may also be triggered top-down during action observation to represent the predicted sensory consequences of the perceived movement.

Involvement of the superior temporal cortex in action execution and action observation.

The role of the superior temporal sulcus (STs) in action execution and action observation remains unsettled. In an attempt to shed more light on the matter, we used the quantitative method of (14)C-deoxyglucose to reveal changes in activity, in the cortex of STs and adjacent inferior and superior temporal convexities of monkeys, elicited by reaching-to-grasp in the light or in the dark and by observation of the same action executed by an external agent. We found that observation of reaching-to-grasp activated the components of the superior temporal polysensory area [STP; including temporo-parieto-occipital association area (TPO), PGa, and IPa], the motion complex [including medial superior temporal area (MST), fundus of superior temporal area (FST), and dorsal and ventral parts of the middle temporal area (MTd and MTv, respectively)], and area TS2.

Topography of Visuomotor Parameters in the Frontal and Premotor Eye Fields.

To determine whether the periarcuate frontal cortex spatially encodes visual and oculomotor parameters, we trained monkeys to repeatedly execute saccades of the same amplitude and direction toward visual targets and we obtained quantitative images of the distribution of metabolic activity in 2D flattened reconstructions of the arcuate sulcus (As) and prearcuate convexity. We found two topographic maps of contraversive saccades to visual targets, separated by a region representing the vertical meridian: the first region straddled the fundus of the As and occupied areas 44 and 6-ventral, whereas the second one occupied areas 8A and 45 in the anterior bank of the As and the prearcuate convexity. The representation of the vertical meridian runs along the posterior borders of areas 8A and 45 (deep in the As).

Viewing a forelimb induces widespread cortical activations.

Given that prerequisite of activating the mirror neuron system is the preshaping of the hand and its interaction with the object during observation of a reaching-to-grasp-an-object action, the effects of viewing the object, the reaching forelimb and the static hand may obscure the effects of observing the grasping action per se. To disentangle these effects, we employed the (14)C-deoxyglucose quantitative autoradiographic method to map the functional activity in the entire cortex of monkeys (Macaca mulatta) which observed the experimenter performing non-goal-directed (purposeless) forelimb movements towards an object that was previously presented but no longer visible. Thus, our monkeys were exposed to the view of an object, a moving arm and a static hand with extended wrist and fingers.

Grasping in the dark activates early visual cortices.

We have previously demonstrated that the primary motor and somatosensory cortices of monkeys are somatotopically activated for action-observation as are for action-generation, indicating that the recruitment of learned somatosensory-motor representations underlies the perception of others' actions. Here we examined the effects of seen and unseen actions on the early visual cortices, to determine whether stored visual representations are employed in addition to the somatosensory-motor ones. We used the quantitative (14)C-deoxyglucose method to map the activity throughout the cortex of the occipital operculum, lunate, and inferior occipital sulci of "rhesus monkeys" who reached to grasp a 3D object either in the light or in the dark or who observed the same action executed by another subject.

The spinal substrate of the suppression of action during action observation.

We have previously demonstrated that the forelimb representations of the primary motor and somatosensory cortices, as well as several premotor and parietal areas, are activated by both action-execution and action-observation, indicating that the spectator mentally simulates the observed action. Moreover, several studies demonstrated repeatedly that corticospinal excitability is modulated during action observation, providing evidence of an activation of the observer's motor system. However, evidence for the involvement of the spinal cord in action observation is controversial.

The place code of saccade metrics in the lateral bank of the intraparietal sulcus.

The lateral intraparietal area (LIP) of monkeys is known to participate in the guidance of rapid eye movements (saccades), but the means it uses to specify movement variables are poorly understood. To determine whether area LIP devotes neural space to encode saccade metrics spatially, we used the quantitative [(14)C]deoxyglucose method to obtain images of the distribution of metabolic activity in the intraparietal sulcus (IPs) of rhesus monkeys trained to repeatedly execute saccades of the same amplitude and direction for the duration of the experiment. Different monkeys were trained to perform saccades of different sizes and in different directions.

Functional imaging of the parietal cortex during action execution and observation.

We used the (14)C-deoxyglucose method to map the functional activity in the cortex of the lateral and medial parietal convexity, the intraparietal and the parietoccipital sulci of monkeys which either reached and grasped a 3D-object or observed the same reaching-to-grasp movements executed by a human. Execution of reaching-to-grasp induced activations in the superior parietal areas SI-forelimb/convexity, PE, PE caudal (PEc); in the intraparietal areas PE intraparietal (PEip), medial intraparietal (MIP), 5 intraparietal posterior, ventral intraparietal (VIP), anterior intraparietal (AIP), lateral intraparietal dorsal; in the inferior parietal areas PF, PFG, PG; in the parietoccipital areas V6, V6A-dorsal; in the medial cortical areas PGm/7m and retrosplenial cortex. Observation of reaching-to-grasp activated areas SI-forelimb/convexity, PE lateral, PEc, PEip, MIP, VIP, AIP, PF, V6, PGm/7m, 31, and retrosplenial cortex.

Mental simulation of action in the service of action perception.

We used the quantitative 14C-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.

Saccade-related information in the superior temporal motion complex: quantitative functional mapping in the monkey.

Although the role of the motion complex [cortical areas middle temporal (V5/MT), medial superior temporal (MST), and fundus of the superior temporal (FST)] in visual motion and smooth-pursuit eye movements is well understood, little is known about its involvement in rapid eye movements (saccades). To address this issue, we used the quantitative 14C-deoxyglucose method to obtain functional maps of the cerebral cortex lying in the superior temporal sulcus of rhesus monkeys executing saccades to visual targets and saccades to memorized targets in complete darkness. Fixational effects were observed in MT-foveal, FST, the anterior part of V4-transitional (V4t), and temporal-occipital areas.

Observation of action: grasping with the mind's hand.

Engagement of the primary motor cortex (MI) during the observation of actions has been debated for a long time. In the present study, we used the quantitative 14C-deoxyglucose method in monkeys that either grasped 3-D objects or observed the same movements executed by humans. We found that the forelimb regions of the MI and the primary somatosensory (SI) cortex were significantly activated in both cases.

When vision guides movement: a functional imaging study of the monkey brain.

Goal-directed reaching requires a precise neural representation of the arm position and the target location. Parietal and frontal cortical areas rely on visual, somatosensory, and motor signals to guide the reaching arm to the desired position in space. To dissociate the regions processing these signals, we applied the quantitative [(14)C]-deoxyglucose method on monkeys reaching either in the light or in the dark.