Modulation of the Intracortical LFP during Action Execution and Observation.

The activity of mirror neurons in macaque ventral premotor cortex (PMv) and primary motor cortex (M1) is modulated by the observation of another's movements. This modulation could underpin well documented changes in EEG/MEG activity indicating the existence of a mirror neuron system in humans. Because the local field potential (LFP) represents an important link between macaque single neuron and human noninvasive studies, we focused on mirror properties of intracortical LFPs recorded in the PMv and M1 hand regions in two macaques while they reached, grasped and held different objects, or observed the same actions performed by an experimenter. Upper limb EMGs were recorded to control for covert muscle activity during observation.The movement-related potential (MRP), investigated as intracortical low-frequency LFP activity (<9 Hz), was modulated in both M1 and PMv, not only during action execution but also during action observation. Moreover, the temporal LFP modulations during execution and observation were highly correlated in both cortical areas. Beta power in both PMv and M1 was clearly modulated in both conditions. Although the MRP was detected only during dynamic periods of the task (reach/grasp/release), beta decreased during dynamic and increased during static periods (hold).Comparison of LFPs for different grasps provided evidence for partially nonoverlapping networks being active during execution and observation, which might be related to different inputs to motor areas during these conditions. We found substantial information about grasp in the MRP corroborating its suitability for brain-machine interfaces, although information about grasp was generally low during action observation.

Arm movements induced by electrical microstimulation in the superior colliculus of the macaque monkey.

Neuronal activity in the deep layers of the macaque (Macaca mulatta) superior colliculus (SC) and the underlying reticular formation is correlated with the initiation and execution of arm movements (Werner, 1993). Although the correlation of this activity with EMGs of proximal arm muscles is as strong as in motor cortex (Werner et al., 1997a; Stuphorn et al., 1999), little is known about the influence of electrical microstimulation in the SC on the initiation and trajectories of arm movements. Our experiments on three macaque monkeys clearly show that arm movements can be elicited by electrical microstimulation in the deep layers of the lateral SC and underlying reticular formation. The most extensively trained monkey, M1, extended his arm toward the screen in front of him more or less stereotypically upon electrical SC stimulation. In two other monkeys, M2 and M3, a larger repertoire of arm movements were elicited, categorized into three movement types, and compared before (M3) and after (M2 and M3) training: twitch (56% vs. 62%), lift (6% vs. 5%), and extend (37% vs. 32%), respectively. Therefore, arm movements induced by electrical stimulation in the monkey SC represent a further component of the functional repertoire of the SC using its impact on motoneurons in the spinal cord, probably via premotor neurons in the brainstem, as well as on structures involved in executing more complex movements such as target-directed reaching. Therefore, the macaque SC could be involved directly in the initiation, execution, and amendment of arm and hand movements.

M1 corticospinal mirror neurons and their role in movement suppression during action observation.

Evidence is accumulating that neurons in primary motor cortex (M1) respond during action observation, a property first shown for mirror neurons in monkey premotor cortex. We now show for the first time that the discharge of a major class of M1 output neuron, the pyramidal tract neuron (PTN), is modulated during observation of precision grip by a human experimenter. We recorded 132 PTNs in the hand area of two adult macaques, of which 65 (49%) showed mirror-like activity. Many (38 of 65) increased their discharge during observation (facilitation-type mirror neuron), but a substantial number (27 of 65) exhibited reduced discharge or stopped firing (suppression-type). Simultaneous recordings from arm, hand, and digit muscles confirmed the complete absence of detectable muscle activity during observation. We compared the discharge of the same population of neurons during active grasp by the monkeys. We found that facilitation neurons were only half as active for action observation as for action execution, and that suppression neurons reversed their activity pattern and were actually facilitated during execution. Thus, although many M1 output neurons are active during action observation, M1 direct input to spinal circuitry is either reduced or abolished and may not be sufficient to produce overt muscle activity.

Neuronal activity in the superior colliculus related to saccade initiation during coordinated gaze-reach movements.

One must be quick and precise when foveating targets to be reached, because the eyes have to guide the hand trajectory by visual feedback, and we may miss a rapidly moving target if our grasping is not fast and accurate enough. To this end, our brains developed mechanisms coordinating gaze and hand movements to optimize the way in which we foveate and reach. One of these mechanisms is the facilitation of the primary saccade--proven in humans and confirmed here in monkeys--which allows the generation of short-latency gaze movements when reaching towards visual targets. Here we tested whether the neuronal activity in the superior colliculus (SC) accounts for this mechanism; alternatively, cortical saccade-related areas could play a major role in the fast initiation of saccades during such elaborated behaviours bypassing the SC. Upon presentation of a target, neurons located at the rostral pole of the SC started the saccade-related pause in their activity earlier in tasks involving coordinated gaze-reach movements than in tasks in which the saccades were made in isolation. In the same tasks neurons located at the caudal SC reached peak firing rates earlier in coordinated gaze-reach movements than with isolated saccades, confirming the tight coupling between their burst activity latencies and the saccadic reaction times. In sum, our results extend the role of the SC in saccade initiation to coordinated gaze-reach movements, identifying its activity as an important part of the distributed neural system for eye-hand coordination.

Role of the rostral superior colliculus in gaze anchoring during reach movements.

When reaching for an object, primates usually look at their target before touching it with the hand. This gaze movement prior to the arm movement allows target fixation, which is usually prolonged until the target is reached. In this manner, a stable image of the object is provided on the fovea during the reach, which is crucial for guiding the final part of the hand trajectory by visual feedback. Here we investigated a neural substrate possibly responsible for this behavior. In particular we tested the influence of reaching movements on neurons recorded at the rostral pole of the superior colliculus (rSC), an area classically related to fixation. Most rSC neurons showed a significant increase in their activity during reaching. Moreover, this increase was particularly high when the reaching movements were preceded by corresponding saccades to the targets to be reached, probably revealing a stronger coupling of the oculo-manual neural system during such a natural task. However, none of the parameters tested--including movement kinematics and target location--was found to be closely related to the observed increase in neural activity. Thus the increase in activity during reaching was found to be rather nonspecific except for its dependence on whether the reach was produced in isolation or in combination with a gaze movement. These results identify the rSC as a neural substrate sufficient for gaze anchoring during natural reaching movements, placing its activity at the core of the neural system dedicated to eye-hand coordination.

Influence of task predictability on the activity of neurons in the rostral superior colliculus during double-step saccades.

Target probability has been shown to modulate motor preparatory activity of neurons in the caudal superior colliculus (SC) of the primate. Here we tested whether top-down processes, such as task predictability, influence the activity of neurons also at the rostral pole of the SC (rSC), classically related to fixation. To investigate this, double-step saccade tasks were embedded in two different paradigms, one containing unpredictable and another containing predictable tasks. During predictable tasks the animals could develop some expectation about the forthcoming second target jump, i.e., anticipate when and where to make the second saccade. Neuronal responses were recorded during both paradigms and compared, revealing the influence of task predictability on the activity of rSC neurons during specific periods of fixation. In particular, neuronal activity stayed significantly lower during the fixation period between two successive saccades in predictable than in unpredictable tasks. In addition there was a learning effect within a session during predictable conditions, i.e., the intersaccadic activity was higher in the early than in the late trials. Further, reaction times for the second saccade were shorter in predictable than in unpredictable tasks. However, we demonstrated that this difference in reaction times cannot be solely accounted for by the reported difference in neural activity, which was mainly influenced by the predictability of the tasks. With these results we show that top-down processes such as predictability are imposed on the activity of neurons in the rostral pole of the primate SC.