SummaryEvidence is accumulating that neurons in primary motor cortex (M1) respond during action observation [1, 2], a property first shown for mirror neurons in monkey premotor cortex [3]. 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 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.
Here, we report the properties of neurons with mirror-like characteristics that were identified as pyramidal tract neurons (PTNs) and recorded in the ventral premotor cortex (area F5) and primary motor cortex (M1) of three macaque monkeys. We analysed the neurons’ discharge while the monkeys performed active grasp of either food or an object, and also while they observed an experimenter carrying out a similar range of grasps. A considerable proportion of tested PTNs showed clear mirror-like properties (52% F5 and 58% M1). Some PTNs exhibited ‘classical’ mirror neuron properties, increasing activity for both execution and observation, while others decreased their discharge during observation (‘suppression mirror-neurons’). These experiments not only demonstrate the existence of PTNs as mirror neurons in M1, but also reveal some interesting differences between M1 and F5 mirror PTNs. Although observation-related changes in the discharge of PTNs must reach the spinal cord and will include some direct projections to motoneurons supplying grasping muscles, there was no EMG activity in these muscles during action observation. We suggest that the mirror neuron system is involved in the withholding of unwanted movement during action observation. Mirror neurons are differentially recruited in the behaviour that switches rapidly between making your own movements and observing those of others.
In search of the neuronal substrate for motion analysis in the ferret (Mustela putorius furo), we extracellularly recorded from extrastriate visual cortex in five pigmented and two albino ferrets under general anaesthesia and paralysis. Visual stimulation consisted of large area random dot patterns moving either on a circular path in the frontoparallel plane or expanding and contracting radially. Strongly direction-selective neurons were recorded in a circumscribed area in and just posterior to the suprasylvian sulcus, thus named by us the posterior suprasylvian area (area PSS). Altogether, we recorded 210 (90%) and 95 (72%) PSS neurons in pigmented and albino ferrets, respectively, that were direction selective. In these neurons responses during random dot pattern stimulation in the preferred direction were at least twice as strong than stimulation in the non-preferred direction. Response strength in preferred direction and tuning sharpness of PSS neurons in albinos were significantly reduced when compared to pigmented animals (median values: 34.1 versus 14.8 spikes/s and 142 versus 165 degrees for pigmented and albino ferrets, respectively). Inter-spike-intervals during visual stimulation were significantly shorter in pigmented (median 9 ms) than in albino PSS neurons (median 14 ms). Our data indicate that area PSS may play a crucial role in motion perception in the ferret.
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.
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