Grasping is a highly complex movement that requires the coordination of multiple hand joints and muscles. Muscle synergies have been proposed to be the functional building blocks that coordinate such complex motor behaviors, but little is known about how they are implemented in the central nervous system. Here we demonstrate that premotor interneurons (PreM-INs) in the primate cervical spinal cord underlie the spatiotemporal patterns of hand muscle synergies during a voluntary grasping task. Using spike-triggered averaging of hand muscle activity, we found that the muscle fields of PreM-INs were not uniformly distributed across hand muscles but rather distributed as clusters corresponding to muscle synergies. Moreover, although individual PreM-INs have divergent activation patterns, the population activity of PreM-INs reflects the temporal activation of muscle synergies. These findings demonstrate that spinal PreM-INs underlie the muscle coordination required for voluntary hand movements in primates. Given the evolution of neural control of primate hand functions, we suggest that spinal premotor circuits provide the fundamental coordination of multiple joints and muscles upon which more fractionated control is achieved by superimposed, phylogenetically newer, pathways.spinal interneurons | precision grip | muscle synergies | motor control | nonhuman primate
The local field potential (LFP) is a population measure, mainly reflecting local synaptic activity. Beta oscillations (12-40 Hz) occur in motor cortical LFPs, but their functional relevance remains controversial. Power modulation studies have related beta oscillations to a "resting" motor cortex, postural maintenance, attention, sensorimotor binding and planning. Frequency modulations were largely overlooked. We here describe context-related beta frequency modulations in motor cortical LFPs. Two monkeys performed a reaching task with 2 delays. The first delay demanded attention in time in expectation of the visual spatial cue, whereas the second delay involved visuomotor integration and movement preparation. The frequency in 2 beta bands (around 20 and 30 Hz) was systematically 2-5 Hz lower during cue expectancy than during visuomotor integration and preparation. Furthermore, the frequency was directionally selective during preparation, with about 3 Hz difference between preferred and nonpreferred directions. Direction decoding with frequency gave similar accuracy as with beta power, and decoding accuracy improved significantly when combining power and frequency, suggesting that frequency might provide an additional signal for brain-machine interfaces. In conclusion, multiple beta bands coexist in motor cortex, and frequency modulations within each band are as behaviorally meaningful as power modulations, reflecting the changing behavioral context and the movement direction during preparation.
If not properly regulated, the large amount of reafferent sensory signals generated by our own movement could destabilize the CNS. We investigated how input from peripheral nerves to spinal cord is modulated during behavior. We chronically stimulated the deep radial nerve (DR; proprioceptive, wrist extensors), the median nerve (M; mixed, wrist flexors and palmar skin) and the superficial radial nerve (SR; cutaneous, hand dorsum) while four monkeys performed a delayed wrist flexion-extension task. Spinal neurons putatively receiving direct sensory input were defined based on their evoked response latency following nerve stimulation. We compared the influence of behavior on the evoked response (responsiveness to a specific peripheral input) and firing rate of 128 neuron-nerve pairs based on their source nerve. Firing rate increased during movement regardless of source nerve, whereas evoked response modulation was strikingly nerve-dependent. In SR ( = 47) and M ( = 27) neurons (cutaneous or mixed input), the evoked response was suppressed during wrist flexion and extension. In contrast, in DR neurons ( = 54, pure proprioceptive input), the evoked response was facilitated exclusively during movements corresponding to the contraction of DR spindle-bearing muscles (i.e., wrist extension). Furthermore, modulations of firing rate and evoked response were uncorrelated in SR and M neurons, whereas they tended to be positively comodulated in DR neurons. Our results suggest that proprioceptive and cutaneous inputs to the spinal cord are modulated differently during voluntary movements, suggesting a refined gating mechanism of sensory signals according to behavior. Voluntary movements produce copious sensory signals, which may overwhelm the CNS if not properly regulated. This regulation is called "gating" and occurs at several levels of the CNS. To evaluate the specificity of sensory gating, we investigated how different sources of somatosensory inputs to the spinal cord were modulated while monkeys performed wrist movements. We recorded activity from spinal neurons that putatively received direct connections from peripheral nerves while stimulating their source nerves, and measured the evoked responses. Whereas cutaneous inputs were suppressed regardless of the type of movement, muscular inputs were specifically facilitated during relevant movements. We conclude that, even at the spinal level, sensory gating is a refined and input-specific process.
The planning of goal-directed movements requires sensory, temporal, and contextual information to be combined. Sensorimotor functions are embedded in large neuronal networks, but it is unclear how networks organize their activity in space and time to optimize behavior. Temporal coordination of activity in many neurons within a network, e.g., spike synchrony, might be complementary to a firing rate code, allowing efficient computation with overall less population activity. Here we asked the question whether intensive practice induces long-term modifications in the temporal structure of synchrony and firing rate at the population level. Three monkeys were trained in a delayed pointing task in which the selection of movement direction depended on correct time estimation. The synchronous firing among pairs of simultaneously recorded neurons in motor cortex was analyzed using the "unitary event" technique. The evolution of synchrony in both time, within the trial, and temporal precision was then quantified at the level of an entire population of neurons by using two different quantification techniques and compared with the population firing rate. We find that the task timing was represented in the temporal structure of significant spike synchronization at the population level. During practice, the temporal structure of synchrony was shaped, with synchrony becoming stronger and more localized in time during late experimental sessions, in parallel with an improvement in behavioral performance. Concurrently, the average population firing rate mainly decreased. Performance optimization through practice might therefore be achieved by boosting the computational contribution of spike synchrony, allowing an overall reduction in population activity.
Motor cortical neurons are activated during movement preparation and execution, and in response to task-relevant visual cues. A few studies also report activation before the expected presentation of cues. Here, we study specifically this anticipatory activity preceding visual cues in motor cortical areas. We recorded the activity of 1215 neurons in the motor cortex of two macaque monkeys while they performed a center-out reaching task, including two consecutive delays of equal duration, known in advance. During the first delay (D1), they had to await the spatial cue and only reach to the cued target after the second delay (D2). Forty-two percent of the neurons displayed anticipatory activity during D1. Among these anticipatory neurons, 59% increased (D1up) their activity and the remaining decreased (D1down) their activity. By classifying the neurons according to these firing rate profiles during D1, we found that the activity during D2 differed in a systematic way. The D1up neurons were more likely to discharge phasically soon after the spatial cue and were less active during movement execution, whereas the D1down neurons showed the opposite pattern. But, regardless of their temporal activity profiles, the two categories seemed equally involved in early and late motor preparation, as reflected in their directional selectivity. This precue activity in motor cortex may reflect two complementary, coexisting processes: the facilitation of incoming spatial information in parallel with the downregulation of corticospinal excitability to prevent a premature response.
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