Elsevier

NeuroImage

Volume 37, Issue 4, 1 October 2007, Pages 1354-1361
NeuroImage

The role of the preSMA and the rostral cingulate zone in internally selected actions

https://doi.org/10.1016/j.neuroimage.2007.06.018Get rights and content

Abstract

In everyday life, one can differentiate between actions that are primarily internally guided and actions that are primarily guided by external events. FMRI studies investigating the neural correlates of internally guided actions usually report activation maxima in the rostral cingulate zone (RCZ) as well as the preSMA. However, the pertinent contrasts were often confounded by perceptual and motor differences between the different conditions. In the current study, we reinvestigated the neural correlates of internally vs. externally selected actions using a paradigm that avoids any such perceptual or motor confound. By doing so, we wanted to address the yet unsolved question which differential role the preSMA and RCZ play in internally guided actions. Subjects were required to make left or right key presses at the midpoint between isochronous pacing signals (a sequence of ‘X’s presented to the left or the right of the fixation point). In the internally selected condition, the location of the ‘X’ was determined by the location of the preceding key press that the subjects selected freely. In the externally selected condition, by contrast, the location of the ‘X’ prescribed the location of the subsequent key press response. We found that the RCZ was differentially activated by internally as compared to externally selected actions. In contrast to previous studies, the preSMA showed equal activity in both conditions and thus did not differentiate between the two modes of action selection. This suggests a primary role for the RCZ in internally selected actions.

Introduction

In everyday life, actions are either more internally guided, for example switching on TV to watch the news, or they are more externally guided by environmental stimuli, for example stopping in front of a red traffic light. Voluntary, internally guided actions are not prompted by external cues, but rather guided by intentions. An internally guided action commonly helps the agent to produce a desired effect in the environment (Prinz, 1997). According to the ideomotor theory, voluntary action control is based on learned associations between movements and their perceivable consequences (James, 1890, 1950). An intentional action, according to the ideomotor theory, can be triggered simply by anticipating these consequences (action–effect or A–E bindings) (Hommel et al., 2001, Prinz, 1997). Externally guided actions, on the other side, help the agent to adapt his behavior to environmental demands. This type of behavior is based on associations between cueing stimuli and subsequent actions (stimulus–response or S–R bindings).

For a long time, the focus of psychological research was on the exploration of the functional and neural underpinnings of externally guided actions. During the last years, however, research focused increasingly on the exploration of internally guided actions and how they differ from externally guided actions (Cunnington et al., 2002, Jahanshahi et al., 1995, Keller et al., 2006, Waszak et al., 2005, Wiese et al., 2004, Wiese et al., 2005). Differences between the two modes of action are observed on the behavioral as well as on the neural level. On the behavioral level, it has been shown that reaction times of externally guided actions are shifted toward the triggering stimuli, whereas reaction times of internally guided actions are shifted towards the produced effects (Keller et al., 2006, Waszak et al., 2005). Similarly, Haggard et al. (2002) found that perceptual onset times of actions and their ensuing effects, on the one hand, and of stimuli and subsequent actions in response to them, on the other hand, attracted each other in time. These findings are in line with the notion that stimuli and responses as well as actions and effects share combined representations (S–R and A–E bindings) (Hommel et al., 2001, Prinz, 1997).

Regarding the underlying neuroanatomical differentiations between the two action modes, Goldberg (1985) emphasized the distinction between a medial and a lateral premotor system, which are involved in internally vs. externally guided actions, respectively. However, as Jahanshahi et al. (1995) outlined, even though the concept is very attractive, recent data question the anatomical and functional distinctiveness of major components of the two systems and suggest that their specialization is a matter of degree rather than absolute. This is supported by findings from electrophysiological as well as neuroimaging experiments which suggest that in both action conditions the same areas are activated, but to a stronger degree in the internally guided condition. On the neurophysiological level, there is evidence that the medial wall of the frontal lobe plays a major role in the execution of internally as compared to externally guided actions. According to Picard and Strick (1996), the frontomedian wall consists of the supplementary motor area (SMA), subdivided into the preSMA and the SMA proper, as well as the cingulate motor areas (CMA), which are subdivided into the rostral cingulate zone (RCZ), and the caudal cingulate zone (CCZ).

It is important to note that the decision to perform an internally guided action has at least two components. First, the agent must decide which action out of a certain subset of actions to perform (‘what-component’), and he must determine when to perform the action (‘when-component’). Most studies that have been published in recent years explored the second component. Usually, in these studies, a condition during which subjects self-initially conducted a key press was compared with a condition in which subjects responded to a visual (Debaere et al., 2003, Deiber et al., 1999, Wiese et al., 2004) or acoustic cue (Cunnington et al., 2002, Jahanshahi et al., 1995, Jenkins et al., 2000). From now on, whenever we refer to the when-component of an action, we will call the action internally or externally timed.

However, more recently some studies also dealt with the ‘what-component’ of voluntary action (Cunnington et al., 2006, Lau et al., 2004a, Lau et al., 2006, van Eimeren et al., 2006). Most of these studies report activation loci in the medial wall of the frontal lobe as a neural correlate of internally guided actions, although the exact locations of activation differ from study to study. While some report peak activation in the preSMA (Deiber et al., 1999, Lau et al., 2006), others show activation in the cingulate motor areas (Debaere et al., 2003, Deiber et al., 1999, Jenkins et al., 2000, Wiese et al., 2004) or in both areas (Cunnington et al., 2006, Deiber et al., 1999, Lau et al., 2004a, van Eimeren et al., 2006). From now on, whenever we refer to the what-component of an action, we will call the action internally or externally selected. (We use the term internally or externally guided in a neutral manner, whenever timed and selected are inappropriate.) In the present study, we varied whether an action was internally or externally selected, whereas the timing of the actions was always internally controlled.

On the neuroanatomical level, it is still not clear which role the preSMA and the RCZ play in internally guided actions. One reason for the ambiguity of these findings might be the fact that in most previous studies perceptual and/or motor factors were confounded with the contrast in question (Cunnington et al., 2002, Debaere et al., 2003, Wiese et al., 2005). In some studies, the externally guided condition consisted of a signal that was missing in the internally guided condition (e.g., Cunnington et al., 2002). Thus the two action modes were not directly comparable. Other studies reported only one experimental (internally timed) condition which was compared with a rest condition (Cunnington et al., 2003, Wiese et al., 2005). Therefore activations could not be unequivocally attributed to the internally timed action itself but might have been part of action generation as a whole.

The problem of confounding factors was especially pertinent in this kind of research, because internally and externally guided actions differed in the sensorimotor context in which they took place. A major challenge for the investigation of the neural correlates of internally guided actions is thus, to develop a paradigm in which externally and internally controlled actions differ only in the action mode.

Recently Waszak et al. (2005) conceived a paradigm in which the two modes of action were directly comparable. They studied the electrophysiological signatures of internally and externally selected key presses. In their paradigm, subjects performed a temporal bisection task, making left or right key presses at the midpoint between 35 isochronous pacing signals (a sequence of ‘X’s presented to the left or the right of the fixation cross). In the internally selected condition, the subjects' key press determined the location of the subsequent ‘X’ on the screen. In this condition, subjects were instructed to generate a random sequence of left and right ‘X’s. In the externally selected condition, by contrast, the subjects’ key press was prompted by the location of the preceding stimulus. The movements in a given externally selected run were yoked (in a disguised fashion) to the movements produced in the preceding internally selected run. This paradigm enabled Waszak et al. (2005) to compare movement timing and EEG-correlates of internally and externally selected actions, although the sensorimotor context of the actions and the kinematics and dynamics of the actions were identical in the two conditions. In order to illuminate the neural correlates of internally selected actions, the present experiment used the Waszak paradigm in an fMRI study. Waszaks' (2005) EEG study told us a lot about the timing of the underlying electrophysiological processes of internally selected actions (for details, see Waszak et al., 2005). However, due to the poor spatial resolution of EEG, it could not tell us for sure where the differences in the neural correlates between the two action modes are manifested in the brain. Because we were mainly interested in the yet unsolved question as to which role the preSMA and the RCZ play in internally selected actions, we expected that combining the advantages of Waszak et al.'s paradigm described above with fMRI would help us to shed some light on answering exactly this question.

Section snippets

Subjects

Sixteen healthy subjects (eight males, eight females) with a mean age of 26.33 years (SD ± 2.92) with normal or corrected to normal vision participated in the study. All subjects were right-handed as indicated by scores on the Edinburgh Handedness Inventory (Oldfield, 1971) with a mean laterality quotient higher than 80. Subjects gave written informed consent to the study. All subjects had extensive experience with participating in fMRI studies and had no history of psychiatric, major medical, or

Behavioral data

T-tests against the bisection point revealed that action times differed in both conditions significantly from 600 ms (internally selected: t(14) =  3.025, p < 0.009; externally selected: t(14) =  5.440, p < 0.000). Furthermore, action times in the internally and externally selected condition differed significantly in the expected direction (MEAN: 569 ms vs. 501 ms; SE: 39.59 ms vs. 70.60 ms), t(14) = 4.238, p < 0.001. Mean asynchronies were smaller for the internally selected (− 31 ms) than for the

Discussion

The aim of the current fMRI study was to disentangle the role of the preSMA and the RCZ in internally selected actions without confounding motor and perceptual differences. We employed the paradigm developed by Waszak et al. (2005) in which internally and externally selected actions did not differ as concerns the timing, the sensorimotor context, and the kinematics of the movements. In the direct comparison of internally vs. externally selected actions, a widespread cortical network was found

Acknowledgments

We thank Ruth Schmitt for carrying out the behavioral pretesting of the experiment, Bettina Johst for programming the experiment, Jane Neumann, and Jöran Lepsien for help with fMRI-statistics.

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