Elsevier

NeuroImage

Volume 34, Issue 1, 1 January 2007, Pages 332-341
NeuroImage

An fMRI approach to particularize the frontoparietal network for visuomotor action monitoring: Detection of incongruence between test subjects’ actions and resulting perceptions

https://doi.org/10.1016/j.neuroimage.2006.08.027Get rights and content

Abstract

Contemporary theories of motor control assume that motor actions underlie a supervisory control system which utilizes reafferent sensory feedbacks of actions for comparison with the original motor programs. The functional network of visuomotor action monitoring is considered to include inferior parietal, lateral and medial prefrontal cortices. To study both sustained monitoring for visuomotor incongruence and the actual detection of incongruence, we used a hybrid fMRI epoch-/event-related design. The basic experimental task was a continuous motor task, comprising a simple racing game. Within certain blocks of this task, incongruence was artificially generated by intermittent takeover of control over the car by the computer. Fifteen male subjects were instructed to monitor for incongruence between their own and the observed actions in order to abstain from their own action whenever the computer took over control.

As a result of both sustained monitoring and actual detection of visuomotor incongruence, the rostral inferior parietal lobule displayed a BOLD signal increase. In contrast, the prefrontal cortex (PFC) exhibited two different activation patterns. Dorsolateral (BA 9/46) and medial/cingulate (BA 8, BA 32) areas of the PFC displayed a greater increase of activation in sustained monitoring, while ventrolateral PFC showed greater event-related activation for the actual detection of visuomotor incongruence.

Our results suggest that the rostral inferior parietal lobule is specifically involved in the reafferent comparison of the test subjects’ own actions and visually perceived actions. Different activation patterns of the PFC may reflect different frontoparietal networks for sustained action monitoring and actual detection of reafferent incongruence.

Introduction

Contemporary theories of motor control assume that motor actions underlie a supervisory control system which utilizes reafferent sensory feedbacks of actual movement consequences for comparison with the original motor programs (Wolpert, 1997, Prinz, 1997). This reafferent control system is considered to be involved in various functions like motor guidance, sensory gating and the generation of awareness about an individual’s own actions.

In addition, the reafferent monitoring system is capable of automatic adjustment to changes of the target location or feedback distortions during movement execution. Within certain spatial and temporal limits, the reafferent adjustment is automatically performed without subjective awareness of the corrections (Fourneret and Jeannerod, 1998). In fact, awareness of the actual state of the motor system rarely emerges as long as the originally intended objectives of actions are achieved.

For sensory gating, a “feed-forward” system of action monitoring is hypothesized to generate predictive models about perceptual consequences of motor plans (Wolpert, 1997, Frith et al., 2000). Insufficient predictive sensory gating and reduced awareness of differences between self-intended and external actions in schizophrenic patients (Blakemore et al., 2000, Franck et al., 2001) suggest that disturbed representation of own motor plans might be fundamental regarding certain psychotic symptoms such as hallucinations and particularly delusions of control (Spence et al., 1997, Frith et al., 2000).

In addition, motor control implies a continuous demand to differentiate between consciously executed movement programs and externally triggered automated movement patterns. The external triggering of automated movements – for example, grabbing a cup or a piece of fruit located in a hand’s spatial field of action – is normally suppressed. This suppression can, however, be invalidated by circumscribed cerebral lesions, such as an infarction of the right medial prefrontal cortex (Giovannetti et al., 2005). The affected subject is aware of a limb, most frequently the left hand, acting on its own accord. It accidentally grabs all objects located in its spatial field of action independently of the subject’s intentions. The phenomenon is usually counted among the symptoms of the “alien hand” syndrome (Goldberg et al., 1981). The occurrence of “anarchic” actions suggests that the link between intentions (i.e., in this context: targets of motor action) and the perception of actions has to be continuously established by action monitoring.

The differential patterns of lesions underlying the distinct symptoms of the alien hand syndrome can be applied to outline the functional anatomy of the already hypothesized feed-forward system of motor control (Wolpert, 1997). Predominantly efferent motor symptoms like the anarchic hand are associated with lesions of medial frontal supplementary motor cortices (Giovannetti et al., 2005) as well as lesions of frontal interhemispheric connections in the anterior corpus callosum. In contrast, lesions of parietal and posterior callosal tissue frequently cause an impaired representation of the patients’ limbs and movements (Frith et al., 2000). Thus, without simultaneous visual perception of its movements, affected subjects may be unable to recognize a hand as being their own.

These observations are in line with recent functional neuroimaging studies. They suggest that certain parts of the medial prefrontal cortex, i.e., the pre-SMA, the anterior cingulate and the medial frontal gyrus, are involved in both analysis and executive control of movements, especially in probabilistic contexts (Volz et al., 2003, Ridderinkhof et al., 2004). As a complement to these potential frontal functions, the parietal cortex is considered to represent visuomotor transformations (Milner and Goodale, 1995). The inferior parietal lobule is particularly activated in reafferent visuomotor processing (Vaillancourt et al., 2006), especially due to the occurrence of reafferent incongruences (Balslev et al., 2006). In monkeys, specific coding for goals of action sequences (i.e., intentions) has been demonstrated in inferior parietal neurons (Fogassi et al., 2005). According to the anatomical connection between the parietal and mid-lateral prefrontal cortex, Petrides (2005) suggested involvement of the mid-dorsolateral prefrontal cortex (PFC) due to monitoring of expected acts and the mid-ventrolateral PFC due to decisions regarding actions.

Here we present a hybrid fMRI epoch-/event-related study of visuomotor action monitoring. Our approach was to render brain areas involved in sustained reafferent monitoring and transient detection of incongruence between the subjects’ own and perceived actions during a simple, continuous motor task. The experimental design resembled blocks of a simple racing video game, where a car had to be kept on a racing track by changing the direction of its movements to the left or the right whenever it reached the boundaries of the track. In the experimental condition, incongruence was artificially generated by intermittent takeover of control by the computer acting as an autopilot. Subjects were instructed to abstain from their own actions as soon as the computer took over control, i.e., as soon as they recognized incongruence between their own and the observed actions, i.e., changes in the car’s direction.

Based on the observations of other authors, we expected inferior posterior parietal, mid-lateral and medial frontal cortices, including the cingulate gyrus, to display significant activation, i.e., an increase in blood oxygenation level-dependent (BOLD) signals during monitoring and detection of incongruence between the subjects’ own and perceived actions. We further expected this hypothesized frontoparietal network to display different local activation patterns for monitoring and actual detection of visuomotor incongruence.

Section snippets

Subjects

Inclusion was restricted to male subjects of similar age to control the influence of gender and age on the acquisition of perceptual–motor skills (Kennedy and Raz, 2005) and to rule out effects of blood estrogen level variation on BOLD signal patterns (Dietrich et al., 2001). After initial acquisition of fMRI data from 18 participants, 3 subjects were excluded due to head movements greater than 3 mm during scanning. Finally, fifteen healthy male participants (mean age: 29.49, SD = 3.75 years)

Behavioral performance

The mean time between two motor actions for all subjects in the CC task (n = 15) was 271 ms (SD = 90 ms). In the MC task, the mean interval between two actions was 291 ms (SD = 55 ms). The point of detection of control transfer to the program was defined as the last movement of the subject after the onset of control by the program. The average duration of the detection process was 715 ms (SD = 214 ms), which means that the subjects needed 2.46 actions after the first action of the program to determine

Discussion

In general, accordance with our hypothesis, posterior parietal areas, lateral and medial frontal cortices, including the cingulate gyrus, displayed a differential BOLD signal increase with (not previously hypothesized) significant lateralization to the right hemisphere in both monitoring (MC > CC) and detection of visuomotor incongruence (OI > OC). The prefrontal cortex exhibited two different activation patterns for the monitoring and detection of visuomotor incongruence. Finally, both tasks

Acknowledgments

We thank the Interdisciplinary Center for Clinical Research, University Hospital of the Technical University Aachen, Aachen, Germany for the support of this study.

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