Elsevier

NeuroImage

Volume 49, Issue 4, 15 February 2010, Pages 3338-3348
NeuroImage

Motor timing and motor sequencing contribute differently to the preparation for voluntary movement

https://doi.org/10.1016/j.neuroimage.2009.11.048Get rights and content

Abstract

Two crucial processes preceding voluntary action are determining the time for movement initiation and planning of the specific sequence of motor output. In this study we aimed to differentiate the neural activity related to motor timing and motor sequencing and to examine over what time periods they contribute to premovement activity during the readiness for voluntary action. Eighteen participants performed self-initiated voluntary finger movements in a readiness potential paradigm, both during EEG measurement and during fMRI. The finger movement task involved three conditions: (1) simple repetitive sequences; (2) increased demand on the sequencing of movement order; and (3) increased demand on the timing of movement initiation. Functional MRI and 64 channels EEG were conducted in two separate sessions. Motor timing and motor sequencing were found to involve different neural processes occurring at different times prior to movement initiation. Motor timing involved greater activation in lateral prefrontal regions over the earliest part of premovement activity, from 1200 ms before movement onset. Motor sequencing involved greater activation of dorsal premotor and parietal areas and was reflected in central and parietal scalp regions only over the later part of premovement activity, within 600 ms of movement onset. We suggest that different neural processes contribute to different aspects of the intended action over different time periods during the preparation for movement, and it is the coordinated activity of these multiple regions that is represented in premovement activity during the readiness for voluntary action.

Introduction

The ability to plan and perform voluntary action is essential to express our intentions and manipulate the environment in relation to our own will. Every voluntary movement is preceded by brain activity aimed at preparing and executing the action. When movements are self-initiated, i.e. performed at our own will without any external cue, this brain activity can start up to 2 s before the execution of the movement. The activity appears in the EEG as a slow-rising negative potential that has been called Bereitschaftspotential or Readiness Potential (RP) (Deecke, 1969, Kornhuber and Deecke, 1965). Neuroimaging studies have shown involvement of a widespread higher-motor network in the preparation for action, including the supplementary motor area (SMA), premotor cortex, basal ganglia, inferior and superior parietal lobes, and prefrontal regions including the anterior cingulate (Ball et al., 1999, Cunnington et al., 2002, Cunnington et al., 2003, Deiber et al., 1999).

Premovement activity is suggested to involve two major components: an abstract level of movement preparation and intention to move followed by specific programming for movement execution. The former component is reflected in the early readiness potential and premovement activity of regions including pre-SMA, prefrontal cortex, lateral premotor areas and parietal lobe. The latter component has been associated with the late readiness potential and activity of the primary motor cortex (M1) and SMA proper (Shibasaki and Hallett, 2006).

The function of the mesial motor areas (pre-SMA, SMA-proper and cingulate motor area) during preparation for movement and the specific cognitive or motor processes that contribute to the earliest component of premovement activity are unclear. Two crucial processes preceding voluntary action are determining when to initiate the action and determining the order of movements that are involved in the action. The former process we refer to in this study as motor timing and corresponds to the internal decision on when to perform a voluntary action (Deecke, 1996). It must be noted that the motor timing we examine here is the process of determining the appropriate time for movement initiation. This may be distinct from other forms of motor timing involved in rhythmic movement or coordinating the timing of sub-movements within a sequence (Bengtsson et al., 2005). The later process, motor sequencing, involves the planning of the specific sequence of motor output required to achieve the intended goal of the action. In this study, we examine the contribution of processes related to the timing of movement initiation and motor sequencing to premovement activity during the preparation and readiness for voluntary action.

Previous studies have shown a role of the SMA in both the timing and the sequencing of movement. Neuroimaging studies show that there is a positive correlation between SMA activity and the ordinal complexity of a sequence of movements (Boecker et al., 1998, Sadato et al., 1996a). Moreover intracranial recordings in monkeys have shown that SMA activity is partly related to the selection of a specific sequence order (Shima and Tanji, 1998, Shima and Tanji, 2000). Neuro-cognitive models of time estimation have pointed to the SMA and fronto-striatal circuits as the neuronal substrate of an internal clock that creates representation of time (Macar et al., 2004, Macar et al., 1999, Meck and Benson, 2002) on which mechanisms of movement initiation rely. Studies on motor timing show that premovement activity in the SMA is affected by rhythm complexity (Bengtsson et al., 2005, Chen et al., 2008, Dhamala et al., 2003, Lewis et al., 2004) and when maintaining movement rhythm in the absence of external cues (Rao et al., 1997).

Motor timing and motor sequencing, however, are also separable processes, as previous studies show that some brain regions have a preferential role in motor timing while others are more involved in motor sequencing.

Numerous studies highlight the crucial role of a fronto-parietal circuit in movement sequencing (Bengtsson et al., 2004, Catalan et al., 1998, Rushworth et al., 2001a, Rushworth et al., 2001b, Rushworth et al., 1997, Rushworth et al., 2001c, Sadato et al., 1996b). Rushworth et al. (2001b) studied the effects of motor attention to movement sequencing, showing enhanced activity in the cingulate motor area, dorsal lateral premotor area and intraparietal sulcus when participants specifically attended to sequencing movements. Moreover, sequence preparation is disrupted by stimulation of the parietal cortex by transcranial magnetic stimulation (Rushworth et al., 2001a) and patients with parietal damage show deficits in using advance information for movement sequencing (Rushworth et al., 1997). Bengtsson and co-workers suggested that the posterior parietal area may process trajectories of movements, while the lateral frontal area and the inferior parietal area may be involved in creating abstract representation of sequences of elements (Bengtsson et al., 2004). Therefore ordering movements in sequence seems to rely on a neural circuit involving frontal and parietal areas.

Other studies show that attention to motor timing and decision on when to move specifically involve activity of the right dorsolateral prefrontal cortex (DLPFC) (Lewis and Miall, 2003, Lewis and Miall, 2006). In a recent time processing model (Lewis and Miall, 2003), SMA and DLPFC have been referred to as key structures for time processing. In this model both these areas are involved in time management but they play different roles. During automatic time processing, SMA may act as an internal clock to create a representation of time intervals. Under cognitively controlled time processing an auxiliary internal clock may also be activated in the right prefrontal cortex. This model is in line with evidence of DLPFC involvement in non-routine decision making on the timing of movements (Jahanshahi and Frith, 1998, Jahanshahi et al., 1995, Jenkins et al., 2000).

In this study, we compared in the same paradigm the process of ordering movements in a sequence with the process of timing for movement initiation and the decision on “when to move.” We aimed to differentiate the pattern of neural activity related to each process and to examine when these different processes contribute to neural activity prior to movement initiation. We employed a self-paced movement task in which we separately manipulated motor timing and motor sequencing. We compared a condition of simple repetitive sequences with two conditions of high processing demand related to movement timing and sequencing respectively. In one, we increased demand on movement sequencing by alternating trial-by-trial between two complex finger sequences. In the other, demand on motor timing was increased by alternating trial-by-trial between two different time intervals between sequences. We used ERPs to identify the critical time periods during movement preparation for processes related to the timing of movement initiation and those related to sequencing of movement order. We also used fMRI to identify the brain areas involved in these two processes. In this way we were able to investigate both when and where motor timing and motor sequencing contribute to the preparation for voluntary action.

Section snippets

Participants

Eighteen young healthy volunteers (7 females and 11 males; mean age: 25.5 ± 2.85 years) participated in the experiment and gave their informed consent. All subjects were right-handed according to the Edinburgh Handedness Inventory (Oldfield, 1971). Data of one participant was excluded from EEG analyses due to technical problems during the EEG recording.

Task

Participants were asked to perform fast self-paced sequences of six consecutive movements and to interpose intervals of several seconds between

Behavioural results

In the EEG session, participants performed more errors in Timing (26 ± 9.3%) and Sequencing (16.2 ± 6.9%) conditions than in the Simple condition (8.2 ± 4.8%) (main effect Condition: F(2, 32) = 71.54, P < 0.05). Moreover, the mean error percentage was higher in the Timing condition than in the Sequencing condition.

The means and standard deviations of time intervals between sequences are shown in Fig. 2. As can be seen, the difference between intervals for odd and even sequences in the timing condition

Discussion

The aim of the study was to examine the processes of timing of movement initiation and sequencing of submovements that both contribute to preparing for voluntary action and to examine how their contribution is reflected in pre-movement brain activity. Our data suggest that preparing an action involves multiple systems that independently process specific characteristics of movements and that rely on independent brain circuits. Indeed brain activity was differently modulated when processing

Acknowledgments

This research was supported by the National Health and Medical Research Council of Australia (NHMRC).

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