It is now commonly accepted that planning and execution of movements are based on distributed processing by neuronal populations in motor cortical areas. It is less clear, though, how these populations organize dynamically to cope with the momentary computational demands. Simultaneously recorded activities of neurons in the primary motor cortex of monkeys during performance of a delayed-pointing task exhibited context-dependent, rapid changes in the patterns of coincident action potentials. Accurate spike synchronization occurred in relation to external events (stimuli, movements) and was commonly accompanied by discharge rate modulations but without precise time locking of the spikes to these external events. Spike synchronization also occurred in relation to purely internal events (stimulus expectancy), where firing rate modulations were distinctly absent. These findings indicate that internally generated synchronization of individual spike discharges may subserve the cortical organization of cognitive motor processes.

Since the first descriptions of sensorimotor rhythms by Berger (1929) and by Jasper and Penfield (1949), the potential role of beta oscillations (~13-30 Hz) in the brain has been intensely investigated. We start this review by showing that experimental studies in humans and monkeys have reached a consensus on the facts that sensorimotor beta power is low during movement, transiently increases after movement end (the "beta rebound") and tonically increases during object grasping. Recently, a new surge of studies exploiting more complex sensorimotor tasks including multiple events, such as instructed delay tasks, reveal novel characteristics of beta oscillatory activity. We therefore proceed by critically reviewing also this literature to understand whether modulations of beta oscillations in task epochs other than those during and after movement are consistent across studies, and whether they can be reconciled with a role for beta oscillations in sensorimotor transmission. We indeed find that there are additional processes that also strongly affect sensorimotor beta oscillations, such as visual cue anticipation and processing, fitting with the view that beta oscillations reflect heightened sensorimotor transmission beyond somatosensation. However, there are differences among studies, which may be interpreted more readily if we assume multiple processes, whose effects on the overall measured beta power overlap in time. We conclude that beta oscillations observed in sensorimotor cortex may serve large-scale communication between sensorimotor and other areas and the periphery.

1. This study was devoted to the neuronal processes underlying the construction of the motor program. Two monkeys were trained in a choice reaction time task to perform precise wrist flexion and extension movements of small and large extent. During a trial, the first visual signal, the preparatory signal (PS), informed the animal completely, partially, or not at all about direction and/or extent of the forthcoming movement. After a constant waiting period, a second visual signal, the response signal (RS), was illuminated calling for execution of the requested movement. 2. Reaction time (RT) and movement time (MT) measurements during the training as well as the recording sessions revealed that providing prior information about movement parameters strongly affected RT, but only slightly affected MT. Reaction time decreased in relation to the amount (number of movement parameters precued) and the type of prior information. Providing information about movement direction shortened RT much more than providing information about movement extent. Behavioral data support a parametric conception of motor programming, i.e., that the programming of the different movement parameters results from assembling separate processes of different duration. These results are compatible with the model in which programming processes are serially and hierachically ordered, movement direction being processed before movement extent. 3. Single-cell recording techniques were used to study neuronal activity of the primary motor (MI) and the premotor (PM) cortex, contralateral to the active arm. The activity of 155 neurons of MI and 158 neurons of PM was recorded during performance of the task. Of these 313 neurons, only 14 neurons did not change their activity during execution of the task. Two hundred and seven neurons whose activity changes were related to movement direction and/or movement extent have been selected for the further study. They were classified into three main groups: 1) execution-related neurons (49 in MI, 27 in PM), 2) preparation- and execution-related neurons (48 in MI, 54 in PM), and 3) preparation-related neurons (8 in MI, 21 in PM). 4. Directionally selective, execution-related neurons were found to be more frequently located within MI (81/105, 77.1%) than within PM (55/102, 53.9%), whereas directionally selective, preparation-related neurons appeared to be more frequently located within PM (47/102, 46.1%) than within MI (24/105, 22.9%).(ABSTRACT TRUNCATED AT 400 WORDS)

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While a goal-directed movement is prepared, motor cortical neurons selectively change their activity in relation to prior information about movement direction. Only little is known, however, about the neuronal representation of partial information about this parameter. We investigated this question by training monkeys in a multidirectional centre-out pointing task. A preparatory signal provided prior information about one, two or three possible adjacent targets, thus manipulating the level of certainty about movement direction. After a 1-s delay, the response signal specified one of the precued targets to indicate the actual movement to be performed. Based on the directional tuning curves of individual motor cortical neurons determined during the reaction time interval, we constructed distributions of the population activation (DPAs), which we were then able to estimate as well during the preparatory period. We found that these distributions were preshaped by prior information, with peaks of activation centred over the range of precued movement directions. These peaks sharpened as the response signal approached, and shifted to the specified movement direction subsequent to that signal. Wider ranges of precued movement directions were represented by broader DPAs. Trials in which monkeys produced short reaction times were characterized by narrower distributions than trials with long reaction times. Our study thus provides evidence for (i) a graded preshaping of the neuronal population representation of movement direction by partial information about this parameter, and (ii) the continuous evolution of the preshaped population representation during the preparatory period towards movement initiation.

While oscillations of the local field potential (LFP) are commonly attributed to the synchronization of neuronal firing rate on the same time scale, their relationship to coincident spiking in the millisecond range is unknown. Here, we present experimental evidence to reconcile the notions of synchrony at the level of spiking and at the mesoscopic scale. We demonstrate that only in time intervals of significant spike synchrony that cannot be explained on the basis of firing rates, coincident spikes are better phase locked to the LFP than predicted by the locking of the individual spikes. This effect is enhanced in periods of large LFP amplitudes. A quantitative model explains the LFP dynamics by the orchestrated spiking activity in neuronal groups that contribute the observed surplus synchrony. From the correlation analysis, we infer that neurons participate in different constellations but contribute only a fraction of their spikes to temporally precise spike configurations. This finding provides direct evidence for the hypothesized relation that precise spike synchrony constitutes a major temporally and spatially organized component of the LFP.

Decisions based on sensory evaluation during single trials may depend on the collective activity of neurons distributed across brain circuits. Previous studies have deepened our understanding of how the activity of individual neurons relates to the formation of a decision and its storage for later report. However, little is known about how decision-making and decision maintenance processes evolve in single trials. We addressed this problem by studying the activity of simultaneously recorded neurons from different somatosensory and frontal lobe cortices of monkeys performing a vibrotactile discrimination task. We used the hidden Markov model to describe the spatiotemporal pattern of activity in single trials as a sequence of firing rate states. We show that the animal's decision was reliably maintained in frontal lobe activity through a selective state sequence, initiated by an abrupt state transition, during which many neurons changed their activity in a concomitant way, and for which both latency and variability depended on task difficulty. Indeed, transitions were more delayed and more variable for difficult trials compared with easy trials. In contrast, state sequences in somatosensory cortices were weakly decision related, had less variable transitions, and were not affected by the difficulty of the task. In summary, our results suggest that the decision process and its subsequent maintenance are dynamically linked by a cascade of transient events in frontal lobe cortices.