Low and high beta rhythms have different motor cortical sources and distinct roles in movement control and spatiotemporal attention.

Low and high beta frequency rhythms were observed in the motor cortex, but their respective sources and behavioral correlates remain unknown. We studied local field potentials (LFPs) during pre-cued reaching behavior in macaques. They contained a low beta band (<20 Hz) dominant in primary motor cortex and a high beta band (>20 Hz) dominant in dorsal premotor cortex (PMd). Low beta correlated positively with reaction time (RT) from visual cue onset and negatively with uninstructed hand postural micro-movements throughout the trial. High beta reflected temporal task prediction, with selective modulations before and during cues, which were enhanced in moments of increased focal attention when the gaze was on the work area. This double-dissociation in sources and behavioral correlates of motor cortical low and high beta, with respect to both task-instructed and spontaneous behavior, reconciles the largely disparate roles proposed for the beta rhythm, by suggesting band-specific roles in both movement control and spatiotemporal attention.

Is there an Intrinsic Relationship between LFP Beta Oscillation Amplitude and Firing Rate of Individual Neurons in Macaque Motor Cortex?

The properties of motor cortical local field potential (LFP) beta oscillations have been extensively studied. Their relationship to the local neuronal spiking activity was also addressed. Yet, whether there is an intrinsic relationship between the amplitude of beta oscillations and the firing rate of individual neurons remains controversial. Some studies suggest a mapping of spike rate onto beta amplitude, while others find no systematic relationship. To help resolve this controversy, we quantified in macaque motor cortex the correlation between beta amplitude and neuronal spike count during visuomotor behavior. First, in an analysis termed "task-related correlation", single-trial data obtained across all trial epochs were included. These correlations were significant in up to 32% of cases and often strong. However, a trial-shuffling control analysis recombining beta amplitudes and spike counts from different trials revealed these task-related correlations to reflect systematic, yet independent, modulations of the 2 signals with the task. Second, in an analysis termed "trial-by-trial correlation", only data from fixed trial epochs were included, and correlations were calculated across trials. Trial-by-trial correlations were weak and rarely significant. We conclude that there is no intrinsic relationship between the firing rate of individual neurons and LFP beta oscillation amplitude in macaque motor cortex.

Distinct Modulations in Sensorimotor Postmovement and Foreperiod ß-Band Activities Related to Error Salience Processing and Sensorimotor Adaptation.

In a recent study, Tan et al. (2014a,b) showed that the increase in ß-power typically observed after a movement above sensorimotor regions (ß-rebound) is attenuated when movement-execution errors are induced by visual perturbations. Moreover, akin to sensorimotor adaptation, the effect depended on the context in which the errors are experienced. Thus the ß-rebound attenuation might relate to neural processes involved in trial-to-trial adaptive mechanisms. In two EEG experiments with human participants, along with the ß-rebound, we examine ß-activity during the preparation of reaches immediately following perturbed movements. In the first experiment, we show that both foreperiod and postmovement ß-activities are parametrically modulated by the sizes of kinematic errors produced by unpredictable mechanical perturbations (force field) independent of their on-line corrections. In the second experiment, we contrast two types of reach errors: movement-execution errors that trigger trial-to-trial adaptive mechanisms and goal errors that do not elicit sensorimotor adaptation. Movement-execution errors were induced by mechanical or visual perturbations, whereas goal errors were caused by unexpected displacements of the target at movement initiation. Interestingly, foreperiod and postmovement ß-activities exhibit contrasting patterns, pointing to important functional differences of their underlying neuronal activity. While both types of reach errors attenuate the postmovement ß-rebound, only the kinematic errors that trigger trial-to-trial motor-command updates influenced ß-activity during the foreperiod. These findings suggest that the error-related modulation of the ß-rebound may reflect salience processing, independent of sensorimotor adaptation. In contrast, modulations in the foreperiod ß-power might relate to the motor-command adjustments activated after movement-execution errors are experienced. SIGNIFICANCE STATEMENT: The functional significance of sensorimotor ß-band (15-25 Hz) oscillations remains uncertain. Recently ß-power was found to be reduced following erroneous movements. We extend and refine this novel finding in two crucial ways. First, by contrasting the EEG correlates of movement errors driving or not driving adaptation we dissociate error-salience processing from error-based adaptation. Second, in addition to ß-activity in error trials, we examine ß-power during the preparation of the subsequent movements. We find clearly distinct patterns of error-related modulations for ß-activities preceding and succeeding movements, highlighting critical functional differences. Postmovement ß-power may reflect error-salience processing independent of sensorimotor adaptation. In contrast, modulations in the foreperiod ß-band power may directly relate to the motor-command adjustments activated after movement-execution errors are experienced.

Signs of timing in motor cortex during movement preparation and cue anticipation.

The capacity to accurately anticipate the timing of predictable events is essential for sensorimotor behavior. Motor cortex holds an established role in movement preparation and execution. In this chapter we review the different ways in which motor cortical activity is modulated by event timing in sensorimotor delay tasks. During movement preparation, both single neuron and population responses reflect the temporal constraints of the task. Anticipatory modulations prior to sensory cues are also observed in motor cortex when the cue timing is predictable. We propose that the motor cortical activity during cue anticipation and movement preparation is embedded in a timing network that facilitates sensorimotor processing. In this context, the pre-cue and post-cue activity may reflect a presetting mechanism, complementing processing during movement execution, while prohibiting premature responses in situations requiring delayed motor output.

Modulations of EEG beta power during planning and execution of grasping movements.

Although beta oscillations (≈ 13-35 Hz) are often considered as a sensorimotor rhythm, their functional role remains debated. In particular, the modulations of beta power during preparation and execution of complex movements in different contexts were barely investigated. Here, we analysed the beta oscillations recorded with electroencephalography (EEG) in a precued grasping task in which we manipulated two critical parameters: the grip type (precision vs. side grip) and the force (high vs. low force) required to pull an object along a horizontal axis. A cue was presented 3 s before a GO signal and provided full, partial or no information about the two movement parameters. We measured beta power over the centro-parietal areas during movement preparation and execution as well as during object hold. We explored the modulations of power in relation to the amount and type of prior information provided by the cue. We also investigated how beta power was affected by the grip and force parameters. We observed an increase in beta power around the cue onset followed by a decrease during movement preparation and execution. These modulations were followed by a transient power increase during object hold. This pattern of modulations did not differ between the 4 movement types (2 grips ×2 forces). However, the amount and type of prior information provided by the cue had a significant effect on the beta power during the preparatory delay. We discuss how these results fit with current hypotheses on the functional role of beta oscillations.

The ups and downs of ß oscillations in sensorimotor cortex.

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.

On the anticipatory precue activity in motor cortex.

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.

Context-related frequency modulations of macaque motor cortical LFP beta oscillations.

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.

Evoked potentials in motor cortical local field potentials reflect task timing and behavioral performance.

Evoked potentials (EPs) are observed in motor cortical local field potentials (LFPs) during movement execution (movement-related potentials [MRPs]) and in response to relevant visual cues (visual evoked potentials [VEPs]). Motor cortical EPs may be directionally selective, but little is known concerning their relation to other aspects of motor behavior, such as task timing and performance. We recorded LFPs in motor cortex of two monkeys during performance of a precued arm-reaching task. A time cue at the start of each trial signaled delay duration and thereby the pace of the task and the available time for movement preparation. VEPs and MRPs were strongly modulated by the delay duration, VEPs being systematically larger in short-delay trials and MRPs larger in long-delay trials. Despite these systematic modulations related to the task timing, directional selectivity was similar in short and long trials. The behavioral reaction time was positively correlated with MRP size and negatively correlated with VEP size, within sessions. In addition, the behavioral performance improved across sessions, in parallel with a slow decrease in the size of VEPs and MRPs. Our results clearly show the strong influence of the behavioral context and performance on motor cortical population activity during movement preparation and execution.

Comparison of local measures of spike time irregularity and relating variability to firing rate in motor cortical neurons.

Spike time irregularity can be measured by the coefficient of variation. However, it overestimates the irregularity in the case of pronounced firing rate changes. Several alternative measures that are local in time and therefore relatively rate-independent were proposed. Here we compared four such measures: CV(2), LV, IR and SI. First, we asked which measure is the most efficient for time-resolved analyses of experimental data. Analytical results show that CV(2) has the less variable estimates. Second, we derived useful properties of CV(2) for gamma processes. Third, we applied CV(2) on recordings from the motor cortex of a monkey performing a delayed motor task to characterize the irregularity, that can be modulated or not, and decoupled or not from firing rate. Neurons with a CV(2)-rate decoupling have a rather constant CV(2) and discharge mainly irregularly. Neurons with a CV(2)-rate coupling can modulate their CV(2) and explore a larger range of CV(2) values.

Interactions between rod and L-cone signals in deuteranopes: gains and phases.

The dynamics of interactions between rod and L-cone driven signals were studied psychophysically in two deuteranopic observers. Flicker detection thresholds for different ratios of rod to L-cone modulation were measured at temporal frequencies between 1 and 15 Hz. A model, which assumes that rod and L-cone driven signals are vector added, can describe the threshold data adequately. We found that up to about 8-10 Hz temporal frequency, rod and L-cone signals interact additively, whereas at higher frequencies the interaction is subtractive. Rod and L-cone signal strengths depend similarly on temporal frequency and are maximal between 3 and 5 Hz. The phase difference between rod and L-cone signals increases linearly with temporal frequency, indicating that their responses have a delay difference of about 20 to 30 ms, consistent with involvement of the faster rod pathway. The data would suggest a nearly complete additivity of the rod and cone driven signals when using flashed stimuli. But, literature data showed only partial additivity of the two, suggesting that different postreceptoral mechanisms are involved in the two tasks.

Lateral interactions in the perception of flicker and in the physiology of the lateral geniculate nucleus.

The perception of flicker strength in a center stimulus can be affected by the presence of a surrounding stimulus. We correlated this effect with the interactions between centers and surrounds of the receptive fields (RFs) of neurons in the retino-geniculate pathways. The responses of cells in the lateral geniculate nucleus (LGN) of two New World monkey species, the common marmoset (Callithrix jacchus), and the owl monkey (Aotus azarae) were measured to two spatially non-overlapping sinusoidally modulating luminance stimuli of equal temporal frequency, one of which mainly stimulated the RF center, the other the RF surround. The relative temporal phase between the center and surround stimuli was varied. The response amplitude as a function of relative phase between the center and surround stimuli can be described by a simple model where the RF center and surround responses are vector-added. A minimal response was reached for stimuli in which the surround stimulus led the center stimulus, indicating that the RF surround response lagged the center response. The flicker strength in the center stimulus perceived by human observers was measured psychophysically. It was found that the perceived flicker strength could be described by the same function as was used for the cell data. There were qualitative similarities between the physiological and the psychophysical data, suggesting that the physiological basis of the psychophysically measured spatial interactions is present as early as the LGN. The data indicated the presence of a nonlinearity in center-surround interactions that is influenced by the stimulus contrast. The possible source of this nonlinearity was studied by comparing the center and the surround responses with those in which they were selectively stimulated.

Centre and surround responses of marmoset lateral geniculate neurones at different temporal frequencies.

The responses of marmoset lateral geniculate neurones to stimuli that were composed of a sinusoidally modulating centre stimulus and a surround that was modulated in counterphase were measured. The size of the stimulus centre was varied. These measurements were repeated at different temporal frequencies between 1 and 30 Hz. The response amplitudes and phases depended in a characteristic manner on the stimulus centre size. The response behaviour could be modelled by assuming Gaussian responsivity profiles of the cells' receptive field (RF) centres and surrounds and a phase delay in the RF surround responses, relative to the centre, enabling the description of RF centre and surround response characteristics. We found that the RF centre-to-surround phase difference increased linearly with increasing temporal frequency, indicating a constant delay difference of about 4.5 to 6 ms. A linear model, including low-pass filters, a lead lag stage and a delay, was used to describe the mean RF centre and surround responses. The separate RF centre and surround responses were less band pass than the full receptive field responses of the cells. The linear model provided less satisfactory fits to M-cell responses than to those of P-cells, indicating additional nonlinearities.