Research reportThe pre-movement component of motor cortical local field potentials reflects the level of expectancy
Introduction
Many features of motor cortical single neuron activity are not strictly related to the motor signal, i.e. movement generation. Instead they are more closely tied to preparation for a planned movement, or even suppression of movement until the appropriate moment (for a review, see [25]). For example, some activity has been described as “pre-processing” [28], i.e. processing of prior information about features of the forthcoming movement. Furthermore, the transient synchronization of two or more neurons at the end of an estimated time interval can reflect instants of signal expectancy [26], [27]. Such properties are linked to the temporal prediction of forthcoming events, which is essential for optimizing motor performance. Indeed, prior information about when a response signal will occur significantly shortens reaction time [22], [25]. If these processes arise in a sufficiently large population of neurons, they should also be manifested in the local field potential (LFP), possibly indicating the degree of coherent network activity. LFPs may be recorded from the same electrode as the spikes of a single neuron, by simply low-pass filtering the signal. The LFP is a spatially averaged signal from a small volume, assumed to reflect mainly the synaptic input received by the neurons within the observed volume [17], [18].
Studies of LFPs recorded in motor cortical areas have mainly focused on three topics: firstly, stimulus-induced (but not stimulus-locked) oscillatory activity ([2], [4], [19], [20], [21], [32]; for a review, see [13], [14]), secondly, movement-aligned potentials [7], [24], and thirdly, correlations between LFPs recorded on different electrodes, including those from different hemispheres [3]. To our knowledge, Gemba and co-workers were the first to study monkey cortical field potentials in relation to both visually-triggered and self-paced movements. They identified a depth-positive (surface-negative) potential, immediately preceding movement onset [12], that was much larger in motor cortex than in adjacent regions [10]. The pre-movement positivity was interpreted as being strongly motor-related; it disappeared when an operator performed the task, instead of the monkey executing the movement [10]. Since then, the pre-movement positivity has been observed by others (e.g. [7], [16], [24]), and is generally assumed to be linked to the generation of the descending motor volley. It is not, however, significantly modulated by movement direction, although later LFP components are directionally sensitive [24].
We recorded LFPs in two monkeys performing two tasks, a choice reaction time task (chRT) and a self-paced movement task (SELF), first presented in ref. [29]. In both tasks, accurate estimation of two time intervals was essential for correct performance. Surprisingly, we observed a large context-related modulation of the pre-movement positivity (P1). When aligned to movement onset, this pre-movement positive component exhibited amplitude differences in relation to the probability of the moment of the response signal, and timing differences in relation to reaction time. Moreover, the presence of P1 depended strongly on the overall behavioral performance of the monkey. Later LFP components (after movement onset) did not exhibit these properties. Preliminary results were presented in ref. [30].
Section snippets
Experimental procedures
Behavioral tasks (Fig. 1, see [29]): Three male Rhesus monkeys were used in this study. Care and treatment of the animals during all stages of the experiments conformed to the European and French Government Regulations. The animals were trained to execute movements in two opposite directions from a common center position. LFPs were recorded in only two of them, monkeys O and K; the third, monkey R, reported in ref. [29], is included for comparison. On a vertical panel, three touch-sensitive
Behavioral results and EMG data
Learning to discriminate or to estimate two time intervals took several months of daily training. Once the monkey learned the durations, the number of errors decreased and the performance, in terms of reaction time, improved. Performance varied largely from monkey to monkey (for the third monkey trained in this task, monkey R, see [29]). Distributions of trial-by-trial response times are shown in Fig. 1C–F for monkeys K and O, in both tasks recorded during all selected sessions (for selection
The pre-movement positivity: an information processing LFP component
A pre-movement positivity (depth-positive–surface-negative), similar to our P1 component, was described by Gemba et al. [10] in cortical field potentials and interpreted as a motor component. We have shown that P1 has properties that are inconsistent with any direct relationship to the descending motor volley. For the same movement, P1 can be very large or virtually non-existent, depending on the degree of uncertainty about the time of RS. In the present data, the P1 component attained its
Acknowledgements
We thank Driss Boussaoud, Bjørg Kilavik, Martin Nawrot, Alex Thomson and Eilon Vaadia for valuable discussions of an earlier version of the manuscript and Martin Nawrot for help in data analysis. WAM was supported by the CNRS (“poste rouge”) during a sabbatical. The research was supported in part by the CNRS and the French Government (ACI Cognitique “Variability and Invariants”).
References (33)
- et al.
Distribution of potentials preceding visually initiated and self-paced hand movements in various cortical areas of the monkey
Brain Res
(1984) - et al.
Analysis of slow cortical potentials preceding self-paced hand movements in the monkey
Exp Neurol
(1979) Synchronized neuronal oscillations and their role on motor processes
Trends Cogn Sci
(1997)Intracellular synaptic potentials of primate motor cortex neurons during voluntary movement
Brain Res
(1979)- et al.
Neuronal activity and information processing in motor control: from stages to continuous flow
Biol Psychol
(1988) - et al.
Dynamical changes and temporal precision of synchronized spiking activity in monkey motor cortex during movement preparation
J Physiol (Paris)
(2000) - et al.
Cortical field potential associated with hand movement on warning-imperative visual stimulus and cerebellum in the monkey
Brain Res
(1990) - et al.
Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex
J Neurophysiol
(1995) - et al.
Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation
J Physiol
(1997) - et al.
Neural interactions between motor cortical hemispheres during bimanual and unimanual arm movements
Eur J Neurosci
(2001)
Local field potential oscillations in cerebellar cortex: synchronization with cerebral cortex during active and passive expectancy
J Neurophysiol
Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity
J Neurophysiol
Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep phases
J Neurosci
Local field potentials related to bimanual movements in the primary and supplementary motor cortices
Exp Brain Res
Azimuth coding in primary auditory cortex of the cat. I. Spike synchrony versus spike count representations
J Neurophysiol
Pyramidal tract activity associated with a conditioned hand movement in the monkey
J Neurophysiol
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