Elsevier

NeuroImage

Volume 23, Issue 3, November 2004, Pages 1186-1191
NeuroImage

Spatial and temporal dissociation in prefrontal cortex during action execution

https://doi.org/10.1016/j.neuroimage.2004.07.047Get rights and content

It is widely accepted that dorsolateral prefrontal cortex (DLPFC) is activated at the time of action generation in humans. However, the previous functional neuroimaging studies that have supported this hypothesis temporally integrated brain dynamics and therefore could not demonstrate when DLPFC underwent activation relative to the emergence of voluntary behavior. Data that are time-locked to the instant of voluntary action execution do not reveal DLPFC activation at that moment. Rather, activated foci are seen at the frontal poles. We investigated this apparent conundrum through three differentially constrained experiments, utilizing functional magnetic resonance imaging to identify those prefrontal areas exhibiting functional change at the moment of spontaneous action execution. We observed profound functional dissociation between anterior and dorsolateral regions, compatible with their involvement at different points during the temporal evolution of action: bilaterally the frontal poles activated at the moment of execution, while simultaneously (and relative to a prior activation state) left DLPFC ‘deactivated.’

Introduction

A characteristic of higher organisms is their ability to select which behaviors to execute (or withhold) and when to make such selections. In humans, this capacity has equated with the ‘will’ (Dilman, 1999) and is subserved by executive centers in the prefrontal cortex (Spence et al., 2002). A body of functional neuroimaging work has implicated dorsolateral prefrontal cortex (DLPFC) in the free selection of response behaviors including random number (Jahanshahi et al., 2000) and letter (de Zubicaray et al., 1998) generation, word stem completion (Desmond et al., 1998), verbal fluency (the generation of word sequences constrained by orthographic or semantic rules; Frith et al., 1991, Phelps et al., 1997, Spence et al., 2000), and willed motor action (the selection of which movements to perform from a set of exemplars; Frith et al., 1991, Hyder et al., 1997, Spence et al., 1998). When brain imaging data are integrated over minutes, DLPFC is also seen to be activated when subjects self-initiate motor action (i.e., when they choose when to execute movements; Jenkins et al., 2000). In an ecologically valid model of spontaneous motor action, we have previously allowed these ‘which’ and ‘when’ components of response selection to coexist simultaneously; our minimally constrained, event-related, functional magnetic resonance imaging (fMRI) experiment identified prefrontal regions that were activated at the moment of action execution (Hunter et al., 2003). In that experiment, our data were time-locked to the execution of an explicit action and revealed activated foci located at the frontal poles, in Brodmann area (BA) 10. We were initially surprised not to find activation of DLPFC. However, we reasoned that our approach differed from previous studies in a critical respect: the utilization of event-related fMRI to study motor action which is entirely self-initiated (c.f., Rowe et al., 2000). Previous studies had used ‘blocked’ fMRI (series of individual events modeled as a single, prolonged, block event; Hyder et al., 1997) or positron emission tomography (PET; not involving a time-series model; Frith et al., 1991, Jenkins et al., 2000, Spence et al., 1998) to investigate the ‘which’ or ‘when’ aspects of response selection. They would have identified those brain regions activated within a block (fMRI) or scanning session (PET), regardless of the temporal relationship between such activation and individual, intrablock (session), motor-action events. Crucially, such studies could not reveal when DLPFC underwent activation relative to the moment of action execution. The apparent discrepancy between our event-related work (DLPFC activation absent) and the blocked fMRI/PET work of others (DLPFC activation present) suggested a new hypothesis: that dorsolateral prefrontal cortex is involved during the production of spontaneous motor action, but its involvement is pivotally before the act, so that it undergoes a relative ‘deactivation’ at the moment of action execution (relative to an earlier, activated state).

Section snippets

Subjects

We used event-related fMRI to investigate healthy, right-handed (Oldfield, 1971), male volunteers. Six subjects participated in an initial experiment, and six different subjects participated in two further replication experiments. Subjects were aged 25 ± 3 years (Experiment 1) and 29 ± 5 years (Experiments 2 and 3). No subject had any clinically significant history of medical disorder. All subjects gave informed consent to participate in the study, which was approved by the North and South

Results

In Experiment 1, we observed deactivation of left DLPFC (BA 46), at the moment of spontaneous motor-action execution. Fig. 1 demonstrates the clear functional dissociation between this area and the bilateral activation foci seen at the frontal poles (BA 10), which we observed in our original analysis (Hunter et al., 2003). Fig. 2 shows averaged hemodynamic series from the three main regions of interest (right and left frontal poles, and left DLPFC) in a time frame encompassing the period

Discussion

We have used event-related fMRI to demonstrate functional dissociation between distinct prefrontal regions at the moment of spontaneous motor-action execution. Specifically, we have shown that, while frontal pole regions are activated at the point of action execution, left DLPFC deactivates, a finding crucially different from those of previous studies.

The area of left DLPFC deactivation that we observed, in Experiment 1, was maximal at a relatively inferior location, close to premotor cortex

Acknowledgments

M.D.H. is supported by the Wellcome Trust. An investigator-led award to S.A.S. from Cephalon (UK) supported R.D.J.G. We thank our radiographer colleagues at the Academic Unit of Radiology, University of Sheffield, for assistance during image acquisition.

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