Dynamical changes and temporal precision of synchronized spiking activity in monkey motor cortex during movement preparation
Introduction
Movement preparation is considered to be based on central processes which are responsible for improving motor performance (for a review see [22]). For that purpose, sensory and contextual information has to be resembled and integrated to shape the motor output. One strong argument in favour of this efficiency hypothesis of preparatory processes is the fact that providing prior information about movement parameters [25], [30] and/or removing time uncertainty about when to move [8], [26] significantly shortens reaction time. On the neuronal level, it has been shown that motor cortical neurones change their activity selectively in relation to prior information about movement parameters [27], [28], [35]. Furthermore, it has been demonstrated that the activity of single motor cortical neurones is highly predictive for performance speed [28], [29]. In this context, it is widely accepted that sensorimotor functions including preparatory processes are based on joint processing in neuronal networks distributed over various brain structures (cf. [23], [24]). However, it is much less clear, how these networks organize dynamically in space and time to cope with momentary computational demands. The concept emerged that computational processes in the brain could also rely on the relative timing of spike discharges among neurones within such functional groups [1], [3], [11], [19], [32], [34], commonly called cell assemblies [17]. An essential ingredient of the notion of co-ordinated ensemble activity is its flexibility and dynamic nature. To critically test if such a temporal scheme is actually implemented in the central nervous system, it is necessary to simultaneously observe the activities of many neurones, and to analyse these activities for signs of temporal co-ordination. One type of temporal co-ordination may be defined by coincident spiking activities. In order to detect and evaluate the occurrence of coincident spikes we used the modified ‘Unitary Events’ analysis [13], [14], [15], [16]. Basically, this technique allows one to determine epochs containing spike coincidences which violate the assumption of independence of the participating neurones. The interdependence is then interpreted as a signature of a functional cell assembly [5]. The statistical null-hypothesis is formulated on the basis of the individual firing probabilities and allows to calculate the number of expected coincidences. The statistical significance of the measured number of coincidences is evaluated by comparing it with the expected number. By application of this analysis in a sliding window one can determine epochs of significant synchronized activity. The temporal precision of spike synchronization is obtained by additionally varying the allowed coincidence width in the analysis [16]. If cell assemblies exist and are involved in cortical information processing, they should be activated in systematic relation to the behavioural task. Our analysis technique allows us to describe a detailed relationship between spike synchronization, i.e. the activation of a cell assembly [5], rate modulation and behaviourally relevant events [12], [26]. The aim of the study was thus to provide a phenomenological description of this relationship by comparing, in the same neurones, the frequency of occurrence of significant synchronization, its modulation in time and its modification in temporal precision with the modulation in firing rate in the context of the performance of two different delayed multi-directional pointing tasks.
Section snippets
Behavioural procedures
Two rhesus monkeys were trained to perform a multi-directional pointing task. They were cared for in the manner described in the Guiding Principles in the Care and Use of Animals of the American Physiological Society and the French government regulations. The animal sat in a primate chair in front of a vertical panel on which seven touch sensitive, light emitting diodes (LEDs) were mounted, one in the centre and six placed equidistantly on a circle around it. In each trial, two signals were
Results
In both tasks, about a quarter of the task-related neurones recorded in the primary motor cortex fulfilled the criteria described in Section 2 and were thus selected for further analysis. During one experimental session, the activity of two to seven neurones was recorded simultaneously. In task 1, among 229 task-related neurones, we selected 56 of them (recorded in twenty sessions) for constituting sixty pairs. In task 2, among 120 task-related neurones 35 of them (recorded in fifteen sessions)
Discussion and conclusion
The aim of the present paper was to critically test the presence of synchronous spiking activity and to characterize its dynamics during movement preparation. Although the results do not yet allow final conclusions about the role of synchronous spiking activity for movement preparation, there are several non-exclusive ways to interpret the presented dynamics of synchronicity. The analysis of the data revealed two main results. First, synchronous spiking activity in motor cortical areas of the
Acknowledgments
We wish to thank Tatjana Nazir and Stefan Rotter for their constructive comments, Annette Bastian for her help during the experiments and Michèle Coulmance for writing data acquisition and analysis software. FG was supported by the French government (MENRT).
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