Behavioural Brain Research 169 (2006) 335–351 Research report The pre-movement component of motor cortical local field potentials reflects the level of expectancy ebastien Roux a , William A. Mackay b,1 , Alexa Riehle a, a Mediterranean Institute of Cognitive Neuroscience (INCM), National Center for Scientific Research (CNRS) & Aix-Marseille University, 31 chemin Joseph Aiguier, 13402 Marseille C´ edex 20, France b Department of Physiology, University of Toronto, Toronto, Ont., Canada M5S 1A8 Received 17 October 2005; received in revised form 3 February 2006; accepted 9 February 2006 Abstract Cortical local field potentials (LFPs) are modulated in parallel with single neuron discharge, but the information they carry is often unclear. Multi-electrode recordings of both LFPs and single neuron activities were made in motor cortex as monkeys performed a delayed pointing task in which the probability of the moment of signal occurrence, and thus movement execution, was manipulated. A large positive LFP component (P1) appeared immediately preceding movement onset only under conditions of low probability, that is, when a response signal was weakly expected. The amplitude of P1 was much smaller when probability of signal occurrence was high, or when the same movement was self-paced. Although P1 has been described as being linked to the descending motor signal, we found that it was more closely associated with the processing of movement- related information than with the ultimate motor command. Its timing did not bear a fixed relationship with movement onset and its frequency of occurrence in each monkey varied in parallel with each animal’s overall performance and the percentage of context-related “pre-processing” neurons encountered. © 2006 Elsevier B.V. All rights reserved. Keywords: Local field potential; Monkey motor cortex; Preparation; Expectancy; Multi-electrodes; Single neurons; Pre-processing 1. 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 appropri- ate 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 neu- rons 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 Corresponding author. Tel.: +33 491 164329; fax: +33 491 164498. E-mail addresses: roux@incm.cnrs-mrs.fr (S. Roux), william.mackay@utoronto.ca (W.A. Mackay), alexa@incm.cnrs-mrs.fr (A. Riehle). 1 Tel.: +1 416 978 2675; fax: +1 416 978 4940. 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 ([2,4,19–21,32]; for a review, see [13,14]), secondly, movement-aligned potentials [7,24], and thirdly, correlations between LFPs recorded on dif- ferent 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 preced- ing 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 0166-4328/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.bbr.2006.02.004