Bjørg Elisabeth Kilavik

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.

Long-Term Modifications in Motor Cortical Dynamics Induced by Intensive Practice

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.

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: CV2, LV, IR and SI. First, we asked which measure is the most efficient for time-resolved analyses of experimental data. Analytical results show that CV2 has the less variable estimates. Second, we derived useful properties of CV2 for gamma processes. Third, we applied CV2 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 CV2-rate decoupling have a rather constant CV2 and discharge mainly irregularly. Neurons with a CV2-rate coupling can modulate their CV2 and explore a larger range of CV2 values.

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.

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.

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.

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

In a recent study, Tan et al. (2014a,b) showed that the increase in β-power typically observed after a movement above sensorimotor regions (β-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 β-rebound attenuation might relate to neural processes involved in trial-to-trial adaptive mechanisms. In two EEG experiments with human participants, along with the β-rebound, we examine β-activity during the preparation of reaches immediately following perturbed movements. In the first experiment, we show that both foreperiod and postmovement β-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 β-activities exhibit contrasting patterns, pointing to important functional differences of their underlying neuronal activity. While both types of reach errors attenuate the postmovement β-rebound, only the kinematic errors that trigger trial-to-trial motor-command updates influenced β-activity during the foreperiod. These findings suggest that the error-related modulation of the β-rebound may reflect salience processing, independent of sensorimotor adaptation. In contrast, modulations in the foreperiod β-power might relate to the motor-command adjustments activated after movement-execution errors are experienced. SIGNIFICANCE STATEMENT The functional significance of sensorimotor β-band (15–25 Hz) oscillations remains uncertain. Recently β-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 β-activity in error trials, we examine β-power during the preparation of the subsequent movements. We find clearly distinct patterns of error-related modulations for β-activities preceding and succeeding movements, highlighting critical functional differences. Postmovement β-power may reflect error-salience processing independent of sensorimotor adaptation. In contrast, modulations in the foreperiod β-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.

Relating firing rate and spike time irregularity in motor cortical neurons

Introduction Cortical neurons exhibit highly irregular inter-spike intervals (ISIs) [1]. Differences in irregularity could be in part due to imbalances of excitatory and inhibitory inputs to the neurons, which determines the statistics of the net input [2]. There is experimental evidence that the intrinsic irregularity of neurons in the awake monkey is constant [3]. However, changes in irregularity have also been reported [4,5] in different cortical areas and different behavioral tasks. The classical measure of spike time irregularity is the coefficient of variation (CV), a global measure defined as the dispersion of the ISIs. However, the CV largely overestimates the irregularity in the case of pronounced changes in firing rate. This led several researchers to propose alternative measures of irregularity that are local in time and therefore relatively independent of rate changes. To our knowledge, these measures have never been compared to each other. Here we compare four such measures: the local coefficient of variation CV2 [6], the local variation LV [3], the measure IR [4] and the measure SI [7]. The first question we address is which of these measures is the most efficient for analyzing experimental data in a time-resolved manner where the number of ISIs is limited. Second, we study the variation of the spike time irregularity of neurons recorded in the motor cortex of a monkey while performing a delayed center-out task.

Modifications in motor cortical spiking dynamics induced by practice

Address: 1The Mediterranean Institute for Cognitive Neuroscience, CNRS – Universite de la Mediterranee, Marseille, France, 2Bernstein Center for Computational Neuroscience, Albert-Ludwigs-Universitat, Freiburg, Germany, 3Neurobiology and Biophysics, Institute of Biology III, AlbertLudwigs-Universitat, Freiburg, Germany and 4Theoretical Neuroscience Group, Riken Brain Science Institute, Wako-Shi, Japan